A facultative endosymbiont in aphids can provide diverse ecological benefits

Abstract

Ecologically important traits of insects are often affected by facultative bacterial endosymbionts. This is best studied in the pea aphid Acyrthosiphon pisum, which is frequently infected by one or more of eight facultative symbiont species. Many of these symbiont species have been shown to provide one ecological benefit, but we have little understanding of the range of effects that a single strain can have. Here, we describe the phenotypes conferred by three strains of the recently discovered bacterium known as X‐type (Enterobacteriaceae), each in their original aphid genotype which also carries a Spiroplasma symbiont. All comparisons are made between aphids that are coinfected with Spiroplasma and X‐type and aphids of the same genotype that harbour only Spiroplasma. We show that in all cases, infection with X‐type protects aphids from the lethal fungal pathogen Pandora neoaphidis, and in two cases, resistance to the parasitoid Aphidius ervi also increases. X‐type can additionally affect aphid stress responses – the presence of X‐type increased reproduction after the aphids were heat‐stressed. Two of the three strains of X‐type are able to provide all of these benefits. Under benign conditions, the aphids tended to suffer from reduced fecundity when harbouring X‐type, a mechanism that might maintain intermediate frequencies in field populations. These findings highlight that a single strain of a facultative endosymbiont has the potential to provide diverse benefits to its aphid host.

Aphid Heritable Symbiont Exploits Defensive Mutualism

“…Based on these findings, we may expect that superinfections involving X-type plus H. defensa will be more common in warmer regions or seasons, although the loss of H. defensa-mediated resistance to parasitism at warmer temperatures (31, 33) obscures this hypothesis. Our results contrast with a previous study finding that European pea aphids superinfected with X-type and Spiroplasma showed decreased susceptibility to numerous stressors relative to those infected with Spiroplasma only (39). Given that this previous study did not isolate X-type single infections and that Spiroplamsa's only associated benefit is fungal protection (24), indirect effects may account for the enhanced protection in superinfected hosts.…”

“…One common HFS, X-type, has been implicated in providing thermal tolerance and enhancing protection against parasitoid wasps and fungal pathogens (25,39). X-type is unusual among pea aphid HFS, as it occurs primarily as a superinfection with a second symbiont, H. defensa (8; this study); however, no studies have disentangled the impact of X-type on the aphid protective phenotype in single-infection and superinfection contexts.…”

“…In all three of these cases (X, H, and XH) reductions in sporulation were small relative to that observed for aphids infected with R. insecticola (Fig. 4) 29.55 and P Յ 0.0001 [24,39]). HFS-infected lines also showed increased host mortality after pathogen exposure, which may be responsible for the observed reduction in sporulation ( No clear indication of antagonistic interactions between superinfecting HFS based on estimates of within-aphid symbiont abundance.…”

“…However, several studies with aphids, including pea aphids, show that symbiont-based protection against parasitoids can be specialized to particular parasitoid species (34)(35)(36)(37), rendering it possible that X-type provides protection specifically against the only other parasitoid, Praon pequodorum, commonly attacking the pea aphid in North America (38). In European pea aphids, some X-type strains have been implicated in providing protection from thermal stress, as well as challenges by the wasp A. ervi and the fungal pathogen P. neoaphidis (39). In this previous study, X-type could not be isolated from the superinfecting symbiont Spiroplasma, but lines with X-type and Spiroplasma generally received more protection than lines with only Spiroplasma, which has also been shown to provide protection against P. neoaphidis (24).…”

The holobiont concept: the case of xylophagous termites and cockroaches

“…>> Approximately here, Figure 2>> Although many microorganism-insect associations are based on nutrient and metabolite exchange, such as P-symbionts Buchnera, Blattabacterium, etc., there is evidence of the involvement of symbionts in other functions, especially those related with S-symbionts such as protection from fungal pathogens [aphids with X-type enterobacteria) (Heyworth and Ferrari 2015)] and from heat damage [aphids carrying "Candidatus Hamiltonella defensa" or "Candidatus Regionella insecticola" better tolerate high temperatures (Rusell and Moran 2006)]. Other examples of host protection from predators, pathogens and parasites include the bacterial symbiont of Paederus beetles, which produces a polyketide toxin that protects the insect larvae against predators such as the wolf spider (Kellner and Dettner 1996).…”