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1
Weldon, S. R., M. R. Strand, and K. M. Oliver. "Phage loss and the breakdown of a defensive symbiosis in aphids." Proceedings of the Royal Society B: Biological Sciences 280, no. 1751 (2013): 20122103. http://dx.doi.org/10.1098/rspb.2012.2103.
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Terrestrial arthropods are often infected with heritable bacterial symbionts, which may themselves be infected by bacteriophages. However, what role, if any, bacteriophages play in the regulation and maintenance of insect–bacteria symbioses is largely unknown. Infection of the aphid Acyrthosiphon pisum by the bacterial symbiont Hamiltonella defensa confers protection against parasitoid wasps, but only when H. defensa is itself infected by the phage A. pisum secondary endosymbiont (APSE). Here, we use a controlled genetic background and correlation-based assays to show that loss of APSE is associated with up to sevenfold increases in the intra-aphid abundance of H. defensa . APSE loss is also associated with severe deleterious effects on aphid fitness: aphids infected with H. defensa lacking APSE have a significantly delayed onset of reproduction, lower weight at adulthood and half as many total offspring as aphids infected with phage-harbouring H. defensa , indicating that phage loss can rapidly lead to the breakdown of the defensive symbiosis. Our results overall indicate that bacteriophages play critical roles in both aphid defence and the maintenance of heritable symbiosis.
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Xu, Shifen, Liyun Jiang, Gexia Qiao, and Jing Chen. "The Bacterial Flora Associated with the Polyphagous Aphid Aphis gossypii Glover (Hemiptera: Aphididae) Is Strongly Affected by Host Plants." Microbial Ecology 79, no. 4 (2019): 971–84. http://dx.doi.org/10.1007/s00248-019-01435-2.
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AbstractAphids live in symbiosis with a variety of bacteria, including the obligate symbiont Buchnera aphidicola and diverse facultative symbionts. The symbiotic associations for one aphid species, especially for polyphagous species, often differ across populations. In the present study, by using high-throughput 16S rRNA sequencing, we surveyed in detail the microbiota in natural populations of the cotton aphid Aphis gossypii in China and assessed differences in bacterial diversity with respect to host plant and geography. The microbial community of A. gossypii was dominated by a few heritable symbionts. Arsenophonus was the most dominant secondary symbiont, and Spiroplasma was detected for the first time. Statistical tests and ordination analyses showed that host plants rather than geography seemed to have shaped the associated symbiont composition. Special symbiont communities inhabited the Cucurbitaceae-feeding populations, which supported the ecological specialization of A. gossypii on cucurbits from the viewpoint of symbiotic bacteria. Correlation analysis suggested antagonistic interactions between Buchnera and coexisting secondary symbionts and more complicated interactions between different secondary symbionts. Our findings lend further support to an important role of the host plant in structuring symbiont communities of polyphagous aphids and will improve our understanding of the interactions among phytophagous insects, symbionts, and environments.
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Gómez-Valero, Laura, Mario Soriano-Navarro, Vicente Pérez-Brocal, et al. "Coexistence of Wolbachia with Buchnera aphidicola and a Secondary Symbiont in the Aphid Cinara cedri." Journal of Bacteriology 186, no. 19 (2004): 6626–33. http://dx.doi.org/10.1128/jb.186.19.6626-6633.2004.
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ABSTRACT Intracellular symbiosis is very common in the insect world. For the aphid Cinara cedri, we have identified by electron microscopy three symbiotic bacteria that can be characterized by their different sizes, morphologies, and electrodensities. PCR amplification and sequencing of the 16S ribosomal DNA (rDNA) genes showed that, in addition to harboring Buchnera aphidicola, the primary endosymbiont of aphids, C. cedri harbors a secondary symbiont (S symbiont) that was previously found to be associated with aphids (PASS, or R type) and an α-proteobacterium that belongs to the Wolbachia genus. Using in situ hybridization with specific bacterial probes designed for symbiont 16S rDNA sequences, we have shown that Wolbachia was represented by only a few minute bacteria surrounding the S symbionts. Moreover, the observed B. aphidicola and the S symbionts had similar sizes and were housed in separate specific bacterial cells, the bacteriocytes. Interestingly, in contrast to the case for all aphids examined thus far, the S symbionts were shown to occupy a similarly sized or even larger bacteriocyte space than B. aphidicola. These findings, along with the facts that C. cedri harbors the B. aphidicola strain with the smallest bacterial genome and that the S symbionts infect all Cinara spp. analyzed so far, suggest the possibility of bacterial replacement in these species.
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Akman Gündüz, E., and A. E. Douglas. "Symbiotic bacteria enable insect to use a nutritionally inadequate diet." Proceedings of the Royal Society B: Biological Sciences 276, no. 1658 (2008): 987–91. http://dx.doi.org/10.1098/rspb.2008.1476.
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Animals generally require a dietary supply of various nutrients (vitamins, essential amino acids, etc.) because their biosynthetic capabilities are limited. The capacity of aphids to use plant phloem sap, with low essential amino acid content, has been attributed to their symbiotic bacteria, Buchnera aphidicola , which can synthesize these nutrients; but this has not been demonstrated empirically. We demonstrate here that phloem sap obtained from the severed stylets of pea aphids Acyrthosiphon pisum feeding on Vicia faba plants generally provided inadequate amounts of at least one essential amino acid to support aphid growth. Complementary analyses using aphids reared on chemically defined diets with each amino acid individually omitted revealed that the capacity of the symbiotic bacterium B. aphidicola to synthesize essential amino acids exceeded the dietary deficit of all phloem amino acids except methionine. It is proposed that this shortfall of methionine was met by aphid usage of the non-protein amino acid 5-methylmethionine in the phloem sap. This study provides the first quantitative demonstration that bacterial symbiosis can meet the nutritional demand of plant-reared aphids. It shows how symbiosis with micro-organisms has enabled this group of animals to escape from the constraint of requiring a balanced dietary supply of amino acids.
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Shigenobu, Shuji, and David L. Stern. "Aphids evolved novel secreted proteins for symbiosis with bacterial endosymbiont." Proceedings of the Royal Society B: Biological Sciences 280, no. 1750 (2013): 20121952. http://dx.doi.org/10.1098/rspb.2012.1952.
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Aphids evolved novel cells, called bacteriocytes, that differentiate specifically to harbour the obligatory mutualistic endosymbiotic bacteria Buchnera aphidicola . The genome of the host aphid Acyrthosiphon pisum contains many orphan genes that display no similarity with genes found in other sequenced organisms, prompting us to hypothesize that some of these orphan genes are related to lineage-specific traits, such as symbiosis. We conducted deep sequencing of bacteriocytes mRNA followed by whole mount in situ hybridizations of over-represented transcripts encoding aphid-specific orphan proteins. We identified a novel class of genes that encode small proteins with signal peptides, which are often cysteine-rich, that are over-represented in bacteriocytes. These genes are first expressed at a developmental time point coincident with the incorporation of symbionts strictly in the cells that contribute to the bacteriocyte and this bacteriocyte-specific expression is maintained throughout the aphid's life. The expression pattern suggests that recently evolved secretion proteins act within bacteriocytes, perhaps to mediate the symbiosis with beneficial bacterial partners, which is reminiscent of the evolution of novel cysteine-rich secreted proteins of leguminous plants that regulate nitrogen-fixing endosymbionts.
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Chong, Rebecca A., and Nancy A. Moran. "Intraspecific genetic variation in hosts affects regulation of obligate heritable symbionts." Proceedings of the National Academy of Sciences 113, no. 46 (2016): 13114–19. http://dx.doi.org/10.1073/pnas.1610749113.
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Symbiotic relationships promote biological diversification by unlocking new ecological niches. Over evolutionary time, hosts and symbionts often enter intimate and permanent relationships, which must be maintained and regulated for both lineages to persist. Many insect species harbor obligate, heritable symbiotic bacteria that provision essential nutrients and enable hosts to exploit niches that would otherwise be unavailable. Hosts must regulate symbiont population sizes, but optimal regulation may be affected by the need to respond to the ongoing evolution of symbionts, which experience high levels of genetic drift and potential selection for selfish traits. We address the extent of intraspecific variation in the regulation of a mutually obligate symbiosis, between the pea aphid (Acyrthosiphon pisum) and its maternally transmitted symbiont, Buchnera aphidicola. Using experimental crosses to identify effects of host genotypes, we measured symbiont titer, as the ratio of genomic copy numbers of symbiont and host, as well as developmental time and fecundity of hosts. We find a large (>10-fold) range in symbiont titer among genetically distinct aphid lines harboring the same Buchnera haplotype. Aphid clones also vary in fitness, measured as developmental time and fecundity, and genetically based variation in titer is correlated with host fitness, with higher titers corresponding to lower reproductive rates of hosts. Our work shows that obligate symbiosis is not static but instead is subject to short-term evolutionary dynamics, potentially reflecting coevolutionary interactions between host and symbiont.
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Burke, Gaelen R., Benjamin B. Normark, Colin Favret, and Nancy A. Moran. "Evolution and Diversity of Facultative Symbionts from the Aphid Subfamily Lachninae." Applied and Environmental Microbiology 75, no. 16 (2009): 5328–35. http://dx.doi.org/10.1128/aem.00717-09.
