Ubiquity of the SymbiontSerratia symbioticain the Aphid Natural Environment: Distribution, Diversity and Evolution at a Multitrophic Level

Abstract

Bacterial symbioses are significant drivers of insect evolutionary ecology. However, despite recent findings that these associations can emerge from environmentally derived bacterial precursors, there is still little information on how these potential progenitors of insect symbionts circulates in the trophic systems. The aphid symbiont Serratia symbiotica represents a valuable model for deciphering evolutionary scenarios of bacterial acquisition by insects, as its diversity includes intracellular host-dependent strains as well as gut-associated strains that have retained some ability to live independently of their hosts and circulate in plant phloem sap. These strains represent a potential reservoir for the emergence of new and more intimate symbioses. Here, we conducted a field study to examine the distribution and diversity of S. symbiotica found in aphid populations, as well as in different compartments of their surrounding environment. A total of 250 aphid colonies, 203 associated insects, and 161 plant samples associated with aphid colonies were screened for S. symbiotica. Twenty percent of aphids were infected with S. symbiotica, and the symbiont includes a wide diversity of strains with varied tissue tropism corresponding to different lifestyle. We also showed that the prevalence of S. symbiotica is influenced by seasonal temperatures. For the first time, we found that S. symbiotica was present in non aphid species and in host plants, and that the prevalence of the bacterium in these samples was higher when associated aphid colonies were infected. Furthermore, phylogenetic analyses suggest the existence of horizontal transfers between the different trophic levels examined. These results provide a completely new picture of the ubiquity of an insect symbiont in nature. They suggest that ecological interactions promote the dissemination of strains that are still free-living and poorly specialized, and for which plants are a proabable reservoir for the acquisition of new bacterial partners in insects.

Secondary symbionts affect aphid fitness and the titer of primary symbiont

“…Together, our study contributes to symbiont function research by revealing the effect of S-symbiont on aphid ecology and the correlation with symbiont titers. Pertinent studies have found that the prevalence of S-symbionts in aphids may be influenced by seasonal temperatures, host plants, parasitoids, and aphid species (Vorburger and Rouchet, 2016;Guidolin and Consoli, 2017;Pons et al, 2022). According to our rough statistics, the prevalence of Hamiltonella defensa or Regiella insecticola was 12.32% (17/138) and 14.40% (19/132) at the location where we collected them.…”

Frequent Drivers, Occasional Passengers: Signals of Symbiont-Driven Seasonal Adaptation and Hitchhiking in the Pea Aphid, Acyrthosiphon pisum

“…However, we do not yet find strong cause to invoke this mode of transfer as a driver of large, rapid pea aphid symbiont dynamics. Indeed, while work in other aphids suggests the likelihood for such movement [84,118], research on some pea aphid symbionts (Serratia, Hamiltonella, Rickettsia) has not uncovered frequent movement through such routes [129,130]. Nevertheless, recent discoveries of plant-mediated movement for slightly divergent Serratia symbionts in other aphids [131], suggest a need for more accurate estimates on the rates of horizontal transfer, and for a broader effort to identify the avenues through which it occurs.…”

“…Phylogenetic analysis of Serratia symbiotica from pea aphids suggest that these symbionts are most closely related to other heritable facultative symbionts from varying aphids. This lineage is, in turn, related to Serratia clades with broader distributions across aphids, other insects, and the plant environment [84], and to (co-)obligate Serratia symbionts of Lachninae aphids [85].…”

Episyrphus balteatus symbiont variation across developmental stages, living states, two sexes, and potential horizontal transmission from prey or environment

“…Such vertical transfer mode promotes the strong stability for the symbiosis maintaining of microbiota and insects, favoring the evolution of microbially mediated effects that improve host insect fitness (Russell and Moran, 2005). In addition, plentiful evidence indicates that symbionts can also undergo horizontal transfer among different insects or be acquired directly from the environment or diets (Hosokawa et al, 2016;Tzuri et al, 2021;Du et al, 2022;Pons et al, 2022), and acquisition of novel symbiont strains for the insects via horizontal transmission can provide fitness benefits to the host, with significant ecological and evolutionary consequences (Łukasik et al, 2015). In contrast to considerable studies about microbiota structure and diversity in aphids (Guo et al, 2017), bees (Steffan et al, 2023), flies (Noman et al, 2020), bugs (Gonella et al, 2020), and beetles (Salem and Kaltenpoth, 2022), knowledge about symbionts in hoverflies was rare.…”

“…To date, plentiful studies exploring genome (Yuan et al, 2022), reproduction (Putra et al, 2009), behavior (Vosteen et al, 2018), and phylogenetic relationships (Wong et al, 2023) have been performed on various hoverfly species. However, studies related to the community and sources of symbionts in hoverflies are few, except for only several bacteria gene identification reports from Pons (Pons et al, 2022) and Sánchez-Galván (Sánchez-Galván et al, 2017). Sánchez-Galván identified three bacteria species genes in the gut of the hoverfly Mallota dusmeti via PCR amplification (Sánchez-Galván et al, 2017).…”