Dataset Information

Culture of an aphid heritable symbiont demonstrates its direct role in defence against parasitoids.

ABSTRACT: Heritable symbionts are common in insects with many contributing to host defence. Hamiltonella defensa is a facultative, bacterial symbiont of the pea aphid, Acyrthosiphon pisum that provides protection against the endoparasitoid wasp Aphidius ervi Protection levels vary among strains of H. defensa that are differentially infected by bacteriophages named APSEs. By contrast, little is known about mechanism(s) of resistance owing to the intractability of host-restricted microbes for functional study. Here, we developed methods for culturing strains of H. defensa that varied in the presence and type of APSE. Most H. defensa strains proliferated at 27°C in co-cultures with the TN5 cell line or as pure cultures with no insect cells. The strain infected by APSE3, which provides high levels of protection in vivo, produced a soluble factor(s) that disabled development of A. ervi embryos independent of any aphid factors. Experimental transfer of APSE3 also conferred the ability to disable A. ervi development to a phage-free strain of H. defensa Altogether, these results provide a critical foundation for characterizing symbiont-derived factor(s) involved in host protection and other functions. Our results also demonstrate that phage-mediated transfer of traits provides a mechanism for innovation in host restricted symbionts.

SUBMITTER: Brandt JW

PROVIDER: S-EPMC5698653 | biostudies-literature | 2017 Nov

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Culture of an aphid heritable symbiont demonstrates its direct role in defence against parasitoids.

Brandt Jayce W JW Chevignon Germain G Oliver Kerry M KM Strand Michael R MR

Proceedings. Biological sciences 20171101 1866

Heritable symbionts are common in insects with many contributing to host defence. Hamiltonella defensa is a facultative, bacterial symbiont of the pea aphid, Acyrthosiphon pisum that provides protection against the endoparasitoid wasp Aphidius ervi Protection levels vary among strains of H. defensa that are differentially infected by bacteriophages named APSEs. By contrast, little is known about mechanism(s) of resistance owing to the intractability of host-restricted ...[more]

PMID: 29093227

Similar Datasets

Project description:Insects and other animals commonly form symbioses with heritable bacteria, which can exert large influences on host biology and ecology. The pea aphid, Acyrthosiphon pisum, is a model for studying effects of infection with heritable facultative symbionts (HFS), and each of its seven common HFS species has been reported to provide resistance to biotic or abiotic stresses. However, one common HFS, called X-type, rarely occurs as a single infection in field populations and instead typically superinfects individual aphids with Hamiltonella defensa, another HFS that protects aphids against attack by parasitic wasps. Using experimental aphid lines comprised of all possible infection combinations in a uniform aphid genotype, we investigated whether the most common strain of X-type provides any of the established benefits associated with aphid HFS as a single infection or superinfection with H. defensa We found that X-type does not confer protection to any tested threats, including parasitoid wasps, fungal pathogens, or thermal stress. Instead, component fitness assays identified large costs associated with X-type infection, costs which were ameliorated in superinfected aphids. Together these findings suggest that X-type exploits the aphid/H. defensa mutualism and is maintained primarily as a superinfection by "hitchhiking" via the mutualistic benefits provided by another HFS. Exploitative symbionts potentially restrict the functions and distributions of mutualistic symbioses with effects that extend to other community members.IMPORTANCE Maternally transmitted bacterial symbionts are widespread and can have major impacts on the biology of arthropods, including insects of medical and agricultural importance. Given that host fitness and symbiont fitness are tightly linked, inherited symbionts can spread within host populations by providing beneficial services. Many insects, however, are frequently infected with multiple heritable symbiont species, providing potential alternative routes of symbiont maintenance. Here we show that a common pea aphid symbiont called X-type likely employs an exploitative strategy of hitchhiking off the benefits of a protective symbiont, Hamiltonella Infection with X-type provides none of the benefits conferred by other aphid symbionts and instead results in large fitness costs, costs lessened by superinfection with Hamiltonella These findings are corroborated by natural infections in field populations, where X-type is mostly found superinfecting aphids with Hamiltonella Exploitative symbionts may be common in hosts with communities of heritable symbionts and serve to hasten the breakdown of mutualisms.