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ABSTRACT Many aphids harbor a variety of endosymbiotic bacteria. The functions of these symbionts can range from an obligate nutritional role to a facultative role in protecting their hosts against environmental stresses. One such symbiont is “Candidatus Serratia symbiotica,” which is involved in defense against heat and potentially also in aphid nutrition. Lachnid aphids have been the focus of several recent studies investigating the transition of this symbiont from a facultative symbiont to an obligate symbiont. In a phylogenetic analysis of Serratia symbionts from 51 lachnid hosts, we found that diversity in symbiont morphology, distribution, and function is due to multiple independent origins of symbiosis from ancestors belonging to Serratia and possibly also to evolution within distinct symbiont clades. Our results do not support cocladogenesis of “Ca. Serratia symbiotica” with Cinara subgenus Cinara species and weigh against an obligate nutritional role. Finally, we show that species belonging to the subfamily Lachninae have a high incidence of facultative symbiont infection.
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Macdonald, Sandy J., Gavin H. Thomas, and Angela E. Douglas. "Waste not, want not: Nitrogen recycling by metabolic pathways shared between an animal and its symbiotic bacteria." Biochemist 35, no. 4 (2013): 20–24. http://dx.doi.org/10.1042/bio03504020.
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A combined computational and experimental analysis of metabolism in the symbiosis between the pea aphid and its obligate endosymbiont Buchnera aphidicola redefines existing notions of symbiotic nitrogen recycling. As a consequence of metabolic pathways shared between the partners, the insect recycles waste ammonia into essential amino acids (EAAs) that are lacking in its diet of sugar-rich but nitrogen-poor plant phloem sap.
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Pérez-Brocal, Vicente, Rosario Gil, Andrés Moya, and Amparo Latorre. "New Insights on the Evolutionary History of Aphids and Their Primary Endosymbiont Buchnera aphidicola." International Journal of Evolutionary Biology 2011 (February 16, 2011): 1–9. http://dx.doi.org/10.4061/2011/250154.
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Since the establishment of the symbiosis between the ancestor of modern aphids and their primary endosymbiont, Buchnera aphidicola, insects and bacteria have coevolved. Due to this parallel evolution, the analysis of bacterial genomic features constitutes a useful tool to understand their evolutionary history. Here we report, based on data from B. aphidicola, the molecular evolutionary analysis, the phylogenetic relationships among lineages and a comparison of sequence evolutionary rates of symbionts of four aphid species from three subfamilies. Our results support previous hypotheses of divergence of B. aphidicola and their host lineages during the early Cretaceous and indicate a closer relationship between subfamilies Eriosomatinae and Lachninae than with the Aphidinae. They also reveal a general evolutionary pattern among strains at the functional level. We also point out the effect of lifecycle and generation time as a possible explanation for the accelerated rate in B. aphidicola from the Lachninae.
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Shang, Feng, Jinzhi Niu, Bi-Yue Ding, and Jin-Jun Wang. "Comparative Insight into the Bacterial Communities in Alate and Apterous Morphs of Brown Citrus Aphid (Hemiptera: Aphididae)." Journal of Economic Entomology 113, no. 3 (2020): 1436–44. http://dx.doi.org/10.1093/jee/toaa016.
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Abstract Wing polyphenism (alate and apterous morphs) in aphids is a trade-off between dispersal and reproduction. How bacterial communities are associated with wing polyphenism in aphids is still not clearly understood. This study used 16S rRNA sequencing to examine the differences in diversity of the bacterial community between alate and apterous morphs in Aphis citricidus, the main vector of the Citrus tristeza virus. Eighty-one operational taxonomic units (OTUs) belonging to 37 orders, 34 classes, and 13 phyla were identified from all samples. Among these OTUs, Wolbachia (79.17%), Buchnera (17.64%), and Pseudomonas (2.99%) were the dominant bacterial genera. The diversity of symbionts varied between the two morphs; apterous morphs had more bacterial diversity (69 OTUs belonging to 45 families, 21 classes, and 12 phyla) than alate morphs (45 OTUs belonging to 36 families, 15 classes, and 10 phyla). In addition, the abundance of five OTUs was significantly different between two morphs. Among these OTUs, two Pseudomonas species (Pseudomonas_brenneri [OTU21] and unclassified_Pseudomonas [OTU13]) represented a high proportion (3.93% and 2.06%) in alate morphs but were present in low abundance (0.006% and 0.002%) in apterous morphs. RT-qPCR showed consistent results with high-throughput DNA sequencing. The preliminary survey showed the difference in composition and frequency of bacteria between alate and apterous morphs. Thus, the results contribute to anew insight of microorganisms that may be involved in wing dimorphism and helpful for controlling the dispersal of this pest through artificial elimination or reinfection of bacterial symbionts or targeting symbiosis-related host genes by RNA interference in future.
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Wilkinson, T. L., D. Adams, L. B. Minto, and A. E. Douglas. "The impact of host plant on the abundance and function of symbiotic bacteria in an aphid." Journal of Experimental Biology 204, no. 17 (2001): 3027–38. http://dx.doi.org/10.1242/jeb.204.17.3027.
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SUMMARY The black-bean aphid Aphis fabae bears populations of coccoid symbiotic bacteria Buchnera spp. at 2.0–3.2×107cellsmg−1aphidmass and rod-shaped secondary symbionts of uncertain taxonomic affiliation at 0.1–0.6×107cellsmg−1aphidmass. Buchnera provides essential amino acids, supplementing the poor supply in the aphid diet of plant phloem sap. Comparison of the performance of A. fabae containing and experimentally deprived of their bacteria showed that the bacteria caused increased larval mass of aphids reared on Chenopodium album and Papaver dubium plants, but not when reared on Lamium purpureum. In the aphids reared on L. purpureum, the density of the bacteria, especially the secondary symbionts, was significantly elevated, and bacterial-mediated production of the essential amino acid threonine was reduced, even though the essential amino acid content of phloem exudates from L. purpureum had a low threonine content. It is proposed that the shortfall in threonine, possibly compounded by the high density of secondary symbionts, may contribute to the poor performance of the aphids on L. purpureum. This study offers the first evidence to suggest plant-mediated interference with the nutritional function of symbiotic bacteria in any phytophagous insect.
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Haynes, S., A. C. Darby, T. J. Daniell, et al. "Diversity of Bacteria Associated with Natural Aphid Populations." Applied and Environmental Microbiology 69, no. 12 (2003): 7216–23. http://dx.doi.org/10.1128/aem.69.12.7216-7223.2003.
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ABSTRACT The bacterial communities of aphids were investigated by terminal restriction fragment length polymorphism and denaturing gradient gel electrophoresis analysis of 16S rRNA gene fragments generated by PCR with general eubacterial primers. By both methods, theγ -proteobacterium Buchnera was detected in laboratory cultures of six parthenogenetic lines of the pea aphid Acyrthosiphon pisum and one line of the black bean aphid Aphis fabae, and one or more of four previously described bacterial taxa were also detected in all aphid lines except one of A. pisum. These latter bacteria, collectively known as secondary symbionts or accessory bacteria, comprised three taxa of γ-proteobacteria (R-type [PASS], T-type [PABS], and U-type [PAUS]) and a rickettsia (S-type [PAR]). Complementary analysis of aphids from natural populations of four aphid species (A. pisum [n= 74], Amphorophora rubi [n= 109], Aphis sarothamni [n= 42], and Microlophium carnosum [n= 101]) from a single geographical location revealed Buchnera and up to three taxa of accessory bacteria, but no other bacterial taxa, in each aphid. The prevalence of accessory bacterial taxa varied significantly among aphid species but not with the sampling month (between June and August 2000). These results indicate that the accessory bacterial taxa are distributed across multiple aphid species, although with variable prevalence, and that laboratory culture does not generally result in a shift in the bacterial community in aphids. Both the transmission patterns of the accessory bacteria between individual aphids and their impact on aphid fitness are suggested to influence the prevalence of accessory bacterial taxa in natural aphid populations.
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Jones, Ryan T., Alberto Bressan, April M. Greenwell, and Noah Fierer. "Bacterial Communities of Two Parthenogenetic Aphid Species Cocolonizing Two Host Plants across the Hawaiian Islands." Applied and Environmental Microbiology 77, no. 23 (2011): 8345–49. http://dx.doi.org/10.1128/aem.05974-11.
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ABSTRACTAphids (Hemiptera: Aphididae) have been the focus of several studies with respect to their interactions with inherited symbionts, but bacterial communities of most aphid species are still poorly characterized. In this research, we used bar-coded pyrosequencing to characterize bacterial communities in aphids. Specifically, we examined the diversity of bacteria in two obligately parthenogenetic aphid species (the melon aphid,Aphis gossypii, and the cardamom aphid,Pentalonia caladii) cocolonizing two plant species (taro,Colocasia esculenta, and ginger,Alpinia purpurata) across four Hawaiian Islands (Hawaii, Kauai, Maui, and Oahu). Results from this study revealed that heritable symbionts dominated the bacterial communities for both aphid species. The bacterial communities differed significantly between the two species, andA. gossypiiharbored a more diverse bacterial community thanP. caladii. The bacterial communities also differed across aphid populations sampled from the different islands; however, communities did not differ between aphids collected from the two host plants.
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McLean, Ailsa H. C., and H. Charles J. Godfray. "Evidence for specificity in symbiont-conferred protection against parasitoids." Proceedings of the Royal Society B: Biological Sciences 282, no. 1811 (2015): 20150977. http://dx.doi.org/10.1098/rspb.2015.0977.
