Bacteriophages Encode Factors Required for Protection in a Symbiotic Mutualism

Oliver, Kerry M.; Degnan, Patrick H.; Hunter, Martha S.; Moran, Nancy A.

doi:10.1126/science.1174463

Cited by 419 publications

(432 citation statements)

References 22 publications

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“…Hamiltonella defensa is found at intermediate frequencies in nature [28,32] and most field-collected H. defensa-infected aphids are also infected by APSE [14,33]. Population cage studies reveal that aphids infected with H. defensa and APSE-3 rapidly spread to near-fixation when parasitism pressure is present, whereas uninfected aphids are favoured in the absence of parasitism [29].…”

Section: Discussionmentioning

confidence: 99%

“…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%

“…APSE-3 infections are also transmitted with very high fidelity, but can be spontaneously lost at very low rates [14]. We therefore used previously established sub-lines from the aphid clone 5A that had been inoculated with the APSE-3-harbouring H. defensa strain A1A (A1A þ !…”

Section: Materials and Methods (A) Study Organismsmentioning

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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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

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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“…2007; Oliver et al. 2009; Hansen and Moran 2014), however eco‐evolutionary aspects are relatively unexplored (Kwiatkowski and Vorburger 2012; Russell et al. 2013; Oliver et al.…”

Section: Introductionmentioning

confidence: 99%

Stress‐induced changes in abundance differ among obligate and facultative endosymbionts of the soybean aphid

Enders

Miller

2016

Ecology and Evolution

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Bacterial endosymbionts can drive evolutionary novelty by conferring adaptive benefits under adverse environmental conditions. Among aphid species there is growing evidence that symbionts influence tolerance to various forms of stress. However, the extent to which stress inflicted on the aphid host has cascading effects on symbiont community dynamics remains poorly understood. Here we simultaneously quantified the effect of host‐plant induced and xenobiotic stress on soybean aphid (Aphis glycines) fitness and relative abundance of its three bacterial symbionts. Exposure to soybean defensive stress (Rag1 gene) and a neurotoxic insecticide (thiamethoxam) substantially reduced aphid composite fitness (survival × reproduction) by 74 ± 10% and 92 ± 2%, respectively, which in turn induced distinctive changes in the endosymbiont microbiota. When challenged by host‐plant defenses a 1.4‐fold reduction in abundance of the obligate symbiont Buchnera was observed across four aphid clonal lines. Among facultative symbionts of Rag1‐stressed aphids, Wolbachia abundance increased twofold and Arsenophonus decreased 1.5‐fold. A similar pattern was observed under xenobiotic stress, with Buchnera and Arsenophonus titers decreasing (1.3‐fold) and Wolbachia increasing (1.5‐fold). Furthermore, variation in aphid virulence to Rag1 was positively correlated with changes in Arsenophonus titers, but not Wolbachia or Buchnera. A single Arsenophonus multi‐locus genotype was found among aphid clonal lines, indicating strain diversity is not primarily responsible for correlated host‐symbiont stress levels. Overall, our results demonstrate the nature of aphid symbioses can significantly affect the outcome of interactions under stress and suggests general changes in the microbiome can occur across multiple stress types.

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“…In aphids infected with a protective symbiont, the parasitoid dies during the egg or larval stage. 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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Bacteriophages Encode Factors Required for Protection in a Symbiotic Mutualism

Cited by 419 publications

References 22 publications

Phage loss and the breakdown of a defensive symbiosis in aphids

Phage loss and the breakdown of a defensive symbiosis in aphids

Stress‐induced changes in abundance differ among obligate and facultative endosymbionts of the soybean aphid

Evidence for specificity in symbiont-conferred protection against parasitoids

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