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

Brandt, Jayce W.; Chevignon, Germain; Oliver, Kerry M.; Strand, Michael R.

doi:10.1098/rspb.2017.1925

Cited by 85 publications

(88 citation statements)

References 54 publications

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“…The primary mechanism of resistance against Braconid wasps in the pea aphid, Acyrthosiphon pisum (Harris), has been attributed to the Acyrthosiphon pisum Secondary Endosymbiont (APSE) bacteriophage that is frequently associated with H. defensa (Moran et al, 2005;Degnan & Moran, 2008a,b;Oliver et al, 2009). Phage-derived factors have been reported to arrest the development of wasp embryos (Brandt et al, 2017). By contrast, resistance of the peach-potato aphid, Myzus persicae (Sulzer), to Braconid wasps was associated with the facultative endosymbiont R. insecticola (von Burg et al, 2008;Vorburger et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

The price of protection: a defensive endosymbiont impairs nymph growth in the bird cherry‐oat aphid, Rhopalosiphum padi

et al. 2018

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Bacterial endosymbionts have enabled aphids to adapt to a range of stressors, but their effects in many aphid species remain to be established. The bird cherry-oat aphid, Rhopalosiphum padi (Linnaeus), is an important pest of cereals worldwide and has been reported to form symbiotic associations with Serratia symbiotica and Sitobion miscanthi L-type symbiont endobacteria, although the resulting aphid phenotype has not been described. This study presents the first report of R. padi infection with the facultative bacterial endosymbiont Hamiltonella defensa. Individuals of R. padi were sampled from populations in Eastern Scotland, UK, and shown to represent seven R. padi genotypes based on the size of polymorphic microsatellite markers; two of these genotypes harbored H. defensa. In parasitism assays, survival of H. defensa-infected nymphs following attack by the parasitoid wasp Aphidius colemani (Viereck) was 5 fold higher than for uninfected nymphs. Aphid genotype was a major determinant of aphid performance on two Hordeum species, a modern cultivar of barley H. vulgare and a wild relative H. spontaneum, although aphids infected with H. defensa showed 16% lower nymph mass gain on the partially resistant wild relative compared with uninfected individuals. These findings suggest that deploying resistance traits in barley will favor the fittest R. padi genotypes, but symbiont-infected individuals will be favored when parasitoids are abundant, although these aphids will not achieve optimal performance on a poor quality host plant.

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Section: Introductionmentioning

confidence: 99%

The price of protection: a defensive endosymbiont impairs nymph growth in the bird cherry‐oat aphid, Rhopalosiphum padi

et al. 2018

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“…Apart from the physical mechanisms and classical innate immune system, there is increasing evidence that insects form intimate partnerships with mutualistic bacteria that protect them against viruses, pathogenic bacteria, parasites, fungi and parasitoids (Bian, Xu, Lu, Xie, & Xi, 2010;Dong, Manfredini, & Dimopoulos, 2009;Flórez, Biedermann, Engl, & Kaltenpoth, 2015;Koch & Schmid-Hempel, 2011;Scarborough, Ferrari, & Godfray, 2005;Teixeira, Ferreira, & Ashburner, 2008). Mechanisms deployed by defensive mutualists for host protection include competing with antagonists for limited host resources (Herren et al, 2014;Paredes, Herren, Schüpfer, & Lemaitre, 2016), production of inhibitory substances such as toxins or antibiotics (Brandt, Chevignon, Oliver, & Strand, 2017;Flórez et al, 2017;Hamilton, Peng, Boulanger, & Perlman, 2015;Kaltenpoth, Göttler, Herzner, & Strohm, 2005;Kroiss et al, 2010), priming or maturation of the host immune system (Emery, Schmidt, & Engel, 2017;Kim et al, 2015;Konrad et al, 2012;Weiss, Maltz, & Aksoy, 2012;Weiss, Wang, & Aksoy, 2011) and improvement of host vigour by modulating nutrient allocation, growth rate or behaviour (Gerardo & Parker, 2014). Additionally, host-symbiont-pathogen interactions can facilitate the evolution of reduced pathogen virulence (Ford, Kao, Williams, & King, 2016;Read, 1994), mitigating detrimental fitness effects on the host.…”

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confidence: 99%

The cotton stainer's gut microbiota suppresses infection of a cotransmitted trypanosomatid parasite

