Buchnera has changed flatmate but the repeated replacement of co‐obligate symbionts is not associated with the ecological expansions of their aphid hosts

Abstract

Symbiotic associations with bacteria have facilitated important evolutionary transitions in insects and resulted in long-term obligate interactions. Recent evidence suggests that these associations are not always evolutionarily stable and that symbiont replacement, and/or supplementation of an obligate symbiosis by an additional bacterium, has occurred during the history of many insect groups. Yet, the factors favouring one symbiont over another in this evolutionary dynamic are not well understood; progress has been hindered by our incomplete understanding of the distribution of symbionts across phylogenetic and ecological contexts. While many aphids are engaged into an obligate symbiosis with a single Gammaproteobacterium, Buchnera aphidicola, in species of the Lachninae subfamily, this relationship has evolved into a 'ménage à trois', in which Buchnera is complemented by a cosymbiont, usually Serratia symbiotica. Using deep sequencing of 16S rRNA bacterial genes from 128 species of Cinara (the most diverse Lachninae genus), we reveal a highly dynamic dual symbiotic system in this aphid lineage. Most species host both Serratia and Buchnera but, in several clades, endosymbionts related to Sodalis, Erwinia or an unnamed member of the Enterobacteriaceae have replaced Serratia. Endosymbiont genome sequences from four aphid species confirm that these coresident symbionts fulfil essential metabolic functions not ensured by Buchnera. We further demonstrate through comparative phylogenetic analyses that cosymbiont replacement is not associated with the adaptation of aphids to new ecological conditions. We propose that symbiont succession was driven by factors intrinsic to the phenomenon of endosymbiosis, such as rapid genome deterioration or competitive interactions between bacteria with similar metabolic capabilities.

A Freeloader? The Highly Eroded Yet Large Genome of the Serratia symbiotica Symbiont of Cinara strobi

“…As members of the Lachninae subfamily, Cinara aphids depend on both Buchnera and an additional symbiont for the supply of essential nutrients, namely EAAs and B-vitamins (Lamelas et al. 2011; Manzano-Marín and Latorre 2014; Meseguer et al. 2017).…”

“…This is seen in different mono- and di-symbiotic systems observed in weevils (Anbutsu et al. 2017), aphids (Vogel and Moran 2013; Meseguer et al. 2017; Chong and Moran 2018), mealybugs (Husnik and McCutcheon 2016; Szabó et al.…”

“…This binning process confirmed the presence of the previously reported putative co-obligate symbionts (Jousselin et al. 2016; Meseguer et al. 2017) ( Buchnera aphidicola and a Sodalis sp.)…”

Microbial community structure reveals instability of nutritional symbiosis during the evolutionary radiation of Amblyomma ticks

“…Vertical transmission actually locks the different symbionts together as co-infection, favouring the evolution of cooperation and dependence between symbionts. The functions of ancestral beneficial symbionts may be complemented by recently acquired cosymbionts and their coexistence can be ultimately stable over millions of years (Meseguer et al, 2017). New beneficial symbionts often originate from microbes that are abundant in the host environment, potentially including entomopathogens, parasites vectored by arthropods or other maternally inherited symbionts, primarily facultative (i.e., not essential) for host survival (Koga & Moran, 2014;Matsuura et al, 2018;McCutcheon et al, 2019;Sachs, Skophammer, & Regus, 2011).…”

Can social partnerships influence the microbiome? Insights from ant farmers and their trophobiont mutualists

“…To successfully access new habitats and resources, however, partnerships need to be reliable (Chomicki, Janda, & Renner, 2017;Meseguer et al, 2017;Mueller, Mikheyev, Solomon, & Cooper, 2011;Simonsen, Dinnage, Barrett, Prober, & Thrall, 2017;Sudakaran, Salem, Kost, & Kaltenpoth, 2012). Especially in cases where microbes do not become physically integrated with their hosts, such as farming mutualisms, environmental context plays a major role in the availability and suitability of particular microbial consortiums (Kaltenpoth et al, 2014;McFall-Ngai, 2008;Poulsen, Fernandez-Marin, Currie, & Boomsma, 2009).…”