Herbivorous turtle ants obtain essential nutrients from a conserved nitrogen-recycling gut microbiome

Abstract

Nitrogen acquisition is a major challenge for herbivorous animals, and the repeated origins of herbivory across the ants have raised expectations that nutritional symbionts have shaped their diversification. Direct evidence for N provisioning by internally housed symbionts is rare in animals; among the ants, it has been documented for just one lineage. In this study we dissect functional contributions by bacteria from a conserved, multi-partite gut symbiosis in herbivorous Cephalotes ants through in vivo experiments, metagenomics, and in vitro assays. Gut bacteria recycle urea, and likely uric acid, using recycled N to synthesize essential amino acids that are acquired by hosts in substantial quantities. Specialized core symbionts of 17 studied Cephalotes species encode the pathways directing these activities, and several recycle N in vitro. These findings point to a highly efficient N economy, and a nutritional mutualism preserved for millions of years through the derived behaviors and gut anatomy of Cephalotes ants.

Dietary specialization in mutualistic acacia‐ants affects relative abundance but not identity of host‐associated bacteria

“…These patterns are in contrast to what has been found in other groups of ants where diet specialization is correlated with a clear change in bacterial community composition (Anderson et al., ; Funaro et al., ; Hu et al., ; Łukasik et al., ; Russell et al., ; Sanders et al., ). There are several possible explanations for why acacia‐ants may not require similar shifts in microbial communities despite their large trophic shift.…”

“…Quantities of the bacterial 16S rRNA gene in the ant taxa examined using qPCR in adults and larvae. All Pseudomyrmex adults, including obligate mutualists, have significantly lower numbers of bacteria than both Camponotus and Cephalotes , the two genera with known beneficial bacterial symbionts (Feldhaar et al., ; Hu et al., ). Significance was determined by Wilcoxon rank‐sum tests with FDR correction ( p < 0.05) [Colour figure can be viewed at wileyonlinelibrary.com]…”

“…For example, the Blochmannia symbionts of carpenter ants in the genus Camponotus contribute to the nutrition of their hosts through nitrogen recycling and amino acid upgrading (Feldhaar et al., ) and Westeberhardia bacteria appear to provide tyrosine precursors to their host Cardiocondyla ants (Klein et al., ). More recently, species in the genus Cephalotes were shown to benefit from the nitrogen recycling capacity of their specialized microbial communities (Hu, Łukasik, Moreau, & Russell, ; Hu et al., ; Russell et al., ; Sanders et al., ). Bacteria in the Cephalotes gut degrade waste urea into ammonia and incorporate this recycled ammonia into glutamate that is then used in the synthesis of amino acids essential to the ant hosts (Hu et al., ).…”

“…More recently, species in the genus Cephalotes were shown to benefit from the nitrogen recycling capacity of their specialized microbial communities (Hu, Łukasik, Moreau, & Russell, ; Hu et al., ; Russell et al., ; Sanders et al., ). Bacteria in the Cephalotes gut degrade waste urea into ammonia and incorporate this recycled ammonia into glutamate that is then used in the synthesis of amino acids essential to the ant hosts (Hu et al., ). This nitrogen recycling capability via a complete urease pathway is also present in Candidatus Tokpelaia symbionts of ants in the predatory genus Harpegnathos (Neuvonen et al., ) and the herbivorous genus Dolichoderus (Bisch et al., ).…”

“…Symbionts with such nitrogen‐recycling capability may be common across the ant family. While the potential for direct nitrogen fixation by bacteria exists in Acromyrmex (Sapountzis et al., ), this process has yet to be demonstrated by internally housed symbionts in any ant (Hu et al., ).…”