Dynamics of genome evolution in facultative symbionts of aphids

Degnan, Patrick H.; Leonardo, Teresa E.; Cass, Bodil N.; Hurwitz, Bonnie; Stern, David L.; Gibbs, Richard A.; Richards, Stephen M.; Moran, Nancy A.

doi:10.1111/j.1462-2920.2009.02085.x

Cited by 84 publications

(96 citation statements)

References 51 publications

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“…Several indicators reveal that the R. insecticola 5.15 genome sequence is near completion. First, the genome size of R. insecticola 5.15 (at 2.01 Mbp) is similar to the previously sequenced R. insecticola LSR1 (at 2.07 Mbp) (Degnan et al 2010; Table 2). Second, the retrieved contigs included 186 of 205 single-copy genes (SICO) that are present in most Gammaproteobacteria (Lerat et al 2003).…”

Section: Genome Sequencing and Annotationmentioning

confidence: 59%

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Genomic basis of endosymbiont-conferred protection against an insect parasitoid

Hansen¹,

Vorburger²,

Moran³

2011

Genome Res.

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Bacterial endosymbionts exert a variety of beneficial effects on insect hosts. In pea aphids (Acyrthosiphon pisum), several inherited endosymbiont species protect their hosts against parasitoid wasps, which are major natural enemies. However, strains of these symbiont species vary in their ability to confer protection against parasitoids, with some conferring almost complete protection and others conferring almost none. In this study, two strains of the endosymbiont Regiella insecticola (R. insecticola 5.15 and R. insecticola LSR1) were found to differ in ability to protect pea aphids attacked by the parasitoid Aphidius ervi. Parasitism trials reveal that R. insecticola 5.15, but not R. insecticola LSR1, significantly reduced parasitoid success and increased aphid survivorship. To address the potential genetic basis of protection conferred by R. insecticola 5.15 we sequenced the genome of this symbiont strain, and then compared its gene repertoire with that of the already sequenced nonprotective strain R. insecticola LSR1. We identified striking differences in gene sets related to eukaryote pathogenicity. The protective strain R. insecticola 5.15 encoded five categories of pathogenicity factors that were missing or inactivated in R. insecticola LSR1. These included genes encoding the O-antigen biosynthetic pathway, an intact Type 1 Secretion System and its secreted RTX toxins, an intact SPI-1 Type 3 Secretion System and its effectors, hemin transport, and the twocomponent system PhoPQ. These five pathogenicity factors and translocation systems are hypothesized to collectively play key roles in the endosymbiont's virulence against parasitoids, resulting in aphid protection. Mechanisms through which these factors may target parasitoids are discussed.

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Section: Genome Sequencing and Annotationmentioning

confidence: 59%

“…A previously sequenced strain, R. insecticola LSR1 (Degnan et al 2010), is closely related to R. insecticola 5AU, and both originated from A. pisum collected in New York, USA. Preliminary assays suggested that R. insecticola LSR1 resembled R. insecticola 5AU in failing to confer any resistance to A. ervi (NA Moran, unpubl.).…”

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confidence: 99%

Genomic basis of endosymbiont-conferred protection against an insect parasitoid

Hansen¹,

Vorburger²,

Moran³

2011

Genome Res.

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“…Population cage studies have shown that, in the absence of parasitoid pressure, the frequencies of H. defensa and S. symbiotica decrease, suggesting that infection with these symbionts imparts a cost to the aphid [26]. The recently completed genome sequences of H. defensa and R. insecticola revealed the absence of most EAA biosynthesis pathways, implying that these symbionts obtain these nutrients from the aphid's free amino acid pool [27,28].…”

Section: Discussionmentioning

confidence: 99%

Sources of variation in dietary requirements in an obligate nutritional symbiosis

Vogel

Moran

2010

Proc. R. Soc. B.

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The nutritional symbiosis between aphids and their obligate symbiont, Buchnera aphidicola , is often characterized as a highly functional partnership in which the symbiont provides the host with essential nutrients. Despite this, some aphid lineages exhibit dietary requirements for nutrients typically synthesized by Buchnera , suggesting that some aspect of the symbiosis is disrupted. To examine this phenomenon in the pea aphid, Acyrthosiphon pisum , populations were assayed using defined artificial diet to determine dietary requirements for essential amino acids (EAAs). Six clones exhibiting dependence on EAAs in their diet were investigated further. In one aphid clone, a mutation in a Buchnera amino acid biosynthesis gene could account for the clone's requirement for dietary arginine. Analysis of aphid F 1 hybrids allowed separation of effects of the host and symbiont genomes, and revealed that both affect the requirement for dietary EAAs in the clones tested. Amino acid requirements were minimally affected by secondary symbiont infection. Our results indicate that variation among pea aphids in dependence on dietary amino acids can result from Buchnera mutation as well as variation in the host genotype.

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“…On the basis of genome sequences, H. defensa and R. insecticola are only able to produce the essential amino acids lysine and threonine (Degnan et al, 2009a, b), but other essential amino acids also increase because of infection with these symbionts. One possibility is that facultative symbiont infection somehow stimulates Buchnera to produce amino acids, as Buchnera is the only organism in the system capable of producing most essential amino acids (Shigenobu et al, 2000).…”

Section: Metabolic Responses To Symbiont Infectionmentioning

confidence: 99%

“…Another possibility is that proteases produced by facultative symbionts are degrading proteins, increasing free amino acid pools in pea aphids. The H. defensa and R. insecticola genomes possess several proteases that could be responsible for this effect (Degnan et al, 2009a, b).…”

Section: Metabolic Responses To Symbiont Infectionmentioning

confidence: 99%

Effects of facultative symbionts and heat stress on the metabolome of pea aphids

2009

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We examined metabolite pools of pea aphids with different facultative symbiont infections, and characterized their effects on aphid metabolism in baseline and heat stress conditions. The bacterial symbiont Serratia symbiotica protects aphid hosts from the detrimental results of heat stress and shields the obligate symbiont Buchnera from effects of heat. We investigated whether broad effects on metabolism might correlate with this protection. Both facultative symbiont infection and heat treatment had large effects on the aphid metabolome. All three pea aphid facultative symbionts had similar effects on aphid metabolism despite their evolutionary diversity. Paradoxically, heat triggers lysis of many S. symbiotica cells and a correlated rapid reduction in S. symbiotica titres within aphid hosts. We conclude that facultative symbionts can have substantial effects on host metabolic pools, and we hypothesize that the protective effects of S. symbiotica may reflect the delivery of protective metabolites to aphid or Buchnera cells, after heat exposure.

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Dynamics of genome evolution in facultative symbionts of aphids

Cited by 84 publications

References 51 publications

Genomic basis of endosymbiont-conferred protection against an insect parasitoid

Genomic basis of endosymbiont-conferred protection against an insect parasitoid

Sources of variation in dietary requirements in an obligate nutritional symbiosis

Effects of facultative symbionts and heat stress on the metabolome of pea aphids

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