BioMetArchive: Geomicrobiological insights into the 1 Million-Year sedimentary record of ferruginous lake Towuti

Lake Towuti, Indonesia is a permanently stratified lake influenced by tropical weathering of an ultramafic catchment. This results in high iron but minimal sulfate inflows into the basin, creating anoxic ferruginous conditions in its bottom waters (>130 m). The International Continental Scientific Drilling Program (ICDP) retrieved a 100-m-long sediment core covering 1 million years of sedimentation history. Through taxonomic and metagenomic analyses, complemented with pre-existing environmental and geochemical datasets, the project BioMetArchive provides a comprehensive characterization of the lacustrine subsurface biosphere in terms of diversity, abundance, and metabolic functions.

As electron acceptors in the pore water became depleted within the upper 0.5 m below lake floor (mblf), cell counts decreased from 109 to 104 cells cm-3, concurrent to a shift in microbiome composition leading to a predominance of Bathyarchaeia. Metabolic features attributed to this class include sulfur transformation and (homo)acetogenic fermentation. Taxonomic profiling of 16S rRNA genes revealed a drastic decrease in microbial diversity inherent to substrate depletion during shallow burial. In contrast, increased compositional variability in sulfate-reducing bacterial populations was observed around tephra layers and diatom oozes, indicative of volcanic eruptions and primary productivity peaks, respectively. Microbial alpha and beta diversity also varied according to the different lithologies of stratigraphic units. In the upper subunit (20 mblf), an active and diverse microbial community involved in OM remineralization is driving effective turnover of volatile fatty acids and other solutes in the pore water. The second subunit (20-70 mblf) harbors a deep biosphere community adapted to a nutrient-depleted environment. In contrast, the lowermost subunit (70-100 mblf) is characterized by increased microbial diversity.

Thus, variations in 16S rRNA gene assemblages show that microbial diversity and composition are closely linked to the depositional history of Lake Towuti. We conclude that dynamic shifts in depositional conditions during the Late Pleistocene are tractable in the taxonomic and functional diversity of the subsurface biosphere. With increasing burial depth, sediment substrate depletion actively selects for acetogenic Bathyarchaeia, highlighting their capability to persist as main constituents of the deep subsurface microbial biosphere.