Insects often harbour heritable symbionts that provide defence against specialized natural enemies, yet little is known about symbiont protection when hosts face simultaneous threats. In pea aphids (
- NSF-PAR ID:
- 10180162
- Date Published:
- Journal Name:
- Applied and Environmental Microbiology
- Volume:
- 86
- Issue:
- 5
- ISSN:
- 0099-2240
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Acyrthosiphon pisum ), the facultative endosymbiontHamiltonella defensa confers protection against the parasitoid,Aphidius ervi , andRegiella insecticola protects against aphid‐specific fungal pathogens, includingPandora neoaphidis . Here, we investigated whether these two common aphid symbionts protect against a specialized virusA .pisum virus (APV), and whether their antifungal and antiparasitoid services are impacted by APV infection. We found that APV imposed large fitness costs on symbiont‐free aphids and these costs were elevated in aphids also housingH .defensa . In contrast, APV titres were significantly reduced and costs to APV infection were largely eliminated in aphids withR .insecticola . To our knowledge,R .insecticola is the first aphid symbiont shown to protect against a viral pathogen, and only the second arthropod symbiont reported to do so. In contrast, APV infection did not impact the protective services of eitherR .insecticola orH .defensa . To better understand APV biology, we produced five genomes and examined transmission routes. We found that moderate rates of vertical transmission, combined with horizontal transfer through food plants, were the major route of APV spread, although lateral transfer by parasitoids also occurred. Transmission was unaffected by facultative symbionts. In summary, the presence and species identity of facultative symbionts resulted in highly divergent outcomes for aphids infected with APV, while not impacting defensive services that target other enemies. These findings add to the diverse phenotypes conferred by aphid symbionts, and to the growing body of work highlighting extensive variation in symbiont‐mediated interactions. -
Abstract Heritable symbionts are common in terrestrial arthropods and often provide beneficial services to hosts. Unlike obligate, nutritional symbionts that largely persist under strict host control within specialized host cells, heritable facultative symbionts exhibit large variation in within-host lifestyles and services rendered with many retaining the capacity to transition among roles. One enigmatic symbiont, Candidatus Fukatsuia symbiotica, frequently infects aphids with reported roles ranging from pathogen, defensive symbiont, mutualism exploiter and nutritional co-obligate symbiont. Here we used an in vitro culture-assisted protocol to sequence the genome of a facultative strain of Fukatsuia from pea aphids (Acyrthosiphon pisum). Phylogenetic and genomic comparisons indicate that Fukatsuia is an aerobic heterotroph, which together with Regiella insecticola and Hamiltonella defensa form a clade of heritable facultative symbionts within the Yersiniaceae (Enterobacteriales). These three heritable facultative symbionts largely share overlapping inventories of genes associated with housekeeping functions, metabolism, and nutrient acquisition, while varying in complements of mobile DNA. One unusual feature of Fukatsuia is its strong tendency to occur as a co-infection with H. defensa. However, the overall similarity of gene inventories among aphid heritable facultative symbionts suggest that metabolic complementarity is not the basis for co-infection, unless playing out on a H. defensa strain-specific basis. We also compared the pea aphid Fukatsuia with a strain from the aphid Cinara confinis (Lachninae) where it is reported to have transitioned to co-obligate status to support decaying Buchnera function. Overall the two genomes are very similar with no clear genomic signatures consistent with such a transition, which suggests co-obligate status in C. confinis was a recent event.more » « less
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Abstract Heritable, facultative symbionts are common in arthropods, often functioning in host defence. Despite moderately reduced genomes, facultative symbionts retain evolutionary potential through mobile genetic elements (MGEs). MGEs form the primary basis of strain‐level variation in genome content and architecture, and often correlate with variability in symbiont‐mediated phenotypes. In pea aphids (
Acyrthosiphon pisum ), strain‐level variation in the type of toxin‐encoding bacteriophages (APSEs) carried by the bacteriumHamiltonella defensa correlates with strength of defence against parasitoids. However, co‐inheritance creates difficulties for partitioning their relative contributions to aphid defence. Here we identified isolates ofH. defensa that were nearly identical except for APSE type. When holdingH. defensa genotype constant, protection levels corresponded to APSE virulence module type. Results further indicated that APSEs move repeatedly within someH. defensa clades providing a mechanism for rapid evolution in anti‐parasitoid defences. Strain variation inH. defensa also correlates with the presence of a second symbiontFukatsuia symbiotica . Predictions that nutritional interactions structured this coinfection were not supported by comparative genomics, but bacteriocin‐containing plasmids unique to co‐infecting strains may contribute to their common pairing. In conclusion, strain diversity, and joint capacities for horizontal transfer of MGEs and symbionts, are emergent players in the rapid evolution of arthropods. -
Abstract Ecologically relevant symbioses are widespread in terrestrial arthropods but based on recent findings these specialized interactions are likely to be especially vulnerable to climate warming. Importantly, empirical data and climate models indicate that warming is occurring asynchronously, with night‐time temperatures increasing faster than daytime temperatures. Daytime (DTW) and night‐time warming (NTW) may impact ectothermic animals and their interactions differently as DTW results in greater daily temperature variation and moves organisms nearer to their thermal limits, while NTW avoids thermal limits and may relieve constraints of cooler night‐time temperatures; a nuance that has largely been ignored in the literature.
