Genomic Signatures of Domestication in a Fungus Obligately Farmed by Leafcutter Ants
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Abstract
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.
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These results strongly support a hypothesis that colonies of different leafcutter ant species are strong barriers to genetic admixture.
It would be cool to also sample from the extremes of L. gongylophorus' natural range (eg. the Texas and Argentinian populations)
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Specifically, we identified and annotated 20 BGCs (18 putatively new) with diverse functions.
It might be helpful to include the antiSMASH annotations in the supplemental as a reference for other fungal researchers.
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Abundant TEs are also known in fungal ectomycorrhiza symbioses
Just out of curiousity, does the Leucocoprinus species in figure 1 also have a lot of TEs? It might be nice to emphasize here if this is conserved even in more distantly related but cultivated species.
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Figure 2: Word clouds representing the clusters of enriched Biological Process terms from the gene ontology enrichment analysis.Each box clusters significant GO terms from similarity matrices of functional terms corresponding to gene gain (or gene family expansion; left column) and loss (or gene family contraction; right column) through each step of the domestication process noted in Figure 1.
Are reproduction-related genes affected too? It would seem that all that vertically transmitted propagation would force a species to use it or lose it.
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Figure 1: Maximum-likelihood phylogeny showing domestication transitions in ant-farmed and closely related free-living fungi.The tree was reconstructed from 1136 sequences of amino-acid from single-copy orthologs shared by all samples. Domestication transitions indicated by colored boxes: 1) yellow: from free-living to ant-cultivated (polyphyletic), 2) blue: from hyphal food to engorged nutritional rewards (higher neoattines transition), and 3) orange: from detrital provisioning to freshly cut plant fragments (leafcutters transition). Gene gain / expansion (+), and gene loss / contraction (-) are represented for each of these transitions (indicated by the red triangle for the transition to ant-cultivated species). All branches received maximum UFBoot support (100%). Scale bar: amino acid substitutions per site.
Presumably the yellow …
Figure 1: Maximum-likelihood phylogeny showing domestication transitions in ant-farmed and closely related free-living fungi.The tree was reconstructed from 1136 sequences of amino-acid from single-copy orthologs shared by all samples. Domestication transitions indicated by colored boxes: 1) yellow: from free-living to ant-cultivated (polyphyletic), 2) blue: from hyphal food to engorged nutritional rewards (higher neoattines transition), and 3) orange: from detrital provisioning to freshly cut plant fragments (leafcutters transition). Gene gain / expansion (+), and gene loss / contraction (-) are represented for each of these transitions (indicated by the red triangle for the transition to ant-cultivated species). All branches received maximum UFBoot support (100%). Scale bar: amino acid substitutions per site.
Presumably the yellow "Leucocoprinus sp" doesn't have gongylidia like the. L. gongylophorus strains and thus lost less genes? Whyn is Leucocoprinus cultivated? Does it have a different reward mechanism for the ants?
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two terpenes with high similarity to (+)-δ-cadinol,
It might be nice to explain what this is typically used for in fungal biology/why it is a common fungal metabolite.
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BUSCO found 89.6% complete Agaricales orthologs
Well done!
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genome assembly of L. gongylophorus from a Panamanian colony of the leafcutter ant, Atta colombica
Was there a reason you selected a strain of fungus from a different population (A. colombica vs A. cephalotes) when there was existing sequencing data that could supplement your data set?
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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
Congratulations on the cool paper and most complete genome of this type of fungus!
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