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Many insects harbour facultative symbiotic bacteria, some of which have been shown to provide resistance against natural enemies. One of the best-known protective symbionts is Hamiltonella defensa , which in pea aphid ( Acyrthosiphon pisum ) confers resistance against attack by parasitoid wasps in the genus Aphidius (Braconidae). We asked (i) whether this symbiont also confers protection against a phylogenetically distant group of parasitoids (Aphelinidae) and (ii) whether there are consistent differences in the effects of bacteria found in pea aphid biotypes adapted to different host plants. We found that some H. defensa strains do provide protection against an aphelinid parasitoid Aphelinus abdominalis. Hamiltonella defensa from the Lotus biotype provided high resistance to A. abdominalis and moderate to low resistance to Aphidius ervi , while the reverse was seen from Medicago biotype isolates. Aphids from Ononis showed no evidence of symbiont-mediated protection against either wasp species and were relatively vulnerable to both. Our results may reflect the different selection pressures exerted by the parasitoid community on aphids feeding on different host plants, and could help explain the maintenance of genetic diversity in bacterial symbionts.
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Romanov, D. A., I. A. Zakharov, and E. V. Shaikevich. "Wolbachia, Spiroplasma, and Rickettsia symbiotic bacteria in aphids (Aphidoidea)." Vavilov Journal of Genetics and Breeding 24, no. 6 (2020): 673–82. http://dx.doi.org/10.18699/vj20.661.
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Aphids are a diverse family of crop pests. Aphids formed a complex relationship with intracellular bacteria. Depending on the region of study, the species composition of both aphids and their facultative endosymbionts varies. The aim of the work was to determine the occurrence and genetic diversity of Wolbachia, Spiroplasma and Rickettsia symbionts in aphids collected in 2018–2019 in Moscow. For these purposes, 578 aphids from 32 collection sites were tested by PCR using specific primers. At least 21 species of aphids from 14 genera and four families were identified by barcoding method, of which 11 species were infected with endosymbionts. Rickettsia was found in six species, Wolbachia in two species, Spiroplasma in one species. The presence of Rickettsia in Impatientinum asiaticum, Myzus cerasi, Hyalopterus pruni, Eucallipterus tiliae, Chaitophorus tremulae and Wolbachia in Aphis pomi and C. tremulae has been described for the first time. A double infection with Rickettsia and Spiroplasma was detected in a half of pea aphid (Acyrthosiphon pisum) individuals. For the first time was found that six species of aphids are infected with Rickettsia that are genetically different from previously known. It was first discovered that A. pomi is infected with two Wolbachia strains, one of which belongs to supergroup B and is genetically close to Wolbachia from C. tremulae. The second Wolbachia strain from A. pomi belongs to the supergroup M, recently described in aphid species. Spiroplasma, which we observed in A. pisum, is genetically close to male killing Spiroplasma from aphids, ladybirds and moths. Both maternal inheritance and horizontal transmission are the pathways for the distribution of facultative endosymbiotic bacteria in aphids.
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Salcedo-Porras, Nicolas, Claudia Umaña-Diaz, Ricardo de Oliveira Barbosa Bitencourt, and Carl Lowenberger. "The Role of Bacterial Symbionts in Triatomines: An Evolutionary Perspective." Microorganisms 8, no. 9 (2020): 1438. http://dx.doi.org/10.3390/microorganisms8091438.
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Insects have established mutualistic symbiotic interactions with microorganisms that are beneficial to both host and symbiont. Many insects have exploited these symbioses to diversify and expand their ecological ranges. In the Hemiptera (i.e., aphids, cicadas, and true bugs), symbioses have established and evolved with obligatory essential microorganisms (primary symbionts) and with facultative beneficial symbionts (secondary symbionts). Primary symbionts are usually intracellular microorganisms found in insects with specialized diets such as obligate hematophagy or phytophagy. Most Heteroptera (true bugs), however, have gastrointestinal (GI) tract extracellular symbionts with functions analogous to primary endosymbionts. The triatomines, are vectors of the human parasite, Trypanosoma cruzi. A description of their small GI tract microbiota richness was based on a few culturable microorganisms first described almost a century ago. A growing literature describes more complex interactions between triatomines and bacteria with properties characteristic of both primary and secondary symbionts. In this review, we provide an evolutionary perspective of beneficial symbioses in the Hemiptera, illustrating the context that may drive the evolution of symbioses in triatomines. We highlight the diversity of the triatomine microbiota, bacterial taxa with potential to be beneficial symbionts, the unique characteristics of triatomine-bacteria symbioses, and the interactions among trypanosomes, microbiota, and triatomines.
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Perkovsky, Evgeny, and Piotr Wegierek. "Aphid–Buchnera–Ant symbiosis; or why are aphids rare in the tropics and very rare further south?" Earth and Environmental Science Transactions of the Royal Society of Edinburgh 107, no. 2-3 (2016): 297–310. http://dx.doi.org/10.1017/s1755691017000147.
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ABSTRACTAt least since the Cretaceous Terrestrial Revolution, the geographical distribution of aphids, particularly in the Northern Hemisphere, has been strongly affected by the low thermal tolerance of their obligatory bacterial symbiont, Buchnera aphidicola, which was why the aphids switched to obligate parthenogenesis in low latitudes. Hormaphidids and greenideids penetrated into the tropics only after the Oligocene strengthening of climate seasonality, and specialisations of the tropical representatives of these families did not allow them to spread further south (in the case of cerataphidines), or only allowed in few cases (in the case of greenideids).Aphids suffered from the Mesozoic–Cenozoic boundary extinction event much more strongly than other insects. The extinction was roughly coincidental with the establishment of the tight symbiosis of aphids with formicine and dolichoderine ants, which was accompanied by the flourishing of all three groups.In the Cretaceous, all of the representatives of extant and subfamilies occupied positions that were subordinate to Armaniinae and Sphecomyrminae. Prior to large ant colonies evolving their efficient ant–aphid mutualism, the aphids remained unprotected before the growing ant predation. The origin of the aphid trophobiosis with large colonies of Formicinae and Dolichoderinae has resulted in the steep decline of aphids left beyond that ant–aphid symbiotic network. By at least the basal Eocene (unlike the Late Cretaceous), ant proportions in the entomofauna increased sharply, and evident dominants emerged. Even now, aphid milkers from small colonies (hundreds of specimens) never protect their symbionts, and homopteran-tending ants are more likely to be dominant, with large colonies of 104–105 workers.The mutualistic ant–aphid system failed to cross the tropical belt during the Cenozoic because of Buchnera's low heat tolerance. As a result, the native southern temperate aphid fauna consists now of seven genera only, five of which are Late Cretaceous relicts. Some of them had relatives in Late Cretaceous amber of the Northern Hemisphere.
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Cayetano, Luis, Lukas Rothacher, Jean-Christophe Simon, and Christoph Vorburger. "Cheaper is not always worse: strongly protective isolates of a defensive symbiont are less costly to the aphid host." Proceedings of the Royal Society B: Biological Sciences 282, no. 1799 (2015): 20142333. http://dx.doi.org/10.1098/rspb.2014.2333.
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Defences against parasites are typically associated with costs to the host that contribute to the maintenance of variation in resistance. This also applies to the defence provided by the facultative bacterial endosymbiont Hamiltonella defensa, which protects its aphid hosts against parasitoid wasps while imposing life-history costs. To investigate the cost–benefit relationship within protected hosts, we introduced multiple isolates of H. defensa to the same genetic backgrounds of black bean aphids, Aphis fabae , and we quantified the protection against their parasitoid Lysiphlebus fabarum as well as the costs to the host (reduced lifespan and reproduction) in the absence of parasitoids. Surprisingly, we observed the opposite of a trade-off. Strongly protective isolates of H. defensa reduced lifespan and lifetime reproduction of unparasitized aphids to a lesser extent than weakly protective isolates. This finding has important implications for the evolution of defensive symbiosis and highlights the need for a better understanding of how strain variation in protective symbionts is maintained.
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Renoz, François, Antoine Champagne, Hervé Degand, et al. "Toward a better understanding of the mechanisms of symbiosis: a comprehensive proteome map of a nascent insect symbiont." PeerJ 5 (May 9, 2017): e3291. http://dx.doi.org/10.7717/peerj.3291.
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Symbiotic bacteria are common in insects and can affect various aspects of their hosts’ biology. Although the effects of insect symbionts have been clarified for various insect symbiosis models, due to the difficulty of cultivating themin vitro, there is still limited knowledge available on the molecular features that drive symbiosis.Serratia symbioticais one of the most common symbionts found in aphids. The recent findings of free-living strains that are considered as nascent partners of aphids provide the opportunity to examine the molecular mechanisms that a symbiont can deploy at the early stages of the symbiosis (i.e., symbiotic factors). In this work, a proteomic approach was used to establish a comprehensive proteome map of the free-livingS. symbioticastrain CWBI-2.3T. Most of the 720 proteins identified are related to housekeeping or primary metabolism. Of these, 76 were identified as candidate proteins possibly promoting host colonization. Our results provide strong evidence thatS. symbioticaCWBI-2.3Tis well-armed for invading insect host tissues, and suggest that certain molecular features usually harbored by pathogenic bacteria are no longer present. This comprehensive proteome map provides a series of candidate genes for further studies to understand the molecular cross-talk between insects and symbiotic bacteria.
