Distinct root-associated fungal communities may account for the persistence of Podocarpus conifers in tropical forest

Podocarps (Podocarpaceae) are one of the few lineages of conifers found in closed canopy tropical forests. They typically have highly restricted distributions that are associated with nutrient-poor sites. Unlike other tree species, the presence of distinct nodule-like structures allows their roots to be easily distinguished from those of co-occurring taxa. In highly infertile ever-wet lower montane forest at Fortuna, Panama, roots of Podocarpus oleifolius occur in three microsites: in the soil; lying on top of surface litter; as aerial roots that climb the trunks of neighboring trees. We examined how microsite affects Podocarpus root fungal community composition by sequencing the internal transcribed spacer (ITS) region, and by measuring root nutrient concentration and phosphatase enzyme activity. We also compared Podocarpus roots collected from the soil with those of two common co-occurring angiosperm trees, Graffenrieda bella and Weinmannia pinnata. We found that root microsite accounted for 11% of the variation in root-associated fungal communities and also affected root calcium, potassium, and manganese concentration. Root fungal diversity, phosphate concentration, and phosphatase activity were unchanged. Across all microsites, the fungal order Helotiales accounted for 50%-60% of ITS reads, while aerial roots had significantly higher abundance of Trechisporales. When comparing across species, Glomeromycota were only detected in very low numbers overall (1.8%-3.3% of reads in angiosperms), and were especially low in Podocarpus (0.14% of reads). In contrast, Podocarpus had a higher fraction of reads belonging to Leotiomycetes than Graffenrieda and Weinmannia. Our findings highlight how root-associated fungal communities vary at the order level with microsite and host species in tropical montane forest. In continuously cool, low-nutrient wet environments, where nutrients are rapidly leached from throughfall, or are mineralized slowly from decomposing organic matter, alternatives to arbuscular mycorrhizal fungi may be especially advantageous to plants. Biotrophic fungi in the Helotiales have been implicated in nutrient transfer in alpine and arctic environments, and together with Trechisporales, may be key unrecognized mutualistic partners in the tropics. Collectively, these taxa may explain the association of podocarps with low-nutrient montane forest.