Kooij, P. W. | bioRxiv Science

bioRxiv2024

Genomic Signatures of Domestication in a Fungus Obligately Farmed by Leafcutter Ants

The naturally selected fungal crop (Leucoagaricus gongylophorus) farmed by leafcutter ants shows striking parallels with artificially selected plant crops domesticated by humans (e.g., polyploidy, engorged nutritional rewards, dependence on cultivation). To date, poorly resolved L. gongylophorus genomes based on short-read sequencing have constrained hypotheses about how millions of years under cultivation by ants shaped the fungal crop genome and potentially drove domestication. We use PacBio HiFi sequencing of L. gongylophorus from the leafcutter ant Atta colombica to identify 18 putatively novel biosynthetic gene clusters that likely cemented life as a cultivar (e.g., plant fragment degradation, ant-farmer communication, antimicrobial defense). Comparative analyses with cultivated and free-living fungi showed genomic signatures of stepwise domestication transitions: 1) free-living to ant-cultivated: loss of genes conferring stress response and detoxification, 2) hyphal food to engorged nutritional rewards: expansions of genes governing cellular homeostasis, carbohydrate metabolism, and siderophore biosynthesis, and 3) detrital provisioning to freshly cut plant fragments: gene expansions promoting cell wall biosynthesis, fatty acid metabolism, and DNA repair. Comparisons across L. gongylophorus fungi farmed by three leafcutter ant species highlight genomic signatures of exclusively vertical clonal propagation and widespread transposable element activity. These results show how natural selection can shape domesticated cultivar genomes towards long-term ecological resilience of farming systems that have thrived across millennia.

evolutionary biology↗

bioRxiv2024

Vertical transmission of fungus-growing ant microbiota is species-specific and constrained by queens

Multipartite symbioses are inherently complex, involving dynamic ecological interactions between organisms with intertwined yet distinct evolutionary histories. The fungus-growing (attine) ants facilitate maintenance of a symbiotic species network through maternal vertical transmission of an obligate fungal symbiont. While the gut microbiomes of fungus-growing ant species are remarkably simple, their fungal gardens support diverse microbial communities. Here, we focus on an understudied transmission bottleneck: the fungal garden pellet that nest-founding queens transfer to inoculate a new fungal garden. We used 16S rRNA metagenomic sequencing to reconstruct the extent of vertical transmission of bacteria to new gardens via queen pellets in four sympatric fungus-growing ant species (Atta sexdens, Atta cephalotes, Acromyrmex echinatior, and Mycetomoellerius mikromelanos) from Central Panama. We also characterized the bacterial communities associated with queen eggs and somatic tissues (mesosomas, guts and ovaries) to assess whether queens are likely to transmit symbiotic bacteria of workers, such as cuticular Actinobacteria and endosymbionts (Wolbachia, Mesoplasma, and Spiroplasma). Our results suggest that garden-associated bacteria are mainly horizontally acquired as the bacterial communities of pellets shared few bacterial taxa with the mature gardens of the four ant species investigated. While the bacterial communities of garden pellets showed some species-specificity, a subset of prevalent bacterial taxa were shared across ant species. Further, our findings provide evidence for vertical transmission of species-specific endosymbiotic bacteria through a transovarial route and/or via fecal droplets. Overall, while we found mixed evidence for vertical transmission of garden bacteria, our results support maternal transmission as a primary route for gut-associated symbionts. While our results suggest that vertical transmission of fungus-growing ant bacterial associates is mediated by the ant hosts, the mechanism behind this host control is not yet understood.

microbiology↗