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Douglas, A. E., L. B. Minto, and T. L. Wilkinson. "Quantifying nutrient production by the microbial symbionts in an aphid." Journal of Experimental Biology 204, no. 2 (2001): 349–58. http://dx.doi.org/10.1242/jeb.204.2.349.
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The symbiotic bacteria Buchnera sp. provide aphids with essential amino acids, nutrients in short supply in the aphid diet of plant phloem sap. The contribution of Buchnera-derived amino acids to net protein growth of the aphid Aphis fabae was quantified from the protein growth of aphids reared on chemically defined diets lacking individual amino acids. The amino acid production rates varied among the nine essential amino acids over the range 8–156 pmol microg(−1)protein day(−1) (for tryptophan and leucine, respectively), equivalent to 0.02-0.33 fmol Buchnera(−1)day(−1). In a complementary metabolic analysis, the aphids incorporated radioactivity from dietary [(14)C]glutamic acid into the essential amino acids isoleucine, lysine and threonine. Incorporation into isoleucine was significantly elevated by the omission of dietary isoleucine, indicating that dietary supply may affect the biosynthetic rates of certain amino acids by Buchnera. Aphids experimentally deprived of Buchnera did not synthesize essential amino acids from dietary glutamic acid. The mortality of aposymbionts was high over 7 days on the phenylalanine-free diet, and their assimilation of dietary leucine was depressed on the complete diet, suggesting that both the absence of bacteria-derived amino acids and the low rates of assimilation of certain dietary amino acids may contribute to the poor growth of these insects.
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McLean, A. H. C., M. van Asch, J. Ferrari, and H. C. J. Godfray. "Effects of bacterial secondary symbionts on host plant use in pea aphids." Proceedings of the Royal Society B: Biological Sciences 278, no. 1706 (2010): 760–66. http://dx.doi.org/10.1098/rspb.2010.1654.
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Aphids possess several facultative bacterial symbionts that have important effects on their hosts' biology. These have been most closely studied in the pea aphid ( Acyrthosiphon pisum ), a species that feeds on multiple host plants. Whether secondary symbionts influence host plant utilization is unclear. We report the fitness consequences of introducing different strains of the symbiont Hamiltonella defensa into three aphid clones collected on Lathyrus pratensis that naturally lack symbionts, and of removing symbionts from 20 natural aphid–bacterial associations. Infection decreased fitness on Lathyrus but not on Vicia faba , a plant on which most pea aphids readily feed. This may explain the unusually low prevalence of symbionts in aphids collected on Lathyrus . There was no effect of presence of symbiont on performance of the aphids on the host plants of the clones from which the H. defensa strains were isolated. Removing the symbiont from natural aphid–bacterial associations led to an average approximate 20 per cent reduction in fecundity, both on the natural host plant and on V. faba , suggesting general rather than plant-species-specific effects of the symbiont. Throughout, we find significant genetic variation among aphid clones. The results provide no evidence that secondary symbionts have a major direct role in facilitating aphid utilization of particular host plant species.
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Gehrer, Lukas, and Christoph Vorburger. "Parasitoids as vectors of facultative bacterial endosymbionts in aphids." Biology Letters 8, no. 4 (2012): 613–15. http://dx.doi.org/10.1098/rsbl.2012.0144.
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Heritable bacterial endosymbionts play an important role in aphid ecology. Sequence-based evidence suggests that facultative symbionts such as Hamiltonella defensa or Regiella insecticola also undergo horizontal transmission. Other than through male-to-female transfer during the sexual generation in autumn, the routes by which this occurs remain largely unknown. Here, we tested if parasitoids or ectoparasitic mites can act as vectors for horizontal transfer of facultative symbionts. Using symbiont-specific primers for diagnostic PCR, we demonstrate for the first time, to our knowledge, that parasitoids can indeed transfer H. defensa and R. insecticola by sequentially stabbing infected and uninfected individuals of their host, Aphis fabae , establishing new, heritable infections. Thus, a natural route of horizontal symbiont transmission is also available during the many clonal generations of the aphid life cycle. No transmissions by ectoparasitic mites were observed, nor did parasitoids that emerged from symbiont-infected aphids transfer any symbionts in our experiments.
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Holt, Jocelyn R., Alex Styer, Jennifer A. White, et al. "Differences in Microbiota Between Two Multilocus Lineages of the Sugarcane Aphid (Melanaphis sacchari) in the Continental United States." Annals of the Entomological Society of America 113, no. 4 (2020): 257–65. http://dx.doi.org/10.1093/aesa/saaa003.
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Abstract The sugarcane aphid (SCA), Melanaphis Sacchari (Zehntner) (Hemiptera: Aphididae), has been considered an invasive pest of sugarcane in the continental United States since 1977. Then, in 2013, SCA abruptly became a serious pest of U.S. sorghum and is now a sorghum pest in 22 states across the continental United States. Changes in insect-associated microbial community composition are known to influence host-plant range in aphids. In this study, we assessed whether changes in microbiota composition may explain the SCA outbreak in U.S. sorghum. We characterized the SCA bacterial microbiota on sugarcane and grain sorghum in four U.S. states, using a metabarcoding approach. In addition, we used taxon-specific polymerase chain reaction (PCR) primers to screen for bacteria commonly reported in aphid species. As anticipated, all SCA harbored the primary aphid endosymbiont Buchnera aphidicola, an obligate mutualistic bacterial symbiont. Interestingly, none of the secondary symbionts, facultative bacteria typically associated with aphids (e.g., Arsenophonus, Hamiltonella, Regiella) were present in either the metabarcoding data or PCR screens (with the exception of Rickettsiella and Serratia, which were detected by metabarcoding at low abundances <1%). However, our metabarcoding detected bacteria not previously identified in aphids (Arcobacter, Bifidobacterium, Citrobacter). Lastly, we found microbial host-associated differentiation in aphids that seems to correspond to genetically distinct aphid lineages that prefer to feed on grain sorghum (MLL-F) versus sugarcane (MLL-D).
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Manzano-Marı́n, Alejandro, Armelle Coeur d’acier, Anne-Laure Clamens, et al. "Serial horizontal transfer of vitamin-biosynthetic genes enables the establishment of new nutritional symbionts in aphids’ di-symbiotic systems." ISME Journal 14, no. 1 (2019): 259–73. http://dx.doi.org/10.1038/s41396-019-0533-6.
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Abstract Many insects depend on obligate mutualistic bacteria to provide essential nutrients lacking from their diet. Most aphids, whose diet consists of phloem, rely on the bacterial endosymbiont Buchnera aphidicola to supply essential amino acids and B vitamins. However, in some aphid species, provision of these nutrients is partitioned between Buchnera and a younger bacterial partner, whose identity varies across aphid lineages. Little is known about the origin and the evolutionary stability of these di-symbiotic systems. It is also unclear whether the novel symbionts merely compensate for losses in Buchnera or carry new nutritional functions. Using whole-genome endosymbiont sequences of nine Cinara aphids that harbour an Erwinia-related symbiont to complement Buchnera, we show that the Erwinia association arose from a single event of symbiont lifestyle shift, from a free-living to an obligate intracellular one. This event resulted in drastic genome reduction, long-term genome stasis, and co-divergence with aphids. Fluorescence in situ hybridisation reveals that Erwinia inhabits its own bacteriocytes near Buchnera’s. Altogether these results depict a scenario for the establishment of Erwinia as an obligate symbiont that mirrors Buchnera’s. Additionally, we found that the Erwinia vitamin-biosynthetic genes not only compensate for Buchnera’s deficiencies, but also provide a new nutritional function; whose genes have been horizontally acquired from a Sodalis-related bacterium. A subset of these genes have been subsequently transferred to a new Hamiltonella co-obligate symbiont in one specific Cinara lineage. These results show that the establishment and dynamics of multi-partner endosymbioses can be mediated by lateral gene transfers between co-ocurring symbionts.
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Darby, A. C., S. M. Chandler, S. C. Welburn, and A. E. Douglas. "Aphid-Symbiotic Bacteria Cultured in Insect Cell Lines." Applied and Environmental Microbiology 71, no. 8 (2005): 4833–39. http://dx.doi.org/10.1128/aem.71.8.4833-4839.2005.
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ABSTRACT The cells and tissues of many aphids contain bacteria known as “secondary symbionts,” which under specific environmental circumstances may be beneficial to the host insect. Such symbiotic bacteria are traditionally described as intractable to cultivation in vitro. Here we show that two types of aphid secondary symbionts, known informally as T type and U type, can be cultured and maintained in three insect cell lines. The identities of the cultured bacteria were confirmed by PCR with sequencing of 16S rRNA gene fragments and fluorescence in situ hybridization. In cell lines infected with bacteria derived from aphids harboring both T type and U type, the U type persisted, while the T type was lost. We suggest that the two bacteria persist in aphids because competition between them is limited by differences in tropism for insect tissues or cell types. The culture of these bacteria in insect cell lines provides a new and unique research opportunity, offering a source of unibacterial material for genomic studies and a model system to investigate the interactions between animal cells and bacteria. We propose the provisional taxon names “Candidatus Consessoris aphidicola” for T type and “Candidatus Adiaceo aphidicola” for U type.