Project description:Insects are often attacked by multiple natural enemies, imposing dynamic selective pressures for the development and maintenance of enemy-specific resistance. Pea aphids (Acyrthosiphon pisum) have emerged as models for the study of variation in resistance against natural enemies, including parasitoid wasps. Internal defenses against their most common parasitoid wasp, Aphidius ervi, are sourced through two known mechanisms- 1) endogenously encoded resistance or 2) infection with the heritable bacterial symbiont, Hamiltonella defensa. Levels of resistance can range from nearly 0-100% against A. ervi but varies based on aphid genotype and the strain of toxin-encoding bacteriophage (called APSE) carried by Hamiltonella. Previously, other parasitoid wasps were found to commonly attack this host, but North American introductions of A. ervi have apparently displaced all other parasitoids except Praon pequodorum, a related aphidiine braconid wasp, which is still found attacking this host in natural populations. To explain P. pequodorum's persistence, multiple studies have compared direct competition between both wasps, but have not examined specificity of host defenses as an indirectly mediating factor. Using an array of experimental aphid lines, we first examined whether aphid defenses varied in effectiveness toward either wasp species. Expectedly, both types of aphid defenses were effective against A. ervi, but unexpectedly, were completely ineffective against P. pequodorum. Further examination showed that P. pequodorum wasps suffered no consistent fitness costs from developing in even highly 'resistant' aphids. Comparison of both wasps' egg-larval development revealed that P. pequodorum's eggs have thicker chorions and hatch two days later than A. ervi's, likely explaining their differing abilities to overcome aphid defenses. Overall, our results indicate that aphids resistant to A. ervi may serve as reservoirs for P. pequodorum, hence contributing to its persistence in field populations. We find that specificity of host defenses and defensive symbiont infections, may have important roles in influencing enemy compositions by indirectly mediating the interactions and abundance of rival natural enemies.

Project description:In grain crops, aphids are important pests, but they can be suppressed by hymenopteran parasitoids. A challenge in incorporating parasitoids into Integrated Pest Management (IPM) programs, however, is that parasitoid numbers can be low during periods within the season when aphids are most damaging. Understanding the population dynamics of key aphid species and their parasitoids is central to ameliorating this problem. To examine the composition and seasonal trends of both aphid and parasitoid populations in south-eastern Australia, samples were taken throughout the winter growing seasons of 2017 and 2018 in 28 fields of wheat and canola. Myzus persicae (Sulzer) was the most abundant aphid species, particularly within canola crops. Across all fields, aphid populations remained relatively low during the early stages of crop growth and increased as the season progressed. Seasonal patterns were consistent across sites, due to climate, crop growth stage, and interactions between these factors. For canola, field edges did not appear to act as reservoirs for either aphids or parasitoids, as there was little overlap in the community composition of either, but for wheat there was much similarity. This is likely due to the presence of similar host plants within field edges and the neighbouring crop, enabling the same aphid species to persist within both areas. Diaeretiella rapae (M'Intosh) was the most common parasitoid across our study, particularly in canola, yet was present only in low abundance at field edges. The most common parasitoid in wheat fields was Aphidius matricariae (Haliday), with field edges likely acting as a reservoir for this species. Secondary parasitoid numbers were consistently low across our study. Differences in parasitoid species composition are discussed in relation to crop type, inter-field variation, and aphid host. The results highlight potential focal management areas and parasitoids that could help control aphid pests within grain crops.

Project description:Insects use endogenous mechanisms and infection with protective symbionts to thwart attacks from natural enemies. Defenses that target specific enemies, however, potentially mediate competition between rivals and thereby impact community composition. Following its introduction to North America to control pea aphids (Acyrthosiphon pisum), the parasitoid Aphidius ervi competitively displaced other parasitoids, except for the native Praon pequodorum. The pea aphid exhibits tremendous clonal variation in resistance to A. ervi, primarily through infection with the heritable bacterial symbiont Hamiltonella defensa, although some symbiont-free aphid genotypes encode endogenous resistance. Interestingly, H. defensa strains and aphid genotypes that protect against A. ervi, provide no protection against the closely related, P. pequodorum. Given the specificity of aphid defenses, we hypothesized that aphid resistance traits may contribute to the continued persistence of P. pequodorum. We conducted multiparasitism assays to determine whether aphid resistance traits mediate internal competition between these two solitary parasitoid species, but found this was not the case; P. pequodorum was the successful internal competitor across lines varying in susceptibility to A. ervi. Next, to determine whether resistance traits influence competitive interactions resulting in the stable persistence of P. pequodorum, we established replicated cages varying in the proportion of resistant aphids and recorded successful parasitism for each wasp species over time. As expected, A. ervi outcompeted P. pequodorum in cages containing only susceptible aphids. However, P. pequodorum not only persisted, but was the superior competitor in populations containing any proportion (20-100%) of resistant aphids (20-100%). Smaller scale, better replicated competition cage studies corroborated this finding, and no-competition and behavioral assays provide insight into the processes mediating competition. Genetic variation, including that acquired via infection with protective symbionts, may provide a supply of hosts susceptible only to particular enemies, mediating competition with effects on community richness and stability.

Dataset Information

Culture of an aphid heritable symbiont demonstrates its direct role in defence against parasitoids.

Publications

Culture of an aphid heritable symbiont demonstrates its direct role in defence against parasitoids.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets