Symbiotic bacterial communities in rainforest fungus-farming ants: evidence for species and colony specificity

Abstract

Animals may host diverse bacterial communities that can markedly affect their behavioral physiology, ecology, and vulnerability to disease. Fungus-farming ants represent a classical example of mutualism that depends on symbiotic microorganisms. Unraveling the bacterial communities associated with fungus-farming ants is essential to understand the role of these microorganisms in the ant-fungus symbiosis. The bacterial community structure of five species of fungus-farmers (non-leaf-cutters; genera Mycocepurus, Mycetarotes, Mycetophylax, and Sericomyrmex) from three different environments in the Brazilian Atlantic rainforest (lowland forest, restinga forest, and sand dunes) was characterized with amplicon-based Illumina sequencing of 16 S ribosomal RNA gene. Possible differences in bacterial communities between ants internal to the nest (on the fungus garden) and external foragers were also investigated. Our results on the richness and diversity of associated bacteria provide novel evidence that these communities are host- and colony-specific in fungus-farming ants. Indeed, the bacterial communities associated with external foragers differ among the five species, and among colonies of the same species. Furthermore, bacterial communities from internal ants vs. foragers do not differ or differ only slightly within each ant species. This study highlights the importance of describing ant-associated bacterial communities to better understand this host-bacterial interaction in the social environment of insect colonies and provides the foundation for future studies on the ecological and evolutionary processes that drive the success of fungus-farming ants.

Three phylogenetically distinct and culturable diazotrophs are perennial symbionts of leaf‐cutting ants

“…In our NGS experiments, we found 502 genera associated with leafcutters, most of them within Alphaproteobacteria, which was represent by a large proportion of the sequences described in 16S rRNA libraries, corroborating previous studies for several species of leaf‐cutting ants (Liberti et al, 2015 ; Sapountzis et al, 2015 , 2019 ; Teseo et al, 2019 ; Vieira et al, 2017 ). Our community analysis (Figure 3 ) suggests that some leafcutter–microbe associations may be species‐specific, as described in basally derived Attini (Ronque et al, 2020 ). On the other hand, some associations were detected in all ant species, as represented by a core leafcutter bacteriome with 84 bacterial genera (Tables S1 and S2 ), which may result from fixed symbiotic associations with shared functional roles, perhaps related to ant nutrition.…”

“…This controversy illustrates the challenges of characterizing the relationship between leafcutters and nutritional bacteria. Other reasons contributing to that include incomplete biogeographic information, poor cultivability of microbial symbionts in laboratory conditions, and high diversity and variability of bacteria groups living integrated in the ant environment (Barcoto et al, 2020 ; Ronque et al, 2020 ). Therefore, the current scenario suggests that multiple bacterial associations may be related to the ants, so it is conceivable that other, yet noncharacterized, nutritional players exist.…”

Male‐biased dispersal in a fungus‐gardening ant symbiosis

“…Our results support greater dispersal abilities in male T. septentrionalis than females. Consequently, this suggests that the dispersal abilities of the vertically transmitted symbiotic fungus (and further associated microbial symbionts; (Ishak et al., 2011; Ronque et al., 2020) are likely also limited and thus also exhibits spatial structure, unless the fungus also has the ability of independent dispersal as suggested in A. texana (Smith et al., 2019). While higher attine fungi are not known to be free living (Nygaard et al., 2016), horizontal movement of fungi could occur among neighboring colonies as documented in less derived attini, that is, by garden sharing or stealing following losses due to predation or pathogen attack (Adams et al., 2000; Green et al., 2002; Kellner et al., 2013).…”

Male-Biased Dispersal in a Female-Dispersed Symbiosis

“…Our results support greater dispersal abilities in male T. septentrionalis than females. Consequently, this suggests that the dispersal abilities of the vertically transmitted symbiotic fungus (and further associated microbial symbionts (Ishak et al, 2011;Ronque, Lyra, Migliorini, Bacci, & Oliveira, 2020)) are likely also limited and thus also exhibits spatial structure, unless the fungus also has the ability of independent dispersal as suggested in A. texana (Smith et al, 2019). Limited female and symbiont co-dispersal could represent a significant bottleneck to fungal diversification (and associated microbes).…”