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Zhang, Bo, Sean P. Leonard, Yiyuan Li, and Nancy A. Moran. "Obligate bacterial endosymbionts limit thermal tolerance of insect host species." Proceedings of the National Academy of Sciences 116, no. 49 (2019): 24712–18. http://dx.doi.org/10.1073/pnas.1915307116.
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The thermal tolerance of an organism limits its ecological and geographic ranges and is potentially affected by dependence on temperature-sensitive symbiotic partners. Aphid species vary widely in heat sensitivity, but almost all aphids are dependent on the nutrient-provisioning intracellular bacterium Buchnera, which has evolved with aphids for 100 million years and which has a reduced genome potentially limiting heat tolerance. We addressed whether heat sensitivity of Buchnera underlies variation in thermal tolerance among 5 aphid species. We measured how heat exposure of juvenile aphids affects later survival, maturation time, and fecundity. At one extreme, heat exposure of Aphis gossypii enhanced fecundity and had no effect on the Buchnera titer. In contrast, heat suppressed Buchnera populations in Aphis fabae, which suffered elevated mortality, delayed development and reduced fecundity. Likewise, in Acyrthosiphon kondoi and Acyrthosiphon pisum, heat caused rapid declines in Buchnera numbers, as well as reduced survivorship, development rate, and fecundity. Fecundity following heat exposure is severely decreased by a Buchnera mutation that suppresses the transcriptional response of a gene encoding a small heat shock protein. Similarly, absence of this Buchnera heat shock gene may explain the heat sensitivity of Ap. fabae. Fluorescent in situ hybridization revealed heat-induced deformation and shrinkage of bacteriocytes in heat-sensitive species but not in heat-tolerant species. Sensitive and tolerant species also differed in numbers and transcriptional responses of heat shock genes. These results show that shifts in Buchnera heat sensitivity contribute to host variation in heat tolerance.
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Xu, Ting-Ting, Li-Yun Jiang, Jing Chen, and Ge-Xia Qiao. "Host Plants Influence the Symbiont Diversity of Eriosomatinae (Hemiptera: Aphididae)." Insects 11, no. 4 (2020): 217. http://dx.doi.org/10.3390/insects11040217.
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Eriosomatinae is a particular aphid group with typically heteroecious holocyclic life cycle, exhibiting strong primary host plant specialization and inducing galls on primary host plants. Aphids are frequently associated with bacterial symbionts, which can play fundamental roles in the ecology and evolution of their host aphids. However, the bacterial communities in Eriosomatinae are poorly known. In the present study, using high-throughput sequencing of the bacterial 16S ribosomal RNA gene, we surveyed the bacterial flora of eriosomatines and explored the associations between symbiont diversity and aphid relatedness, aphid host plant and geographical distribution. The microbiota of Eriosomatinae is dominated by the heritable primary endosymbiont Buchnera and several facultative symbionts. The primary endosymbiont Buchnera is expectedly the most abundant symbiont across all species. Six facultative symbionts were identified. Regiella was the most commonly identified facultative symbiont, and multiple infections of facultative symbionts were detected in the majority of the samples. Ordination analyses and statistical tests show that the symbiont community of aphids feeding on plants from the family Ulmaceae were distinguishable from aphids feeding on other host plants. Species in Eriosomatinae feeding on different plants are likely to carry different symbiont compositions. The symbiont distributions seem to be not related to taxonomic distance and geographical distance. Our findings suggest that host plants can affect symbiont maintenance, and will improve our understanding of the interactions between aphids, their symbionts and ecological conditions.
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Russell, Jacob A., and Nancy A. Moran. "Horizontal Transfer of Bacterial Symbionts: Heritability and Fitness Effects in a Novel Aphid Host." Applied and Environmental Microbiology 71, no. 12 (2005): 7987–94. http://dx.doi.org/10.1128/aem.71.12.7987-7994.2005.
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ABSTRACT Members of several bacterial lineages are known only as symbionts of insects and move among hosts through maternal transmission. Such vertical transfer promotes strong fidelity within these associations, favoring the evolution of microbially mediated effects that improve host fitness. However, phylogenetic evidence indicates occasional horizontal transfer among different insect species, suggesting that some microbial symbionts retain a generalized ability to infect multiple hosts. Here we examine the abilities of three vertically transmitted bacteria from the Gammaproteobacteria to infect and spread within a novel host species, the pea aphid, Acyrthosiphon pisum. Using microinjection, we transferred symbionts from three species of natural aphid hosts into a common host background, comparing transmission efficiencies between novel symbionts and those naturally infecting A. pisum. We also examined the fitness effects of two novel symbionts to determine whether they should persist under natural selection acting at the host level. Our results reveal that these heritable bacteria vary in their capacities to utilize A. pisum as a host. One of three novel symbionts failed to undergo efficient maternal transmission in A. pisum, and one of the two efficiently transmitted bacteria depressed aphid growth rates. Although these findings reveal that negative fitness effects and low transmission efficiency can prevent the establishment of a new infection following horizontal transmission, they also indicate that some symbionts can overcome these obstacles, accounting for their widespread distributions across aphids and related insects.
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Dion, Emilie, Sarah Erika Polin, Jean-Christophe Simon, and Yannick Outreman. "Symbiont infection affects aphid defensive behaviours." Biology Letters 7, no. 5 (2011): 743–46. http://dx.doi.org/10.1098/rsbl.2011.0249.
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Aphids harbour both an obligate bacterial symbiont, Buchnera aphidicola , and a wide range of facultative ones. Facultative symbionts can modify morphological, developmental and physiological host traits that favour their spread within aphid populations. We experimentally investigated the idea that symbionts may also modify aphid behavioural traits to enhance their transmission. Aphids exhibit many behavioural defences against enemies. Despite their benefits, these behaviours have some associated costs leading to reduction in aphid reproduction. Some aphid individuals harbour a facultative symbiont Hamiltonella defensa that provides protection against parasitoids. By analysing aphid behaviours in the presence of parasitoids, we showed that aphids infected with H. defensa exhibited reduced aggressiveness and escape reactions compared with uninfected aphids. The aphid and the symbiont have both benefited from these behavioural changes: both partners reduced the fitness decrements associated with the behavioural defences. Such symbiont-induced changes of behavioural defences may have consequences for coevolutionary processes between host organisms and their enemies.
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Fakhour, Samir, François Renoz, Jérôme Ambroise, et al. "Insight into the bacterial communities of the subterranean aphid Anoecia corni." PLOS ONE 16, no. 8 (2021): e0256019. http://dx.doi.org/10.1371/journal.pone.0256019.
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Many insect species are associated with bacterial partners that can significantly influence their evolutionary ecology. Compared to other insect groups, aphids harbor a bacterial microbiota that has the reputation of being poorly diversified, generally limited to the presence of the obligate nutritional symbiont Buchnera aphidicola and some facultative symbionts. In this study, we analyzed the bacterial diversity associated with the dogwood-grass aphid Anoecia corni, an aphid species that spends much of its life cycle in a subterranean environment. Little is known about the bacterial diversity associated with aphids displaying such a lifestyle, and one hypothesis is that close contact with the vast microbial community of the rhizosphere could promote the acquisition of a richer bacterial diversity compared to other aphid species. Using 16S rRNA amplicon Illumina sequencing on specimens collected on wheat roots in Morocco, we identified 10 bacterial operational taxonomic units (OTUs) corresponding to five bacterial genera. In addition to the obligate symbiont Buchnera, we identified the facultative symbionts Serratia symbiotica and Wolbachia in certain aphid colonies. The detection of Wolbachia is unexpected as it is considered rare in aphids. Moreover, its biological significance remains unknown in these insects. Besides, we also detected Arsenophonus and Dactylopiibacterium carminicum. These results suggest that, despite its subterranean lifestyle, A. corni shelter a bacterial diversity mainly limited to bacterial endosymbionts.
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Liu, Qian, Hui Zhang, Lingda Zeng, Yuhua Yu, Xiaolan Lin, and Xiaolei Huang. "Coexistence of Three Dominant Bacterial Symbionts in a Social Aphid and Implications for Ecological Adaptation." Insects 12, no. 5 (2021): 416. http://dx.doi.org/10.3390/insects12050416.
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Aphids are associated with an array of symbionts that have diverse ecological and evolutionary effects on their hosts. To date, symbiont communities of most aphid species are still poorly characterized, especially for the social aphids. In this study, high-throughput 16S rDNA amplicon sequencing was used to assess the bacterial communities of the social aphid Pseudoregma bambucicola, and the differences in bacterial diversity with respect to ant attendance and time series were also assessed. We found that the diversity of symbionts in P. bambucicola was low and three dominant symbionts (Buchnera, Pectobacterium and Wolbachia) were stably coexisting. Pectobacterium may help P. bambucicola feed on the hard bamboo stems, and genetic distance analysis suggests that the Pectobacterium in P. bambucicola may be a new symbiont species. Wolbachia may be associated with the transition of reproduction mode or has a nutritional role in P. bambucicola. Statistical tests on the diversity of bacterial communities in P. bambucicola suggest that aphid populations attended by ants usually have a significantly higher evenness than populations without ant attendance but there was no significant difference among aphid populations from different seasons.
