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

Abstract

Acacia-ant mutualists in the genus Pseudomyrmex nest obligately in acacia plants and, as we show through stable isotope analysis, feed at a remarkably low trophic level. Insects with diets such as these sometimes depend on bacterial symbionts for nutritional enrichment. We, therefore, examine the bacterial communities associated with acacia-ants in order to determine whether they host bacterial partners likely to contribute to their nutrition. Despite large differences in trophic position, acacia-ants and related species with generalized diets do not host distinct bacterial taxa. However, we find that a small number of previously undescribed bacterial taxa do differ in relative abundance between acacia-ants and generalists, including several Acetobacteraceae and Nocardiaceae lineages related to common insect associates. Comparisons with an herbivorous generalist, a parasite that feeds on acacias and a mutualistic species with a generalized diet show that trophic level is likely responsible for these small differences in bacterial community structure. While we did not experimentally test for a nutritional benefit to hosts of these bacterial lineages, metagenomic analysis reveals a Bartonella relative with an intact nitrogen-recycling pathway widespread across Pseudomyrmex mutualists and generalists. This taxon may be contributing to nitrogen enrichment of its ant hosts through urease activity and, concordant with an obligately host-associated lifestyle, appears to be experiencing genomewide relaxed selection. The lack of distinctiveness in bacterial communities across trophic level in this group of ants shows a remarkable ability to adjust to varied diets, possibly with assistance from these diverse ant-specific bacterial lineages.

Bacterial communities within Phengaris (Maculinea) alcon caterpillars are shifted following transition from solitary living to social parasitism of Myrmica ant colonies

“…Actinomycetales are known for their associations with leaf-cutter ants, growing on specialized structures and protecting their hosts against parasites and pathogens (Barke et al, 2010;Currie, Poulsen, Mendenhall, Boomsma, & Billen, 2006;Haeder, Wirth, Herz, & Spiteller, 2009;Mattoso, Moreira, & Samuels, 2012). Actinomycetes with antifungal properties have also been identified in Myrmica rugulosa (Kost et al, 2007), and are a core component of the microbiota in other ants that do not farm fungi, such as Pseudomyrmex species (Rubin, Kautz, Wray, & Moreau, 2018). However, these bacteria are not currently known to enhance digestion in ants or caterpillars.…”

Abdominal microbial communities in ants depend on colony membership rather than caste and are linked to colony productivity

“…These bacteria carry genes with enzymatic functions that the animal hosts would otherwise not have access to (Engel & Moran, ; Zilber‐Rosenberg & Rosenberg, ). A high diversity in gut bacterial communities exists between species, which are often tightly linked to an animal's lifestyle, especially its diet (Anderson et al, ; Ley et al, ; Rubin, Kautz, Wray, & Moreau, ). For instance, wood‐feeding termites harbor bacteria in their gut, which produce enzymes that aid in the digestion of their high‐cellulose food (Brune, ).…”

“…| 13451 SEGERS Et al. which are often tightly linked to an animal's lifestyle, especially its diet (Anderson et al, 2012;Ley et al, 2008;Rubin, Kautz, Wray, & Moreau, 2019). For instance, wood-feeding termites harbor bacteria in their gut, which produce enzymes that aid in the digestion of their high-cellulose food (Brune, 2014).…”

Convergence, constraint and the potential for mutualism between ants and gut microbes

“…As Sapountzis et al () note, future studies of higher‐attine lineages that independently recolonized South America will clarify the extent of the geographic and phylogenetic nature of these constraints. Moreover, although the higher attines that diversified in Middle America have higher gut bacterial densities than do other attines, even these species appear to have fewer gut bacteria than other, non‐attine ants whose gut bacteria confer known nutritional benefits (Rubin, Kautz, Wray, & Moreau, ; Sanders et al ).…”

“…Rubin et al () compared gut bacterial communities across 11 species of Pseudomyrmex , including four species of obligate acacia‐nesting ants and several dietary generalists, and between Pseudomyrmex and other arboreal ant genera. They report fewer gut bacteria in any of the 11 species of Pseudomyrmex , including the acacia ants, than in the herbivorous camponotines and cephalotines.…”