Genomic erosion and extensive horizontal gene transfer in gut-associated Acetobacteraceae

Abstract

Background Symbiotic relationships between animals and bacteria have profound impacts on the evolutionary trajectories of each partner. Animals and gut bacteria engage in a variety of relationships, occasionally persisting over evolutionary timescales. Ants are a diverse group of animals that engage in many types of associations with taxonomically distinct groups of bacterial associates. Here, we bring into culture and characterize two closely-related strains of gut associated Acetobacteraceae (AAB) of the red carpenter ant, Camponotus chromaiodes . Results Genome sequencing, assembly, and annotation of both strains delineate stark patterns of genomic erosion and sequence divergence in gut associated AAB. We found widespread horizontal gene transfer (HGT) in these bacterial associates and report elevated gene acquisition associated with energy production and conversion, amino acid and coenzyme transport and metabolism, defense mechanisms, and lysine export. Both strains have acquired the complete NADH-quinone oxidoreductase complex, plausibly from an Enterobacteriaceae origin, likely facilitating energy production under diverse conditions. Conservation of several lysine biosynthetic and salvage pathways and accumulation of lysine export genes via HGT implicate L-lysine supplementation by both strains as a potential functional benefit for the host. These trends are contrasted by genome-wide erosion of several amino acid biosynthetic pathways and pathways in central metabolism. We perform phylogenomic analyses on both strains as well as several free living and host associated AAB. Based on their monophyly and deep divergence from other AAB, these C. chromaiodes gut associates may represent a novel genus. Together, our results demonstrate how extensive horizontal transfer between gut associates along with genome-wide deletions leads to mosaic metabolic pathways . More broadly, these patterns demonstrate that HGT and genomic erosion shape metabolic capabilities of persistent gut associates and influence their genomic evolution. Conclusions Using comparative genomics, our study reveals substantial changes in genomic content in persistent associates of the insect gastrointestinal tract and provides evidence for the evolutionary pressures inherent to this environment. We describe patterns of genomic erosion and horizontal acquisition that result in mosaic metabolic pathways. Accordingly, the phylogenetic position of both strains of these associates form a divergent, monophyletic clade sister to gut associates of honey bees and more distantly to Gluconobacter. Electronic supplementary material The online version of this article (10.1186/s12864-019-5844-5) contains supplementary material, which is available to authorized users.

Oecophyllibacter saccharovoransgen. nov. sp. nov., a bacterial symbiont of the weaver antOecophylla smaragdina

“…We believe that the small genome size is a result of genome reduction after participating in long term symbiotic relationship with the host ant species, O. smaragdina. Similar phenomenon of genome reduction had been reported in gut associated Acetobacteraceae of red carpenter ant [14] and Asaia endosymbionts of mosquitoes [15].…”

“…These AAB are known to survive acidic environment in insect guts and tolerate sugar-rich diets of the host [13]. It is also noteworthy that long term symbiosis of these AAB with different insect hosts resulted in significantly reduced size and gene content of their genomes [14,15].…”

Formicine ants swallow their highly acidic poison for gut microbial selection and control

“…Apart from specialized intracellular endosymbionts associated with the midgut in the ant tribe Camponotini (Degnan et al, 2004, Feldhaar et al, 2007, Russell et al, 2017, Williams and Wernegreen, 2015), formicine ant species have only low abundances of microbial associates in their gut lumen but carry members of the bacterial family Acetobacteracea as a major part of their gut microbiota (Brown and Wernegreen, 2016, Chua et al, 2018, He et al, 2011, Ivens et al, 2018). Some formicine gut associated Acetobacteracea show signs of genomic and metabolic adaptations to their host environment indicating coevolution (Brown and Wernegreen, 2019). But the recurrent presence of Acetobacteracea in the gut of formicine ants potentially also reflects direct transmission of bacteria among individuals, selective uptake on the part of the ants, specific adaptation for colonizing ant guts on the part of the bacteria, or some combination of all three (Engel and Moran, 2013).…”

Acetobacteraceae in the honey bee gut comprise two distant clades with diverging metabolism and ecological niches

“…CoA to 2-oxoglutarate (four steps). Several Acetobacteraceae have been reported to 535 harbor partial or modified TCA cycles, especially those that utilize oxidative 536 fermentation to gain energy (Brown and Wernegreen 2019;Mullins, et al 2008). 537…”