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Smith, Thomas E., and Nancy A. Moran. "Coordination of host and symbiont gene expression reveals a metabolic tug-of-war between aphids and Buchnera." Proceedings of the National Academy of Sciences 117, no. 4 (2020): 2113–21. http://dx.doi.org/10.1073/pnas.1916748117.
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Symbioses between animals and microbes are often described as mutualistic, but are subject to tradeoffs that may manifest as shifts in host and symbiont metabolism, cellular processes, or symbiont density. In pea aphids, the bacterial symbiont Buchnera is confined to specialized aphid cells called bacteriocytes, where it produces essential amino acids needed by hosts. This relationship is dynamic; Buchnera titer varies within individual aphids and among different clonal aphid lineages, and is affected by environmental and host genetic factors. We examined how host genotypic variation relates to host and symbiont function among seven aphid clones differing in Buchnera titer. We found that bacteriocyte gene expression varies among individual aphids and among aphid clones, and that Buchnera gene expression changes in response. By comparing hosts with low and high Buchnera titer, we found that aphids and Buchnera oppositely regulate genes underlying amino acid biosynthesis and cell growth. In high-titer hosts, both bacteriocytes and symbionts show elevated expression of genes underlying energy metabolism. Several eukaryotic cell signaling pathways are differentially expressed in bacteriocytes of low- versus high-titer hosts: Cell-growth pathways are up-regulated in low-titer genotypes, while membrane trafficking, lysosomal processes, and mechanistic target of rapamycin (mTOR) and cytokine pathways are up-regulated in high-titer genotypes. Specific Buchnera functions are up-regulated within different bacteriocyte environments, with genes underlying flagellar body secretion and flagellar assembly overexpressed in low- and high-titer hosts, respectively. Overall, our results reveal allowances and demands made by both host and symbiont engaged in a metabolic “tug-of-war.”
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Russell, Calum W., Sophie Bouvaine, Peter D. Newell, and Angela E. Douglas. "Shared Metabolic Pathways in a Coevolved Insect-Bacterial Symbiosis." Applied and Environmental Microbiology 79, no. 19 (2013): 6117–23. http://dx.doi.org/10.1128/aem.01543-13.
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ABSTRACTThe symbiotic bacteriumBuchnera aphidicolalacks key genes in the biosynthesis of five essential amino acids (EAAs), and yet its animal hosts (aphids) depend on the symbiosis for the synthesis of these EAAs (isoleucine, leucine, methionine, phenylalanine, and valine). We tested the hypothesis, derived from genome annotation, that the missingBuchnerareactions are mediated by host enzymes, with the exchange of metabolic intermediates between the partners. The specialized host cells bearingBuchnerawere separated into aBuchnerafraction and aBuchnera-free host cell fraction (HF). Addition of HF to isolatedBuchnerapreparations significantly increased the production of leucine and phenylalanine, and recombinant enzymes mediating the final reactions in branched-chain amino acid and phenylalanine synthesis rescued the production of these EAAs byBuchnerapreparations without HF. The likely precursors for the missing proximal reactions in isoleucine and methionine synthesis were identified, and they differed from predictions based on genome annotations: synthesis of 2-oxobutanoate, the aphid-derived precursor of isoleucine synthesis, was stimulated by homoserine and not threonine via threonine dehydratase, and production of the homocysteine precursor of methionine was driven by cystathionine, not cysteine, via reversal of the transsulfuration pathway. The evolution of shared metabolic pathways in this symbiosis can be attributed to host compensation for genomic deterioration in the symbiont, involving changes in host gene expression networks to recruit specific enzymes to the host cell.
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Adams, D., T. L. Wilkinson, and A. E. Douglas. "The aphid‐bacterial symbiosis: a comparison between pea aphids and black bean aphids." Entomologia Experimentalis et Applicata 80, no. 1 (1996): 275–78. http://dx.doi.org/10.1111/j.1570-7458.1996.tb00934.x.
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Wilkinson, T., D. Ashford, J. Pritchard, and A. Douglas. "Honeydew sugars and osmoregulation in the pea aphid Acyrthosiphon pisum." Journal of Experimental Biology 200, no. 15 (1997): 2137–43. http://dx.doi.org/10.1242/jeb.200.15.2137.
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Pea aphids, Acyrthosiphon pisum, containing their symbiotic bacteria (untreated aphids) and experimentally deprived of their bacteria by treatment with the antibiotic rifampicin (antibiotic-treated aphids) were reared on the plant Vicia faba. The sugars in the honeydew produced by untreated aphids comprised predominantly the monosaccharides glucose and fructose, while the honeydew of antibiotic-treated aphids contained considerable amounts of oligosaccharides of up to 16 hexose units. The honeydew and haemolymph of the aphids were iso-osmotic, and their osmotic pressure was significantly lower in untreated aphids (0.91­0.95 MPa) than in antibiotic-treated aphids (1.01­1.05 MPa) (P<0.05). For insects reared on chemically defined diets containing 0.15­1.0 mol l-1 sucrose (osmotic pressure 1.1­4.0 MPa), the osmotic pressure of the aphid haemolymph did not vary with dietary osmotic pressure, but was regulated to approximately 1.0 MPa in untreated and 1.3 MPa in antibiotic-treated aphids. The sugars in the aphid honeydew varied with dietary sucrose concentration; with monosaccharides dominant at low concentrations and oligosaccharides dominant at high concentrations of dietary sucrose. The lowest dietary sucrose concentration at which honeydew oligosaccharides were detected was 0.2 mol l-1 for the antibiotic-treated aphids and 0.3 mol l-1 for untreated aphids. These data indicate that the aphid, and not its associated microbiota, mediates the synthesis of oligosaccharides when the osmotic pressure of the ingesta is high.
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Funk, Daniel J., Jennifer J. Wernegreen, and Nancy A. Moran. "Intraspecific Variation in Symbiont Genomes: Bottlenecks and the Aphid-Buchnera Association." Genetics 157, no. 2 (2001): 477–89. http://dx.doi.org/10.1093/genetics/157.2.477.
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Abstract Buchnera are maternally transmitted bacterial endosymbionts that synthesize amino acids that are limiting in the diet of their aphid hosts. Previous studies demonstrated accelerated sequence evolution in Buchnera compared to free-living bacteria, especially for nonsynonymous substitutions. Two mechanisms may explain this acceleration: relaxed purifying selection and increased fixation of slightly deleterious alleles under drift. Here, we test the divergent predictions of these hypotheses for intraspecific polymorphism using Buchnera associated with natural populations of the ragweed aphid, Uroleucon ambrosiae. Contrary to expectations under relaxed selection, U. ambrosiae from across the United States yielded strikingly low sequence diversity at three Buchnera loci (dnaN, trpBC, trpEG), revealing polymorphism three orders of magnitude lower than in enteric bacteria. An excess of nonsynonymous polymorphism and of rare alleles was also observed. Local sampling of additional dnaN sequences revealed similar patterns of polymorphism and no evidence of food plant-associated genetic structure. Aphid mitochondrial sequences further suggested that host bottlenecks and large-scale dispersal may contribute to genetic homogenization of aphids and symbionts. Together, our results support reduced Ne as a primary cause of accelerated sequence evolution in Buchnera. However, our study cannot rule out the possibility that mechanisms other than bottlenecks also contribute to reduced Ne at aphid and endosymbiont loci.
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Nichols, Holly L., Elliott B. Goldstein, Omid Saleh Ziabari, and Benjamin J. Parker. "Intraspecific variation in immune gene expression and heritable symbiont density." PLOS Pathogens 17, no. 4 (2021): e1009552. http://dx.doi.org/10.1371/journal.ppat.1009552.
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Host genetic variation plays an important role in the structure and function of heritable microbial communities. Recent studies have shown that insects use immune mechanisms to regulate heritable symbionts. Here we test the hypothesis that variation in symbiont density among hosts is linked to intraspecific differences in the immune response to harboring symbionts. We show that pea aphids (Acyrthosiphon pisum) harboring the bacterial endosymbiont Regiella insecticola (but not all other species of symbionts) downregulate expression of key immune genes. We then functionally link immune expression with symbiont density using RNAi. The pea aphid species complex is comprised of multiple reproductively-isolated host plant-adapted populations. These ‘biotypes’ have distinct patterns of symbiont infections: for example, aphids from the Trifolium biotype are strongly associated with Regiella. Using RNAseq, we compare patterns of gene expression in response to Regiella in aphid genotypes from multiple biotypes, and we show that Trifolium aphids experience no downregulation of immune gene expression while hosting Regiella and harbor symbionts at lower densities. Using F1 hybrids between two biotypes, we find that symbiont density and immune gene expression are both intermediate in hybrids. We propose that in this system, Regiella symbionts are suppressing aphid immune mechanisms to increase their density, but that some hosts have adapted to prevent immune suppression in order to control symbiont numbers. This work therefore suggests that antagonistic coevolution can play a role in host-microbe interactions even when symbionts are transmitted vertically and provide a clear benefit to their hosts. The specific immune mechanisms that we find are downregulated in the presence of Regiella have been previously shown to combat pathogens in aphids, and thus this work also highlights the immune system’s complex dual role in interacting with both beneficial and harmful microbes.
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Russell, Calum W., Anton Poliakov, Meena Haribal, Georg Jander, Klaas J. van Wijk, and Angela E. Douglas. "Matching the supply of bacterial nutrients to the nutritional demand of the animal host." Proceedings of the Royal Society B: Biological Sciences 281, no. 1791 (2014): 20141163. http://dx.doi.org/10.1098/rspb.2014.1163.