In laboratory experiments, we investigated how the timing of warming influences a widespread defensive mutualism involving the pea aphid
Acyrthosiphon pisum , and its heritable symbiont,Hamiltonella defensa , which protects against an important natural enemy, the parasitic waspAphidius ervi .Three aphid sublines were experimentally created from single aphid genotype susceptible to
A. ervi : one line infected with a highly protectiveH. defensa strain, one infected with a moderately protective strain and one without any facultative symbiont. We examined aphid fitness in the presence and absence of parasitoids and when exposed to an average 2.5°C increase occurring across three warming scenarios (night‐time vs. daytime vs. uniform) relative to no‐warming controls.An increase of 2.5°C, as predicted to occur by the IPCC before 2100, was sufficient to disable the aphid defensive mutualism regardless of the timing of warming; a surprising result given that the daily maxima for control and NTW scenarios were identical. We also found that warming negatively impacted (a) symbiont‐mediated interactions between host and parasitoid more than symbiont‐free ones; (b) species interactions (host–parasitoid) more than each participant independently and (c) aphids more than parasitoids even though higher trophic levels are generally predicted to be more affected by warming.
Here we show that 2.5°C warming, regardless of timing, negatively impacted a common microbe‐mediated defensive mutualism. While this was a laboratory‐based study, results suggest that temperature increases predicted in the near‐term may disrupt the many ecological symbioses present in terrestrial ecosystems.
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Abstract Animal‐associated microbiomes are often comprised of structured, multispecies communities, with particular microbes showing trends of co‐occurrence or exclusion. Such structure suggests variable community stability, or variable costs and benefits—possibilities with implications for symbiont‐driven host adaptation. In this study, we performed systematic screening for maternally transmitted, facultative endosymbionts of the pea aphid,
Acyrthosiphon pisum . Sampling across six locales, with up to 5 years of collection in each, netted significant and consistent trends of community structure. Co‐infections betweenSerratia symbiotica andRickettsiella viridis were more common than expected, whileRickettsia and X‐type symbionts colonized aphids withHamiltonella defensa more often than expected.Spiroplasma co‐infected with other endosymbionts quite rarely, showing tendencies to colonize as a single species monoculture. Field estimates of maternal transmission rates help to explain our findings: whileSerratia andRickettsiella improved each other's transmission,Spiroplasma reduced transmission rates of co‐infecting endosymbionts. In summary, our findings show that North American pea aphids harbour recurring combinations of facultative endosymbionts. Common symbiont partners play distinct roles in pea aphid biology, suggesting the creation of “generalist” aphids receiving symbiont‐based defence against multiple ecological stressors. Multimodal selection, at the host level, may thus partially explain our results. But more conclusively, our findings show that within‐host microbe interactions, and their resulting impacts on transmission rates, are an important determinant of community structure. Widespread distributions of heritable symbionts across plants and invertebrates hint at the far‐reaching implications for these findings, and our work further shows the benefits of symbiosis research within a natural context.