2018

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The evolutionary and ecological success of many insects is attributed to mutualistic partnerships with bacteria that confer hosts with novel traits including food digestion, nutrient supplementation, detoxification of harmful compounds and defence against natural enemies. Dysdercus fasciatus firebugs (Hemiptera: Pyrrhocoridae), commonly known as cotton stainers, possess a simple but distinctive gut bacterial community including B vitamin-supplementing Coriobacteriaceae symbionts. In addition, their guts are often infested with the intestinal trypanosomatid parasite Leptomonas pyrrhocoris (Kinetoplastida: Trypanosomatidae). In this study, using experimental bioassays and fluorescence in situ hybridization (FISH), we report on the protective role of the D. fasciatus gut bacteria against L. pyrrhocoris. We artificially infected 2nd instars of dysbiotic and symbiotic insects with a parasite culture and measured parasite titres, developmental time and survival rates. Our results show that L. pyrrhocoris infection increases developmental time and slightly modifies the quantitative composition of the gut microbiota. More importantly, we found significantly higher parasite titres and a tendency towards lower survival rates in parasite-infected dysbiotic insects compared to symbiotic controls, indicating that the gut bacteria successfully interfere with the establishment or proliferation of L. pyrrhocoris. The colonization of symbiotic bacteria on the peritrophic matrix along the gut wall, as revealed by FISH, likely acts as a barrier blocking parasite attachment or entry into the hemolymph. Our findings show that in addition to being nutritionally important, D. fasciatus' gut bacteria complement the host's immune system in preventing parasite invasions and that a stable gut microbial community is integral for the host's health.

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“…More relevant may be that the protection against parasitoids conferred by H. defensa appears to have a different mechanistic basis than that conferred by R5.15. It is possible that the APSE-encoded factors, presumably toxins (Moran et al, 2005a), that have been shown to be causally involved in H. defensa-mediated disruption of parasitoid development (Brandt et al, 2017), will also cause some 'collateral damage' to the host. This APSE phage is not present in the genome of R. insecticola strain R5.15 (Hansen et al, 2012).…”

Section: Discussionmentioning

confidence: 99%

Estimating costs of aphid resistance to parasitoids conferred by a protective strain of the bacterial endosymbiont Regiella insecticola

Jamin

Vorburger

2019

Entomologia Exp Applicata

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Heritable bacterial endosymbionts are common in aphids (Hemiptera: Aphididae), and they can influence ecologically important traits of their hosts. It is generally assumed that their persistence in a population is dependent on a balance between the costs and benefits they confer. A good example is Hamiltonella defensa Moran et al., a facultative symbiont that provides a benefit by strongly increasing aphid resistance to parasitoid wasps, but becomes costly to the host in the absence of parasitoids. Regiella insecticola Moran et al. is another common symbiont of aphids and generally does not influence resistance to parasitoids. In the green peach aphid, Myzus persicae (Sulzer), however, one strain (R5.15) was discovered that behaves like H. defensa in that it provides strong protection against parasitoid wasps. Here we compare R5.15‐infected and uninfected lines of three M. persicae clones to test whether this protective symbiont is costly as well, i.e., whether it has any negative effects on aphid life‐history traits. Furthermore, we transferred R5.15 to two other aphid species, the pea aphid, Acyrthosiphon pisum (Harris), and the black bean aphid, Aphis fabae Scopoli, where this strain is also protective against parasitoids and where we could compare its effects with those of additional, non‐protective strains of R. insecticola. Negative effects of R5.15 on host survival and lifetime reproduction were limited and frequently non‐significant, and these effects were comparable or in one case weaker than those of R. insecticola strains that are not protective against parasitoid wasps. Unless the benefit of protection is counteracted by detrimental effects on traits that were not considered in this study, R. insecticola strain R5.15 should have a high potential to spread in aphid populations.

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

Cited by 85 publications

References 54 publications

The price of protection: a defensive endosymbiont impairs nymph growth in the bird cherry‐oat aphid, Rhopalosiphum padi

The price of protection: a defensive endosymbiont impairs nymph growth in the bird cherry‐oat aphid, Rhopalosiphum padi

The cotton stainer's gut microbiota suppresses infection of a cotransmitted trypanosomatid parasite

Estimating costs of aphid resistance to parasitoids conferred by a protective strain of the bacterial endosymbiont Regiella insecticola

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