Ants mediate community composition of root‐associated fungi in an ant‐plant mutualism

Abstract

Cross‐kingdom interactions with plants were frequently related to microbial pathogens and herbivores. Yet, mutualistic interactions that involve multiple partners can confer cross‐kingdom functional benefits, which have been understudied. Ant gardens (AGs) are recognized as one of the most sophisticated of all symbioses between ants and flowering plants, forming good models to study cross‐kingdom interactions. The aim of this study was to examine whether ant‐plant interactions can influence the community composition of root‐associated fungi. We assessed whether two AG ant species, Camponotus femoratus and Neoponera goeldii, confer different physico‐chemical properties to their nests, and affect root fungal community composition and fungal functional guilds in the bromeliad Aechmea mertensii. The diversity and community composition of root‐associated fungi depended on ant species identity. The two ants had a contrasting influence on the structure and chemistry of the nest, and on the floristic diversity of the AGs. Multiple drivers may therefore determine the root‐associated fungal communities. As the outcome of the ant‐bromeliad interaction depends on the ant species, and because the plants are also involved in interactions with root‐associated symbionts, this study provided evidence that ecologically relevant symbioses can be mediated by cross‐kingdom interactions. Abstract in French is available with online material.

Fungi as mutualistic partners in ant-plant interactions

“…Some fungal strains isolated from galleries or domatia are ubiquitous and seem not to be specific to the ant species pointing towards an environmental acquisition ( Hirose et al., 2013 ; Nepel et al., 2014 ; Nepel et al., 2016 ; Vasse et al., 2017 ; Greenfield et al., 2021 ). Ant workers can bring spores or hyphal fragments from the environment into the nest by collecting pieces of soil and various organic debris from the ground or the canopy as has been highlighted in other interactions ( Abbott, 2002 ; Leroy et al., 2022 ). De novo acquisition of fungal species from the environment at each ant generation would explain the high number of genotypes and OTUs in domatia that do not cluster in the domatia symbiont clade ( Voglmayr et al., 2011 ; Vasse et al., 2017 ; Greenfield et al., 2021 ).…”

Mutualistic interactions between ants and fungi: A review

“…A study on the epiphytic tank bromeliad Aechmea mertensii specifically associated with Neotropical ant gardens showed the presence of mycorrhizal fungi of the Glomerales and Diversisporales that, thanks to their network of filaments among the roots, provide this plant with moisture and nutrients that it would not obtain otherwise (Leroy et al, 2022 ). Furthermore, endophytic fungi belonging to the Ascomycota were also noted as well as some Basidiomycota to a lesser degree.…”

“…Among the Ascomycota, Hypocreales, Chaetothyriales, and Eurotiales were more represented in the ant gardens initiated by the ponerine Neoponera mertensii than in those built by the formicine Camponotus femoratus , the contrary being true for Capnodiales. Thus, the identity of the ant species influences the root‐associated fungal diversity, endophytic fungi having a beneficial effect on the host plants (Leroy et al, 2019 , 2022 ). It would be interesting to verify in the future if the same is true for other ant garden epiphytes and if the endophytic fungi participate in reinforcing these ant gardens.…”