Bacterial microbiomes from vertically transmitted fungal inocula of the leaf‐cutting ant Atta texana

Abstract

2 Originality-Significance Statement: An ongoing debate is whether beneficial microbiomes can be inherited from parent to offspring generations. We survey bacterial microbiomes present in the fungal cultivar inocula of leaf-cutting ants, which are vertically transmitted and could potentially lead to co-propagation of beneficial fungus-bacteria consortia to improve health and growth of incipient gardens. SummaryMicrobiome surveys provide clues for the functional roles of symbiotic microbial communities and their hosts. In this study, we elucidated bacterial microbiomes associated with the vertically-transmitted fungal inocula (pellets) used by foundress queens of the leafcutting ant Atta texana as starter-cultures for new gardens. As reference microbiomes, we also surveyed bacterial microbiomes of foundress queens, gardens, and brood of incipient nests. Pseudomonas, Acinetobacter, Propionibacterium, and Corynebacterium were consistently present in high abundance in microbiomes. Some pellet and ant samples contained abundant bacteria from an Entomoplasmatales-clade, and a separate PCR-based survey of Entomoplasmatales bacteria in eight attine ant-genera from Brazil placed these bacteria in a monophyletic clade within the bacterial genus Mesoplasma. The attine antMesoplasma association parallels a similar association between a closely-related, monophyletic Entomoplasmatales-clade and army ants. Of thirteen A. texana nests surveyed, three nests with exceptionally high Mesoplasma abundance died, whereas the other nests survived. It is unclear whether Mesoplasma was the primary cause of mortality, or Mesoplasma became abundant in moribund nests for non-pathogenic reasons. However, the consistent and geographically widespread presence of Mesoplasma suggests an important functional role in the association with attine ants.

Microbial composition of spiny ants (Hymenoptera: Formicidae: Polyrhachis) across their geographic range

“…Our statistical tests also gave similar results to those observed for the mantel tests, suggesting that the phylogeny of the host (subgenera) explains part of the bacterial community, and host location (country or biogeography) none. This result corroborates Meirelles et al [88] that also did not find any geographic signature in the bacterial community from the fungus-growing ant, Atta texana (Buckley). Certainly the specificity found in some strains of Enterobacteriaceae within subgenera of Polyrhachis contributed to our findings of correlation between bacterial community and phylogeny of the host (vertical transfer).…”

First Insight into Microbiome Profiles of Myrmecophilous Beetles and Their Host, Red Wood Ant Formica polyctena (Hymenoptera: Formicidae)—A Case Study

“…We found that all tested bacterial communities were predominated by three phyla (Proteobacteria, Actinobacteria, and Firmicutes), with each comprising a different share of the microbiome depending on species or sample tested (Table S1). Those phyla are frequently listed as the most abundant in bacterial communities associated with insect taxa [61][62][63][64], including ants [49,[65][66][67][68][69][70] and myrmecophilous caterpillars of Lycaenidae butterflies [71][72][73]. In some cases, the joint abundance of those phyla may exceed even 90% of bacterial community membership [63].…”

The evolution of abdominal microbiomes in fungus‐growing ants

“…The functional significance of the few but occasionally highly abundant Mollicutes OTUs remains enigmatic. It is very unlikely that they are pathogens (Anderson et al, ; Funaro et al, ; Kautz, Rubin, Russell, & Moreau, ; Meirelles et al, ; Sapountzis et al, ) and rather suggests that the high prevalences of EntAcro1 in the leaf‐cutting ants may be related to actively herbivorous foraging habits (De Fine Licht & Boomsma, ) which also implies the ingestion of plant sap and fruit juices (Littledyke & Cherrett, ). Their consistent localization in the fat body suggests that beneficial interactions with energy and nutrient decomposition processes are likely (Arrese & Soulages, ), particularly because some close relatives of the two most common EntAcro1 and EntAcro10 OTUs are associated with other insects with specialized diets where they may be mutualists (Lo, Ku, Chen, Chang, & Kuo, ).…”