Transporter gene family evolution in ectomycorrhizal fungi in relation to mineral weathering capabilities

Abstract. Ectomycorrhizal (ECM) fungi play an important role in biological mineral weathering and show increased mycelial base cation content when grown with minerals. However, the mechanisms underlying base cation mobilisation and uptake remain poorly understood. With a focus on the mineral weathering ECM genus Suillus, we investigated evolutionary expansions and contractions of base cation transporter gene families across a phylogeny of 108 Agaricomycetes species. We also quantified base cation uptake by ECM and saprotrophic fungal species, including Suillus, under pure culture conditions with and without mineral additions, and assessed correlations between uptake and base cation transporter family copy numbers. We hypothesised that (1) greater base cation uptake depends on higher gene copy numbers of base cation transporter families resulting from evolutionary expansions, (2) weathering of mineral additions enhances base cation uptake by Suillus, and (3) Suillus species exhibit greater base cation uptake in mineral amended conditions compared to other fungi. We identified 25 base cation transporter families with significant expansions and contractions across the phylogeny, and many within Suillus, underscoring the ecological importance of base cation transport in this genus. Suillus and Piloderma, another ECM genus, showed higher mycelial cation concentrations when grown with minerals compared to nutrient limited conditions, confirming mineral-derived uptake. Nine significant positive correlations were detected between base cation uptake and base cation transporter gene family copy numbers in mineral amended conditions. This indicates that in some cases, such as for the Mg2+ transporter-E family, expansions in transporter families likely support enhanced base cation acquisition. Overall, these findings suggest that Suillus species have undergone rapid evolutionary changes in base cation transporter family copy numbers, potentially linked to their mineral weathering abilities. Further studies integrating transcriptional regulation of transporter genes will be essential to elucidate the mechanisms governing base cation mobilisation and uptake in Suillus and other ECM fungi.