Bacterial microbiota associated with ants of the genus Tetraponera

Abstract

Tropical arboreal ants mainly feed as 'secondary herbivores', relying mostly on nitrogen-poor homopteran exudates as food. It has been speculated that this nitrogen-limitation of their diet may be overcome by nutritional upgrading with the help of symbiotic bacteria. We examined the bacterial diversity associated with several representatives of three species groups of the arboreal ant genus Tetraponera based on genes encoding 16S rRNA, citrate synthase and a structural protein of the dinitrogenase complex ( nifH ). The bacterial microflora showed group-specificity, suggesting long-term association between ants and bacteria. In all specimens of four species of the nigra group, we detected bacteria closely related to Bartonella (order Rhizobiales). Ants of the allaborans group harboured bacteria belonging to the enterobacteria. In Tetraponera pilosa of the third species group, we found the enterobacterium Pantoea agglomerans . In spite of the different phylogenetic affiliation of the bacteria identified in the three species groups, the presence of nifH in most species suggests a role in nitrogen metabolism of the bacterial microbiota. We also detected a high infection rate with the intracellular bacterium Wolbachia in all Tetraponera species groups. Besides the widespread bacteria found in Tetraponera , we discovered a diverse group of bacteria represented by single sequences.

Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants

“…Specifically, 75% (14/19) of the ants harboring Rhizobiales [including Cataulacus (one species), Cephalotes (four species), Dolichoderus spp. (seven colonies), Procryptocerus batesi, and Tetraponera attenuata] belonged to clades of known exudate-feeding arboreal ants that have previously been shown to harbor gut bacteria (16,17,(22)(23)(24). Because stable isotope measures had previously classified relatives of these hosts as herbivores (30,31), our findings suggested a relationship between trophic level and the distribution of these symbionts.…”

“…Nitrogen fixation has previously been proposed as a mechanism for dietary supplementation by bacterial symbionts (16). To examine this possibility, we screened for bacterial nifH genes in herbivorous ants.…”

“…The nifH gene encodes the dinitrogenase reductase subunit of the nitrogen-fixing nitrogenase enzyme, which converts atmospheric N 2 into NH 3 , a form of nitrogen that can be modified for use by eukaryotes. Stoll and colleagues first detected nifH sequences in ants from the genera Echinopla, Dolichoderus, and Tetraponera (16). Focusing on ants that hosted Rhizobiales, we amplified and sequenced nifH genes from a broader range of herbivorous ants, including Cephalotes, Dolichoderus, Procryptocerus, and Tetramorium species (SI and Table S2).…”

“…Throughout the course of their 115-168 million year history (7,8), these diverse and ecologically dominant insects have repeatedly evolved symbiotic relationships with sap-feeding insects (9), plants (10), and microbes (11,12,13), including nitrogen-recycling and upgrading Blochmannia species harbored by ants from the Camponotini (carpenter ants) (14,15). With only a few exceptions outside of this group (16)(17)(18)(19)(20) and the tribe Attini (13), we know little about the identities and significance of bacteria across Ͼ12,000 described ant species. However, researchers have recently hypothesized nutritional roles for microbes in a number of ants (21), suggesting that bacteria have shaped the evolution of ant diets.…”

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“…Other ants harbour extracellular bacteria in their hindguts, which are assumed to recycle nitrogenous waste and thus nutritionally upgrade the diet of their host (reviewed by Cook & Davidson 2006). By associating with bacteria, these ants, although capable of occasionally obtaining protein through scavenging or predation, gain an important advantage by having the ability to subsist on nitrogen-poor diets such as plant exudates and honeydew without experiencing protein deficiencies (Davidson et al 2003;Stoll et al 2007;Russell et al 2010). Similarly, many cockroaches, which are also typical omnivores, harbour intracellular bacteria (Blattabacterium sp.…”