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Various animals derive nutrients from symbiotic microorganisms with much-reduced genomes, but it is unknown whether, and how, the supply of these nutrients is regulated. Here, we demonstrate that the production of essential amino acids (EAAs) by the bacterium Buchnera aphidicola in the pea aphid Acyrthosiphon pisum is elevated when aphids are reared on diets from which that EAA are omitted, demonstrating that Buchnera scale EAA production to host demand. Quantitative proteomics of bacteriocytes (host cells bearing Buchnera ) revealed that these metabolic changes are not accompanied by significant change in Buchnera or host proteins, suggesting that EAA production is regulated post-translationally. Bacteriocytes in aphids reared on diet lacking the EAA methionine had elevated concentrations of both methionine and the precursor cystathionine, indicating that methionine production is promoted by precursor supply and is not subject to feedback inhibition by methionine. Furthermore, methionine production by isolated Buchnera increased with increasing cystathionine concentration. We propose that Buchnera metabolism is poised for EAA production at certain maximal rates, and the realized release rate is determined by precursor supply from the host. The incidence of host regulation of symbiont nutritional function via supply of key nutritional inputs in other symbioses remains to be investigated.
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Fukatsu, Takema. "Secondary Intracellular Symbiotic Bacteria in Aphids of the GenusYamatocallis (Homoptera: Aphididae: Drepanosiphinae)." Applied and Environmental Microbiology 67, no. 11 (2001): 5315–20. http://dx.doi.org/10.1128/aem.67.11.5315-5320.2001.
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ABSTRACT A novel secondary intracellular symbiotic bacterium from aphids of the genus Yamatocallis (subfamily Drepanosiphinae) was characterized by using molecular phylogenetic analysis, in situ hybridization, and diagnostic PCR detection. In the aphid tissues, this bacterium (tentatively designated YSMS [Yamatocallis secondary mycetocyte symbiont]) was found specifically in large cells surrounded by primary mycetocytes harboringBuchnera cells. Of nine drepanosiphine aphids examined, YSMS was detected in only two species of the same genus,Yamatocallis tokyoensis and Yamatocallis hirayamae. In natural populations of these aphids, YSMS was present in 100% of the individuals. Phylogenetic analysis based on 16S ribosomal DNA (rDNA) sequences demonstrated that YSMS ofY. tokyoensis and Y. hirayamae constitute a distinct and isolated clade in the γ subdivision of the classProteobacteria. No 16S rDNA sequences of secondary endosymbionts characterized so far from other aphids showed phylogenetic affinity to YSMS. Based on these results, I suggest that YSMS was acquired by an ancestor of the genus Yamatocallisand has been conserved throughout the evolution of the lineage. By using the nucleotide substitution rate for 16S rDNA ofBuchnera spp., the time of acquisition of YSMS was estimated to be about 13 to 26 million years ago, in the Miocene epoch of the Tertiary period.
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Simonet, Pierre, Karen Gaget, Séverine Balmand, et al. "Bacteriocyte cell death in the pea aphid/Buchnera symbiotic system." Proceedings of the National Academy of Sciences 115, no. 8 (2018): E1819—E1828. http://dx.doi.org/10.1073/pnas.1720237115.
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Symbiotic associations play a pivotal role in multicellular life by facilitating acquisition of new traits and expanding the ecological capabilities of organisms. In insects that are obligatorily dependent on intracellular bacterial symbionts, novel host cells (bacteriocytes) or organs (bacteriomes) have evolved for harboring beneficial microbial partners. The processes regulating the cellular life cycle of these endosymbiont-bearing cells, such as the cell-death mechanisms controlling their fate and elimination in response to host physiology, are fundamental questions in the biology of symbiosis. Here we report the discovery of a cell-death process involved in the degeneration of bacteriocytes in the hemipteran insect Acyrthosiphon pisum. This process is activated progressively throughout aphid adulthood and exhibits morphological features distinct from known cell-death pathways. By combining electron microscopy, immunohistochemistry, and molecular analyses, we demonstrated that the initial event of bacteriocyte cell death is the cytoplasmic accumulation of nonautophagic vacuoles, followed by a sequence of cellular stress responses including the formation of autophagosomes in intervacuolar spaces, activation of reactive oxygen species, and Buchnera endosymbiont degradation by the lysosomal system. We showed that this multistep cell-death process originates from the endoplasmic reticulum, an organelle exhibiting a unique reticular network organization spread throughout the entire cytoplasm and surrounding Buchnera aphidicola endosymbionts. Our findings provide insights into the cellular and molecular processes that coordinate eukaryotic host and endosymbiont homeostasis and death in a symbiotic system and shed light on previously unknown aspects of bacteriocyte biological functioning.
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Adams, D., and A. E. Douglas. "How symbiotic bacteria influence plant utilisation by the polyphagous aphid, Aphis fabae." Oecologia 110, no. 4 (1997): 528–32. http://dx.doi.org/10.1007/s004420050190.
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Grenier, Anne-Marie, Gabrielle Duport, Sylvie Pagès, Guy Condemine, and Yvan Rahbé. "The Phytopathogen Dickeya dadantii (Erwinia chrysanthemi 3937) Is a Pathogen of the Pea Aphid." Applied and Environmental Microbiology 72, no. 3 (2006): 1956–65. http://dx.doi.org/10.1128/aem.72.3.1956-1965.2006.
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ABSTRACT Dickeya dadantii (Erwinia chrysanthemi) is a phytopathogenic bacterium causing soft rot diseases on many crops. The sequencing of its genome identified four genes encoding homologues of the Cyt family of insecticidal toxins from Bacillus thuringiensis, which are not present in the close relative Pectobacterium carotovorum subsp. atrosepticum. The pathogenicity of D. dadantii was tested on the pea aphid Acyrthosiphon pisum, and the bacterium was shown to be highly virulent for this insect, either by septic injury or by oral infection. The lethal inoculum dose was calculated to be as low as 10 ingested bacterial cells. A D. dadantii mutant with the four cytotoxin genes deleted showed a reduced per os virulence for A. pisum, highlighting the potential role of at least one of these genes in pathogenicity. Since only one bacterial pathogen of aphids has been previously described (Erwinia aphidicola), other species from the same bacterial group were tested. The pathogenic trait for aphids was shown to be widespread, albeit variable, within the phytopathogens, with no link to phylogenetic positioning in the Enterobacteriaceae. Previously characterized gut symbionts from thrips (Erwinia/Pantoea group) were also highly pathogenic to the aphid, whereas the potent entomopathogen Photorhabdus luminescens was not. D. dadantii is not a generalist insect pathogen, since it has low pathogenicity for three other insect species (Drosophila melanogaster, Sitophilus oryzae, and Spodoptera littoralis). D. dadantii was one of the most virulent aphid pathogens in our screening, and it was active on most aphid instars, except for the first one, probably due to anatomical filtering. The observed difference in virulence toward apterous and winged aphids may have an ecological impact, and this deserves specific attention in future research.
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Schepers, Matthew J., James N. Yelland, Nancy A. Moran, and David W. Taylor. "Isolation of the Buchnera aphidicola flagellum basal body complexes from the Buchnera membrane." PLOS ONE 16, no. 5 (2021): e0245710. http://dx.doi.org/10.1371/journal.pone.0245710.
Full textAbstract:
Buchnera aphidicola is an intracellular bacterial symbiont of aphids and maintains a small genome of only 600 kbps. Buchnera is thought to maintain only genes relevant to the symbiosis with its aphid host. Curiously, the Buchnera genome contains gene clusters coding for flagellum basal body structural proteins and for flagellum type III export machinery. These structures have been shown to be highly expressed and present in large numbers on Buchnera cells. No recognizable pathogenicity factors or secreted proteins have been identified in the Buchnera genome, and the relevance of this protein complex to the symbiosis is unknown. Here, we show isolation of Buchnera flagellum basal body proteins from the cellular membrane of Buchnera, confirming the enrichment of flagellum basal body proteins relative to other proteins in the Buchnera proteome. This will facilitate studies of the structure and function of the Buchnera flagellum structure, and its role in this model symbiosis.
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Reymond, Nancie, Federica Calevro, José Viñuelas, et al. "Different Levels of Transcriptional Regulation Due to Trophic Constraints in the Reduced Genome of Buchnera aphidicola APS." Applied and Environmental Microbiology 72, no. 12 (2006): 7760–66. http://dx.doi.org/10.1128/aem.01118-06.
Full textAbstract:
ABSTRACT Symbiotic associations involving intracellular microorganisms and animals are widespread, especially for species feeding on poor or unbalanced diets. Buchnera aphidicola, the obligate intracellular bacterium associated with most aphid species, provides its hosts with essential amino acids (EAAs), nutrients in short supply in the plant phloem sap. The Buchnera genome has undergone severe reductions during intracellular evolution. Genes for EAA biosynthesis are conserved, but most of the transcriptional regulatory elements are lost. This work addresses two main questions: is transcription in Buchnera (i) regulated and (ii) scaled to aphid EAA demand? Two microarray experiments were designed for profiling the gene expression in Buchnera. The first one was characterized by a specific depletion of tyrosine and phenylalanine in the aphid diet, and the second experiment combined a global diminution of EAAs in the aphid diet with a sucrose concentration increase to manipulate the aphid growth rate. Aphid biological performance and budget analysis (the balance between EAAs provided by the diet and those synthesized by Buchnera) were performed to quantify the nutritional demand from the aphids toward their symbiotic bacteria. Despite the absence of known regulatory elements, a significant transcriptional regulation was observed at different levels of organization in the Buchnera genome: between genes, within putative transcription units, and within specific metabolic pathways. However, unambiguous evidence for transcriptional changes underpinning the scaling of EAA biosynthesis to aphid demand was not obtained. The phenotypic relevance of the transcriptional response from the reduced genome of Buchnera is addressed.
