A Quaternary Sedimentary Ancient DNA (<i>sed</i>aDNA) Record of Fungal–Terrestrial Ecosystem Dynamics in a Tropical Biodiversity Hotspot (Lake Towuti, Sulawesi, Indonesia)

Abstract

Short-term observations suggest that environmental changes affect the diversity and composition of soil fungi, significantly influencing forest resilience, plant diversity, and soil processes. However, time-series experiments should be supplemented with geobiological archives to capture the long-term effects of environmental changes on fungi–soil–plant interactions, particularly in undersampled, floristically diverse tropical forests. We recently conducted trnL-P6 amplicon sequencing to generate a sedimentary ancient DNA (sedaDNA) record of the regional catchment vegetation of the tropical waterbody Lake Towuti (Sulawesi, Indonesia), spanning over one million years (Myr) of the lake’s developmental history. In this study, we performed 18SV9 amplicon sequencing to create a parallel paleofungal record to (a) infer the composition, origins, and functional guilds of paleofungal community members and (b) determine the extent to which downcore changes in fungal community composition reflect the late Pleistocene evolution of the Lake Towuti catchment. We identified at least 52 members of Ascomycota (predominantly Dothiodeomycetes, Eurotiomycetes, and Leotiomycetes) and 12 members of Basidiomycota (primarily Agaricales and Polyporales). Spearman correlation analysis of the relative changes in fungal community composition, geochemical parameters, and paleovegetation assemblages revealed that the overwhelming majority consisted of soil organic matter and wood-decaying saprobes, except for a necrotrophic phytopathogenic association between Mycosphaerellaceae (Cadophora) and wetland herbs (Alocasia) in more-than-1-Myr-old silts and peats deposited in a pre-lake landscape, dominated by small rivers, wetlands, and peat swamps. During the lacustrine stage, vegetation that used to grow on ultramafic catchment soils during extended periods of inferred drying showed associations with dark septate endophytes (Ploettnerulaceae and Didymellaceae) that can produce large quantities of siderophores to solubilize mineral-bound ferrous iron, releasing bioavailable ferrous iron needed for several processes in plants, including photosynthesis. Our study showed that sedaDNA metabarcoding paired with the analysis of geochemical parameters yielded plausible insights into fungal-plant-soil interactions, and inferred changes in the paleohydrology and catchment evolution of tropical Lake Towuti, spanning more than one Myr of deposition.

Keywords

• Lake Towuti
• tropics
• <i>sed</i>aDNA
• fungi
• quaternary
• ultramafic