Investigation of Microbial Interactions and Ecosystem Dynamics in a Low O2 Cyanobacterial Mat.

Abstract

Cyanobacteria are believed to be responsible for the oxygenation of the Earth’s atmosphere and oceans, which enabled the evolution of metabolisms that depend on O2. Little is known about cyanobacteria adapted to low-O2, sulfidic conditions, which dominated the oceans when oxygenic photosynthesis first evolved. To better understand how such cyanobacteria function and contribute to biogeochemistry, metagenomics and metatranscriptomics were used to characterize modern cyanobacterial mats that thrive under low-O2, sulfidic conditions in the Middle Island Sinkhole (MIS) of Lake Huron. Metagenomics revealed a consortium of microorganisms that regulate biogeochemical cycling at the sediment/water interface. The mats were dominated by Phormidium, a cyanobacterium that was inferred to perform anoxygenic photosynthesis in the presence of sulfide based on (i) primary production rate experiments, (ii) expression of sulfide quinone reductase, and (iii) a high ratio of transcripts for photosystem I to photosystem II. Combined with excess organic matter, chemical reductants and rapid utilization of O2 by respiration, this anoxygenic photosynthesis makes the MIS mats a net sink for O2. Such anoxygenic cyanobacterial mats were likely widespread under the low-O2 conditions of the Proterozoic, and may help to explain why atmospheric O2 levels remained low for much of Earth’s history. Genome sequences were reconstructed for the dominant mat organisms, and transcript abundance was used to identify organisms expressing metabolic pathways that regulate geochemical cycling at MIS. Desulfobacterales were responsible for mediating production of sulfide, which likely contributes to hypoxia at MIS and regulates oxygenic versus anoxygenic photosynthesis by Phormidium. Members of the Proteobacteria were found to perform aerobic oxidation of various sulfur species, H2 and CO. Viral predation was detected by two way exchange of DNA between Phormidium and PhV1, an abundant virus at MIS. Phormidium used viral DNA within a CRISPR system to defend itself, while PhV1 was found to possess a host derived nblA gene, which breaks down photosynthetic pigments. Overall, this work suggests that ancient cyanobacterial mats were not necessarily a source for O2, and that sulfide concentration, metabolic products from other organisms, viral predation, and light availability could all influence cyanobacterial production of O2 in low-O2 environments.