Deep divergence and rapid evolutionary rates in gut-associated Acetobacteraceae of ants.

Bryan P Brown,Jennifer J Wernegreen

doi:10.1186/s12866-016-0721-8

Abstract

BackgroundSymbiotic associations between gut microbiota and their animal hosts shape the evolutionary trajectories of both partners. The genomic consequences of these relationships are significantly influenced by a variety of factors, including niche localization, interaction potential, and symbiont transmission mode. In eusocial insect hosts, socially transmitted gut microbiota may represent an intermediate point between free living or environmentally acquired bacteria and those with strict host association and maternal transmission.ResultsWe characterized the bacterial communities associated with an abundant ant species, Camponotus chromaiodes. While many bacteria had sporadic distributions, some taxa were abundant and persistent within and across ant colonies. Specially, two Acetobacteraceae operational taxonomic units (OTUs; referred to as AAB1 and AAB2) were abundant and widespread across host samples. Dissection experiments confirmed that AAB1 and AAB2 occur in C. chromaiodes gut tracts. We explored the distribution and evolution of these Acetobacteraceae OTUs in more depth. We found that Camponotus hosts representing different species and geographical regions possess close relatives of the Acetobacteraceae OTUs detected in C. chromaiodes. Phylogenetic analysis revealed that AAB1 and AAB2 join other ant associates in a monophyletic clade. This clade consists of Acetobacteraceae from three ant tribes, including a third, basal lineage associated with Attine ants. This ant-specific AAB clade exhibits a significant acceleration of substitution rates at the 16S rDNA gene and elevated AT content. Substitutions along 16S rRNA in AAB1 and AAB2 result in ~10 % reduction in the predicted rRNA stability.ConclusionsCombined, these patterns in Camponotus-associated Acetobacteraceae resemble those found in cospeciating gut associates that are both socially and maternally transmitted. These associates may represent an intermediate point along an evolutionary trajectory manifest most extremely in symbionts with strict maternal transmission. Collectively, these results suggest that Acetobacteraceae may be a frequent and persistent gut associate in Camponotus species and perhaps other ant groups, and that its evolution is strongly impacted by this host association.Electronic supplementary materialThe online version of this article (doi:10.1186/s12866-016-0721-8) contains supplementary material, which is available to authorized users.

Highlights

Symbiotic associations between gut microbiota and their animal hosts shape the evolutionary trajectories of both partners
Two Acetobacteraceae (AAB) operational taxonomic unit (OTU) are abundant in the gaster microbiota of C. chromaiodes To characterize the microbiota of C. chromaiodes, sequencing of the V4 and V5 regions of 16S rDNA was performed using the Ion PGM instrument
Across the ant samples, pyrosequencing generated 343,834 total reads. These datasets were dominated by the intracellular bacteria Blochmannia and Wolbachia, both known to associate with Camponotus [31, 32]

Summary

Introduction

Symbiotic associations between gut microbiota and their animal hosts shape the evolutionary trajectories of both partners. Associations between gut bacteria and their hosts have had profound impacts on the evolutionary trajectories of both partners [1]. These interactions have facilitated the success of many animal groups by providing key benefits to the host, such as contributions to host nutrition in termites [2], immune defense in moths [3], kin recognition in Drosophila [4], and toxin production in the antlion [5]. Among bacteria, inhabiting an animal gut can have a range of genomic consequences These can include general adaptations that favor colonization of the gut environment and long-term signatures of coevolution with a specific host. In murine models, increased bacterial mutation rates have been demonstrated to facilitate colonization of the gut niche by expediting

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