Adaptation of Microbialite-Associated Prokaryotic Communities to Natural and Experimental Anoxic Conditions

Abstract

Microbialites are rocks formed by microbial communities that influence, promote, and/or control the precipitation of mineral phases. The oldest microbialites date back to the Archean and formed under globally anoxic conditions. Accordingly, modern microbialites developing under oxic conditions are limited analogs of their earliest predecessors. We discovered microbialites in the deep, seasonally anoxic water column of crater lakes Alchichica and Atexcac (Mexico). We studied the prokaryotic communities of plankton and microbialites from oxic and anoxic layers, alongside the temporal dynamics of microbialite communities incubated under strict continuous anoxia. 16S rRNA gene amplicon sequencing showed shifts in the relative abundance of taxa under anoxia, rather than changes in overall diversity. Regardless of their original depth, microbialite-associated communities from oxic and anoxic zones converged after ~25 weeks of laboratory exposure to a N₂-H₂-CO₂ (85:10:5) atmosphere. Sequences assigned to likely anoxygenic photosynthetic taxa, notably within the Alpha- and Gammaproteobacteria, together with phyla associated with sulfate-reduction and other sulfur-cycling bacteria, increased in relative abundance. We isolated seven bacterial strains under anoxia, some of them biomineralizing. Several of these strains were cyanobacteria affiliated with the Leptolyngbyales, suggesting that they either continue to perform oxygenic photosynthesis or, hypothetically, switch to H₂S-dependent anoxygenic photosynthesis. Our results indicate that these microbialite communities adapt to long-term anoxia (more than 70 weeks) under laboratory conditions, likely sustaining photosynthetic alkalinization and carbonate precipitation under such conditions.