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Sakurai, Makiko, Ryuichi Koga, Tsutomu Tsuchida, Xian-Ying Meng, and Takema Fukatsu. "Rickettsia Symbiont in the Pea Aphid Acyrthosiphon pisum: Novel Cellular Tropism, Effect on Host Fitness, and Interaction with the Essential Symbiont Buchnera." Applied and Environmental Microbiology 71, no. 7 (2005): 4069–75. http://dx.doi.org/10.1128/aem.71.7.4069-4075.2005.
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ABSTRACT In natural populations of the pea aphid Acyrthosiphon pisum, a facultative bacterial symbiont of the genus Rickettsia has been detected at considerable infection frequencies worldwide. We investigated the effects of the Rickettsia symbiont on the host aphid and also on the coexisting essential symbiont Buchnera. In situ hybridization revealed that the Rickettsia symbiont was specifically localized in two types of host cells specialized for endosymbiosis: secondary mycetocytes and sheath cells. Electron microscopy identified bacterial rods, about 2 μm long and 0.5 μm thick, in sheath cells of Rickettsia-infected aphids. Virus-like particles were sometimes observed in association with the bacterial cells. By an antibiotic treatment, we generated Rickettsia-infected and Rickettsia-eliminated aphid strains with an identical genetic background. Comparison of these strains revealed that Rickettsia infection negatively affected some components of the host fitness. Quantitative PCR analysis of the bacterial population dynamics identified a remarkable interaction between the coexisting symbionts: Buchnera population was significantly suppressed in the presence of Rickettsia, particularly at the young adult stage, when the aphid most actively reproduces. On the basis of these results, we discussed the possible mechanisms that enable the prevalence of Rickettsia infection in natural host populations in spite of the negative fitness effects observed in the laboratory.
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McLean, Ailsa H. C., Benjamin J. Parker, Jan Hrček, Lee M. Henry, and H. Charles J. Godfray. "Insect symbionts in food webs." Philosophical Transactions of the Royal Society B: Biological Sciences 371, no. 1702 (2016): 20150325. http://dx.doi.org/10.1098/rstb.2015.0325.
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Recent research has shown that the bacterial endosymbionts of insects are abundant and diverse, and that they have numerous different effects on their hosts' biology. Here we explore how insect endosymbionts might affect the structure and dynamics of insect communities. Using the obligate and facultative symbionts of aphids as an example, we find that there are multiple ways that symbiont presence might affect food web structure. Many symbionts are now known to help their hosts escape or resist natural enemy attack, and others can allow their hosts to withstand abiotic stress or affect host plant use. In addition to the direct effect of symbionts on aphid phenotypes there may be indirect effects mediated through trophic and non-trophic community interactions. We believe that by using data from barcoding studies to identify bacterial symbionts, this extra, microbial dimension to insect food webs can be better elucidated. This article is part of the themed issue ‘From DNA barcodes to biomes’.
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Moran, Nancy A., Jacob A. Russell, Ryuichi Koga, and Takema Fukatsu. "Evolutionary Relationships of Three New Species of Enterobacteriaceae Living as Symbionts of Aphids and Other Insects." Applied and Environmental Microbiology 71, no. 6 (2005): 3302–10. http://dx.doi.org/10.1128/aem.71.6.3302-3310.2005.
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ABSTRACT Ecological studies on three bacterial lineages symbiotic in aphids have shown that they impose a variety of effects on their hosts, including resistance to parasitoids and tolerance to heat stress. Phylogenetic analyses of partial sequences of gyrB and recA are consistent with previous analyses limited to 16S rRNA gene sequences and yield improved confidence of the evolutionary relationships of these symbionts. All three symbionts are in the Enterobacteriaceae. One of the symbionts, here given the provisional designation “Candidatus Serratia symbiotica,” is a Serratia species that has acquired a symbiotic lifestyle. The other two symbionts, here designated “Candidatus Hamiltonella defensa” and “Candidatus Regiella insecticola,” are sister groups to one another and together show a relationship to species of Photorhabdus.
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Wieczorek, Karina, Mariusz Kanturski, Cezary Sempruch, and Piotr Świątek. "The reproductive system of the male and oviparous female of a model organism—the pea aphid, Acyrthosiphon pisum (Hemiptera, Aphididae)." PeerJ 7 (September 2, 2019): e7573. http://dx.doi.org/10.7717/peerj.7573.
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The structure of the reproductive system of the sexual generation—males and oviparous females—of the pea aphid Acyrthosiphon pisum (Harris) (Hemiptera, Aphididae), a serious pest of cultivated plants of Fabaceae, was investigated. For the first time we describe the morphology, histology and ultrastructure of the reproductive system in both morphs of the sexual generation of aphids within one species, using light and fluorescent microscopy, as well as transmission and scanning electron microscopy. The results revealed that males have testes composed of three follicles fused by the upper ends of the vasa efferentia, the vasa deferentia run independently, the accessory glands are asymmetric and the ejaculatory duct shortened. Oviparous females have ovaries composed of seven ovarioles each. The lateral oviducts join to a short common oviduct connected with the unpaired spermatheca and paired accessory glands. Yolky eggs with an aggregation of symbiotic bacteria at the posterior pole are produced. Histologically, the components of genital tracts are broadly similar: the epithelial cells of the walls of the vasa deferentia and accessory glands of the male and oviparous female have secretory functions which correlate with the age of the studied morphs. We also found symbiotic bacteria within the vasa deferentia epithelial cells in males and within the cells of the lateral oviducts of females. Because the pea aphid is listed among the 14 species that are of the greatest economic importance, our results will be useful for managing aphid populations, protecting plants and ensuring global food security.
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Badji, Cesar Auguste, Zoé Sol-Mochkovitch, Charlotte Fallais, et al. "Alarm Pheromone Responses Depend on Genotype, but Not on the Presence of Facultative Endosymbionts in the Pea Aphid Acyrthosiphon pisum." Insects 12, no. 1 (2021): 43. http://dx.doi.org/10.3390/insects12010043.
Full textAbstract:
Aphids use an alarm pheromone, E-β farnesene (EBF), to warn conspecifics of potential danger. The antennal sensitivity and behavioural escape responses to EBF can be influenced by different factors. In the pea aphid, Acyrthosiphon pisum, different biotypes are adapted to different legume species, and within each biotype, different genotypes exist, which can carry or not Hamiltonella defensa, a bacterial symbiont that can confer protection against natural enemies. We investigate here the influence of the aphid genotype and symbiotic status on the escape behaviour using a four-way olfactometer and antennal sensitivity for EBF using electroantennograms (EAGs). Whereas the investigated three genotypes from two biotypes showed significantly different escape and locomotor behaviours in the presence of certain EBF doses, the infection with H. defensa did not significantly modify the escape behaviour and only marginally influenced the locomotor behaviour at high doses of EBF. Dose-response curves of EAG amplitudes after stimulation with EBF differed significantly between aphid genotypes in correlation with behavioural differences, whereas antennal sensitivity to EBF did not change significantly as a function of the symbiotic status. The protective symbiont H. defensa does thus not modify the olfactory sensitivity to the alarm pheromone. How EBF sensitivity is modified between genotypes or biotypes remains to be investigated.
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Badji, Cesar Auguste, Zoé Sol-Mochkovitch, Charlotte Fallais, et al. "Alarm Pheromone Responses Depend on Genotype, but Not on the Presence of Facultative Endosymbionts in the Pea Aphid Acyrthosiphon pisum." Insects 12, no. 1 (2021): 43. http://dx.doi.org/10.3390/insects12010043.
Full textAbstract:
Aphids use an alarm pheromone, E-β farnesene (EBF), to warn conspecifics of potential danger. The antennal sensitivity and behavioural escape responses to EBF can be influenced by different factors. In the pea aphid, Acyrthosiphon pisum, different biotypes are adapted to different legume species, and within each biotype, different genotypes exist, which can carry or not Hamiltonella defensa, a bacterial symbiont that can confer protection against natural enemies. We investigate here the influence of the aphid genotype and symbiotic status on the escape behaviour using a four-way olfactometer and antennal sensitivity for EBF using electroantennograms (EAGs). Whereas the investigated three genotypes from two biotypes showed significantly different escape and locomotor behaviours in the presence of certain EBF doses, the infection with H. defensa did not significantly modify the escape behaviour and only marginally influenced the locomotor behaviour at high doses of EBF. Dose-response curves of EAG amplitudes after stimulation with EBF differed significantly between aphid genotypes in correlation with behavioural differences, whereas antennal sensitivity to EBF did not change significantly as a function of the symbiotic status. The protective symbiont H. defensa does thus not modify the olfactory sensitivity to the alarm pheromone. How EBF sensitivity is modified between genotypes or biotypes remains to be investigated.