Diversity of Bacteria Associated with Natural AphidPopulations

Haynes, Susan R.; Darby, Alistair C.; Daniell, Tim J.; Webster, Gordon; Veen, F. J. Frank van; Godfray, H.C.F.; Prosser, James I.; Douglas, Alex

doi:10.1128/aem.69.12.7216-7223.2003

Cited by 128 publications

(111 citation statements)

References 43 publications

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“…The regular occurrence of coinfections in field populations (3,6,7,17) is one of several indicators that the horizontal transmission of facultative symbionts among maternal lineages must occur regularly in pea aphid populations. Horizontal transmission within and among species is also demonstrated by molecular phylogenetic analyses (3,16,17).…”

Section: Prior Evidence For Horizontal Transfer Of Aphid Facultative mentioning

confidence: 99%

“…In the pea aphid, Acyrthosiphon pisum, three species of symbionts, all members of the Enterobacteriaceae (''Candidatus Hamiltonella defensa,'' ''Candidatus Serratia symbiotica,'' and ''Candidatus Regiella insecticola''), occur at high frequencies in field populations. Individual aphids can be infected with zero, one, or two symbiont types (3)(4)(5)(6)(7). Strains of each of these facultative symbionts have been shown to confer major fitness benefits on their aphid hosts, such as the ability to overcome infection by wasp parasitoids (8,9), resistance to fungal pathogens (10), expansion of host-plant range (11), and tolerance to heat stress (12)(13)(14)(15).…”

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confidence: 99%

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Sexual acquisition of beneficial symbionts in aphids

Moran

Dunbar

2006

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

227

221

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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: Prior Evidence For Horizontal Transfer Of Aphid Facultative mentioning

confidence: 99%

mentioning

confidence: 99%

Sexual acquisition of beneficial symbionts in aphids

Moran

Dunbar

2006

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

227

221

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“…One of these is ''Candidatus Hamiltonella defensa'' (previously known as ''T type'' or ''PABS'', ref. 1), a member of the Enterobacteriaceae that is found in aphids as well as other insect families (1)(2)(3)(4)(5). In pea aphids, the effects of attack by parasitoid wasps are ameliorated by infection with H. defensa: the wasp larva dies prematurely, allowing the aphid host to develop to the adult stage and to reproduce (6).…”

mentioning

confidence: 99%

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

Moran

Degnan

Santos

et al. 2005

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

289

271

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Aphids maintain mutualistic symbioses involving consortia of coinherited organisms. All possess a primary endosymbiont, Buchnera, which compensates for dietary deficiencies; many also contain secondary symbionts, such as Hamiltonella defensa, which confers defense against natural enemies. Genome sequences of uncultivable secondary symbionts have been refractory to analysis due to the difficulties of isolating adequate DNA samples. By amplifying DNA from hemolymph of infected pea aphids, we obtained a set of genomic sequences of H. defensa and an associated bacteriophage. H. defensa harbors two type III secretion systems, related to those that mediate host cell entry by enteric pathogens. The phage, called APSE-2, is a close relative of the previously sequenced APSE-1 but contains intact homologs of the gene encoding cytolethal distending toxin (cdtB), which interrupts the eukaryotic cell cycle and which is known from a variety of mammalian pathogens. The cdtB homolog is highly expressed, and its genomic position corresponds to that of a homolog of stx (encoding Shiga-toxin) within APSE-1. APSE-2 genomes were consistently abundant in infected pea aphids, and related phages were found in all tested isolates of H. defensa, from numerous insect species. Based on their ubiquity and abundance, these phages appear to be an obligate component of the H. defensa life cycle. We propose that, in these mutualistic symbionts, phage-borne toxin genes provide defense to the aphid host and are a basis for the observed protection against eukaryotic parasites.Acrythosiphon pisum ͉ Hamiltonella defensa ͉ lamboid phage ͉ aphid ͉ Enterobacteriaceae

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“…The Sutton) at 20°C with the 18 L:6D regime. The aphids were confirmed to lack gut microorganisms by microscopical examination and polymerase chain recation (PCR) assays using the general 16S rRNA gene primers 16SA1 and 16SB1 and DNA from isolated aphid guts as a template; and no secondary symbionts were detected by diagnostic PCR assays 13 with total aphid DNA as a template (data not shown). Additionally, surface-sterilized aphids yielded no microorganisms that grew on standard microbiological media.…”

Section: Methodsmentioning

confidence: 99%

“…First, it is the only animal symbiosis for which the genome of both partners has been sequenced (http:// www.iagc.org). 12 Second, B. aphidicola is the dominant, and often sole, microbial partner of aphids, 13 enabling the animalmicrobial interaction to be anchored to a single microorganism of known gene content. By contrast, the microbiota of many animals, including humans, is complex, comprising hundredsto-thousands of interacting microbial taxa, and function cannot be coupled with confidence to any single species.…”

Section: Introductionmentioning

confidence: 99%

Integrated Metabonomic−Proteomic Analysis of an Insect−Bacterial Symbiotic System

et al. 2010

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The health of animals, including humans, is dependent on their resident microbiota, but the complexity of the microbial communities makes these associations difficult to study in most animals. Exceptionally, the microbiology of the pea aphid Acyrthosiphon pisum is dominated by a single bacterium Buchnera aphidicola (B. aphidicola). A 1 H NMR-based metabonomic strategy was applied to investigate metabolic profiles of aphids fed on a low essential amino acid diet and treated by antibiotic to eliminate B. aphidicola. In addition, differential gel electrophoresis (DIGE) with mass spectrometry was utilized to determine the alterations of proteins induced by these treatments. We found that these perturbations resulted in significant changes to the abundance of 15 metabolites and 238 proteins. Ten (67%) of the metabolites with altered abundance were amino acids, with nonessential amino acids increased and essential amino acids decreased by both perturbations. Over-represented proteins in the perturbed treatments included catabolic enzymes with roles in amino acid degradation and glycolysis, various cuticular proteins, and a C-type lectin and regucalcin with candidate defensive roles. This analysis demonstrates the central role of essential amino acid production in the relationship and identifies candidate proteins and processes underpinning the function and persistence of the association.

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Diversity of Bacteria Associated with Natural AphidPopulations

Cited by 128 publications

References 43 publications

Sexual acquisition of beneficial symbionts in aphids

Sexual acquisition of beneficial symbionts in aphids

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

Integrated Metabonomic−Proteomic Analysis of an Insect−Bacterial Symbiotic System

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