The players in a mutualistic symbiosis: Insects, bacteria, viruses, and virulence genes

Moran, Nancy A.; Degnan, Patrick H.; Santos, Scott R.; Dunbar, Helen E.; Ochman, Howard

doi:10.1073/pnas.0507029102

Cited by 289 publications

(278 citation statements)

References 67 publications

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“…The H. defensa genome appears to encode two intact type III secretion systems, which are used by many pathogens for invading and manipulating host cells (22). All strains of H. defensa studied also contain variable phage genomes that sometimes encode toxins targeted to eukaryotic cells (22).…”

Section: Discussionmentioning

confidence: 99%

Sexual acquisition of beneficial symbionts in aphids

Moran

Dunbar

2006

Proc. Natl. Acad. Sci. U.S.A.

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230

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A noted cost of mating is the risk of acquiring sexually transmitted infections that are detrimental to the recipient. But many microbial associates of eukaryotes are mutualistic, raising the possibility that sexual contact provides the opportunity to acquire symbionts that are beneficial. In aphids, facultative bacterial symbionts, which benefit hosts by conferring resistance to natural enemies or to heat, are transmitted maternally with high fidelity and are maintained stably throughout hundreds of parthenogenetic generations in the laboratory. Data from field populations indicate that horizontal transfer of these facultative symbionts is frequent, and transfections are readily achieved by microinjection or ingestion in artificial diet. However, no natural mechanism for the horizontal transfer of these symbionts has been identified. Here we demonstrate that during sexual reproduction, male-borne symbionts can be acquired by females and subsequently transferred to sexually and parthenogenetically produced progeny, establishing stable, maternally transmitted associations. In our experiments, sexually transmitted symbionts resulted in (i) infection of previously uninfected matrilines, (ii) a double infection in a matriline already bearing a different symbiont, and (iii) replacement of the maternal symbiont. We also observed some cases in which maternal symbionts failed to become established in sexually produced progeny. Microscopy indicated that symbionts were abundant in the male reproductive system, which demonstrates a natural route of nonmaternal transfer of insect symbionts. Because such transfer can generate coinfections, thereby creating opportunities for symbiont competition and recombination, paternal inheritance has major consequences for expectations regarding symbiont evolution.Acyrthosiphon pisum ͉ mutualism ͉ symbiosis

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Section: Discussionmentioning

confidence: 99%

Sexual acquisition of beneficial symbionts in aphids

Moran

Dunbar

2006

Proc. Natl. Acad. Sci. U.S.A.

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230

221

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“…In addition to encoding pathways that benefit both the bacterial and animal hosts [8,10,14], bacteriophages may alter symbiont abundance within individual hosts and thereby play critical roles in the maintenance of heritable symbiosis within host populations.…”

Section: Discussionmentioning

confidence: 99%

“…There are two APSE variants (APSE-2 and APSE-3) commonly found in North American populations of A. pisum. Each variant shares a core of conserved genes but also contains a variable region consisting of holin, lysozyme and toxin genes from two protein families: cytolethal distending toxin (CdtB; APSE-2), and YD-repeat toxin (Ydp; APSE-3) [8,9]. Phylogenetic evidence shows that APSEs move these pathways horizontally between H. defensa lineages [9].…”

Section: Introductionmentioning

confidence: 99%

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Phage loss and the breakdown of a defensive symbiosis in aphids

Weldon

Strand²,

Oliver³

2013

Proc. R. Soc. B.

101

111

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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 insectbacteria 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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“…Protection by H. defensa is dependent on the presence of a bacteriophage, termed APSE (A. pisum Secondary Endosymbiont) [24], which carries putative toxin genes affecting eukaryotes [25,26]. Variation in toxin genes is correlated with variation in the strength of protection [11,27,28], while strains lacking the phage [25,28], or which carry phages with apparently inactivated toxin genes [29], provide no protection.…”

Section: Introductionmentioning

confidence: 99%

Evidence for specificity in symbiont-conferred protection against parasitoids

2015

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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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The players in a mutualistic symbiosis: Insects, bacteria, viruses, and virulence genes

Cited by 289 publications

References 67 publications

Sexual acquisition of beneficial symbionts in aphids

Sexual acquisition of beneficial symbionts in aphids

Phage loss and the breakdown of a defensive symbiosis in aphids

Evidence for specificity in symbiont-conferred protection against parasitoids

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