Seasonal Shifts in Community Composition and Proteome Expression in a Sulfur-Cycling Cyanobacterial Mat

Seasonal changes in light and physicochemical conditions have strong impacts on cyanobacteria, but how they affect community structure, metabolism, and biogeochemistry of cyanobacterial mats remains unclear. Light may be particularly influential for cyanobacterial mats exposed to sulfide by altering the balance of oxygenic photosynthesis and sulfide-driven anoxygenic photosynthesis. We studied temporal shifts in irradiance, water chemistry, and community structure and function of microbial mats in Middle Island Sinkhole (MIS), where anoxic and sulfate-rich groundwater provides habitat for cyanobacteria that conduct both oxygenic and anoxygenic photosynthesis. Seasonal changes in light and groundwater chemistry were accompanied by shifts in bacterial community composition, with a succession of dominant cyanobacteria from Phormidium to Planktothrix, and an increase in diatoms, sulfur-oxidizing bacteria, and sulfate-reducing bacteria from summer to autumn. Differential abundance of cyanobacterial light harvesting proteins likely reflects a physiological response of cyanobacteria to light level. Beggiatoa sulfur oxidation proteins were more abundant in autumn. Correlated abundances of taxa through time suggest interactions between sulfur oxidizers and sulfate reducers, sulfate reducers and heterotrophs, and cyanobacteria and heterotrophs. These results support the conclusion that seasonal change, including light availability, has a strong influence on community composition and biogeochemical cycling of sulfur and O2 in cyanobacterial mats. Originality-Significance Statement Cyanobacterial mats are found in terrestrial and aquatic environments on modern Earth and their fossil remains are present throughout the geologic record. They are biogeochemical oases that underpin diverse metabolic interactions, transform key nutrients and fix carbon, and can thrive in extreme environments. Mat-forming cyanobacteria can be metabolically versatile and conduct both oxygenic and anoxygenic photosynthesis using sulfide (OP and AP), thereby participating in both oxygen and sulfur cycling. The effect of seasonality on ecological factors constraining photosynthetic production and geochemical cycling in extreme cyanobacterial mats is not well known. In this study, we surveyed the mat community composition via bacterial 16S rRNA genes, microbial activity via metaproteomics, and water physico- and geochemistry over multiple seasons and years of the cyanobacterial mat in Middle Island Sinkhole, an O2-poor benthic sinkhole in Lake Huron, Michigan. We found that higher availability of sulfate-rich groundwater, together with higher light intensity, coincided with dominance of the metabolically flexible cyanobacterium Phormidium during the summer. Diverse sulfur cycling bacteria were more successful in other seasons when the mat experienced lower light and sulfate availability. These results provide insights into how seasonal environmental dynamics can shape the community structure and metabolisms of microbial mats, ultimately controlling biogeochemical cycling in these ecological hotspots.