Buchnerahas 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 favoring 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 fulfill essential metabolic functions not ensured by Buchnera. We further demonstrate through comparative phylogenetic analyses that co-symbiont 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.

Happens in the best of subfamilies: establishment and repeated replacements of co‐obligate secondary endosymbionts within Lachninae aphids

“…Additionally, using a specific primer designed to target the 16S rRNA gene of the SLSS of Eulachnus spp. A similar approach has been recently been used to successfully detect symbionts associated to Cinara species Meseguer et al, 2016). Although we lacked enough specimens to perform FISH microscopy, we were able to amplify a sequence from a SLSS from a population of the closely related aphid species Cinara (Schizolachnus) pineti.…”

“…Known secondary symbionts of Lachninae differ in tissue tropism and cell shape (Buchner, 1953;Fukatsu and Ishikawa, 1998;Pyka-Fo sciak and Szklarzewicz, 2008;Michalik et al, 2014), as well as in phylogenetic origin (Russell et al, 2003;Lamelas et al, 2008;Burke et al, 2009;Jousselin et al, 2016;Meseguer et al, 2016). Although different bacterial taxa have been found associated to Lachninae aphids, many species of this subfamily have been systematically found associated with members of the bacterial genus Serratia, mainly Serratia symbiotica Russell et al 2003;Lamelas et al, 2008;Burke et al, 2009;Chen et al 2015;Jousselin et al, 2016) (for a summary see Table S1).…”

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, ). 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, ; Matsuura et al, ; McCutcheon et al, ; Sachs, Skophammer, & Regus, ).…”

Band‐aids for Buchnera and B vitamins for all

“…To better understand cosymbiosis in this group, Meseguer et al . () targeted 371 aphids from an estimated 128 Cinara species. They performed 16S rRNA amplicon sequencing to describe the resident microbiota, including replication within species to assess symbiont fixation (i.e.…”

“…But in this issue, Meseguer et al . () report on a different flavour of cosymbiosis among conifer‐feeding Cinara aphids.…”