Highly similar microbial communities are shared among related and trophically similar ant species

Abstract

Ants dominate many terrestrial ecosystems, yet we know little about their nutritional physiology and ecology. While traditionally viewed as predators and scavengers, recent isotopic studies revealed that many dominant ant species are functional herbivores. As with other insects with nitrogen-poor diets, it is hypothesized that these ants rely on symbiotic bacteria for nutritional supplementation. In this study, we used cloning and 16S sequencing to further characterize the bacterial flora of several herbivorous ants, while also examining the beta diversity of bacterial communities within and between ant species from different trophic levels. Through estimating phylogenetic overlap between these communities, we tested the hypothesis that ecologically or phylogenetically similar groups of ants harbor similar microbial flora. Our findings reveal: (i) clear differences in bacterial communities harbored by predatory and herbivorous ants; (ii) notable similarities among communities from distantly related herbivorous ants and (iii) similar communities shared by different predatory army ant species. Focusing on one herbivorous ant tribe, the Cephalotini, we detected five major bacterial taxa that likely represent the core microbiota. Metabolic functions of bacterial relatives suggest that these microbes may play roles in fixing, recycling, or upgrading nitrogen. Overall, our findings reveal that similar microbial communities are harbored by ants from similar trophic niches and, to a greater extent, by related ants from the same colonies, species, genera, and tribes. These trends hint at coevolved histories between ants and microbes, suggesting new possibilities for roles of bacteria in the evolution of both herbivores and carnivores from the ant family Formicidae.

Cephaloticoccus gen. nov., a new genus of ‘Verrucomicrobia’ containing two novel species isolated from Cephalotes ant guts

“…These symbionts are protected by a proventricular filter (Lanan et al, 2016), remain stable in laboratory-reared colonies and likely coevolved with their hosts (Sanders et al, 2014). 'Verrucomicrobia' belonging to the order Opitutales are consistently detected at high numbers in the ant midgut (Anderson et al, 2012;Hu et al, 2014;Lanan et al, 2016). As such, these vastly abundant Opitutales symbionts may play important contributory roles in host nutrition and disease resistance (Dillon & Dillon, 2004).…”

“…By using PCR amplification and DNA sequencing techniques, previous studies have shown that members of the 'Verrucomicrobia' constitute part of a stable, autochthonous community of symbionts maintained in the guts of Cephalotes 'turtle' ants (Anderson et al, 2012;Kautz et al, 2013;Russell et al, 2009). These symbionts are protected by a proventricular filter (Lanan et al, 2016), remain stable in laboratory-reared colonies and likely coevolved with their hosts (Sanders et al, 2014).…”

“…Strain CAG34 T was isolated from the guts of Cephalotes rohweri ants and strain CV41 T was isolated from the guts of Cephalotes varians. C. rohweri ants were collected from Tucson Mountain Park, Tucson, AZ, USA (32.23 N 111.12 W) in 2010 and reared in the laboratory as previously described (Anderson et al, 2012) until degutting. Wild C. varians ants were collected from hollow mangrove twigs from Crocodile Lake National Wildlife Refuge, Key Largo, FL, USA (25.29 N 80.31 W) in October 2012.…”

Ventosimonas gracilis gen. nov., sp. nov., a member of the Gammaproteobacteria isolated from Cephalotes varians ant guts representing a new family, Ventosimonadaceae fam. nov., within the order ‘Pseudomonadales’

“…Studies using PCR amplification and DNA sequencing techniques have revealed that Cephalotes ants harbor a core gut microbiota (Anderson et al, 2012;Hu et al, 2014;Kautz et al, 2013;Russell et al, 2009). Bacteria in this core microbiota consistently include members of the Burkholderiales, Rhizobiales, Xanthomonadales, Opitutales and Pseudomonadales phylotypes (Anderson et al, 2012;Hu et al, 2014;Russell et al, 2009), signifying their importance as stable, autochthonous members of the gut community (Hu et al, 2014;Sanders et al, 2014).…”

“…Studies using PCR amplification and DNA sequencing techniques have revealed that Cephalotes ants harbor a core gut microbiota (Anderson et al, 2012;Hu et al, 2014;Kautz et al, 2013;Russell et al, 2009). Bacteria in this core microbiota consistently include members of the Burkholderiales, Rhizobiales, Xanthomonadales, Opitutales and Pseudomonadales phylotypes (Anderson et al, 2012;Hu et al, 2014;Russell et al, 2009), signifying their importance as stable, autochthonous members of the gut community (Hu et al, 2014;Sanders et al, 2014). These symbionts are likely to have coevolved with their hosts over their evolutionary history (Sanders et al, 2014), and, as shown for symbionts in the termite (Brune & Ohkuma, 2011;Wertz et al, 2012;Wertz & Breznak, 2007b) and honeybee gut (Engel et al, 2012;Engel & Moran, 2013;Kwong & Moran, 2013), likely confer beneficial functions to host nutrition and disease resistance (Dillon & Dillon, 2004).…”