Localization of bacterial communities within gut compartments across Cephalotes turtle ants.

Peter J Flynn,Catherine L D’Amelio,Shuang-Jiang Liu,Jon G Sanders,Corrie S Moreau,Jacob A Russell

doi:10.1128/aem.02803-20

Peter J Flynn, Catherine L D’Amelio + Show 4 more

Open Access

https://doi.org/10.1128/aem.02803-20

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Abstract

Microbial communities within the animal digestive tract often provide important functions for their hosts. The composition of eukaryotes' gut bacteria can be shaped by host diet, vertical bacterial transmission, and physiological variation within the digestive tract. In several ant taxa, recent findings have demonstrated that nitrogen provisioning by symbiotic bacteria makes up for deficiencies in herbivorous diets. Using 16S rRNA amplicon sequencing and qPCR, this study examined bacterial communities at a fine scale across one such animal group, the turtle ant genus Cephalotes We analyzed the composition and colonization density across four portions of the digestive tract to understand how bacterial diversity is structured across gut compartments, potentially allowing for specific metabolic functions of benefit to the host. In addition, we aimed to understand if caste differentiation or host relatedness influences the gut bacterial communities of Cephalotes ants. Microbial communities were found to vary strongly across Cephalotes gut compartments in ways that transcend both caste and host phylogeny. Despite this, caste and host phylogeny still have detectable effects. We demonstrated microbial community divergence across gut compartments, possibly due to the varying function of each gut compartment for digestion.IMPORTANCE Gut compartments play an important role in structuring the microbial community within individual ants. The gut chambers of the turtle ant digestive tract differ remarkably in symbiont abundance and diversity. Furthermore, caste type explains some variation in the microbiome composition. Finally, the evolutionary history of the Cephalotes species structures the microbiome in our study, which elucidates a trend in which related ants maintain related microbiomes, conceivably owing to co-speciation. Amazingly, gut compartment-specific signatures of microbial diversity, relative abundance, composition, and abundance have been conserved over Cephalotes evolutionary history, signifying that this symbiosis has been largely stable for over 50 million years.

Highlights

Microbial communities within the animal digestive tract often provide important functions for their hosts
Ileum, rectum, and gaster plots, we found that the C. texanus samples cluster together away from every other Cephalotes species, which form a nondistinct cluster in the gaster and midgut principal coordinate analysis (PCoA) plots (Fig. 6A and C) and a more Cephalotes species-specific cluster in the ileum and rectum PCoA plots (Fig. 6D and E)
While gut compartmentalization of microbes has been well studied in mammals and birds [46,47,48] and has been observed in insect groups such as termites [49] and beetles [50], few studies have documented specific microbial gut compartmentalization within ants. To understand if this pattern is common across Cephalotine ants, we examined the microbial community within each gut compartment in a variety of species spanning the Cephalotes phylogeny

Summary

Introduction

Microbial communities within the animal digestive tract often provide important functions for their hosts. The composition of eukaryotes’ gut bacteria can be shaped by host diet, vertical bacterial transmission, and physiological variation within the digestive tract. We analyzed the composition and colonization density across four portions of the digestive tract to understand how bacterial diversity is structured across gut compartments, potentially allowing for specific metabolic functions of benefit to the host. We aimed to understand if caste differentiation or host relatedness influences the gut bacterial communities of Cephalotes ants. Ants are an extremely successful clade of animals both in terms of their sheer biomass as well as their diversity, and their associated microbes play an important functional role for species of various dietary types. The benefits of the Blochmannia gut symbionts could be a reason for the evolutionary success of the Camponotini tribe [16]

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