Genomic and Functional Investigations Into Seasonally-Impacted and Morphologically-Distinct Anoxygenic Photosynthetic Cyanobacterial Mats

Abstract

Cyanobacteria are key members of modern photosynthetic microbial mats, by providing organic matter and nutrients to the ecosystem. With their innovation of oxygenic photosynthesis (OP) over 2 billion years ago and the wide distribution of microbial mats in the geologic record, cyanobacteria have shaped Earth’s redox history. Select modern cyanobacteria are also capable of anoxygenic photosynthesis using sulfide (AP), an older metabolism than OP and a less-understood biological mechanism that limited the rise of oxygen. This dissertation used molecular and ecological techniques to investigate modern anoxygenic cyanobacteria. In Chapter I, I outline the current understanding of AP cyanobacterial mats in modern and ancient ecosystems. In Chapter II, I described the genome of a cultured AP cyanobacterium, Geitlerinema sp. PCC9228. Genomic analysis of Geitlerinema revealed numerous adaptations to low-oxygen and sulfidic conditions, which were potentially prevalent for much of Earth’s history. I applied knowledge of cyanobacterial genetic adaptation to AP from Geitlerinema, to the microbial mats of Middle Island Sinkhole (MIS), a submerged sinkhole impacted by low-O2, sulfur-rich groundwater. In Chapter III, I characterized the impact of seasonally changing light conditions and geochemistry on the microbial community (16S rRNA genes and metagenomics) and its function (metaproteomics). The dominant AP cyanobacteria, Phormidium and Planktothrix, are abundant and active in summer when light is highest. In contrast, when light is lower in autumn, sulfide-oxidizing bacteria are more active. The shift in microbial community function has implications for oxygen and sulfur cycling in the mat. In Chapter IV, I applied metagenomics and metaproteomics to distinct mat morphotypes in MIS. I observed flat purple cyanobacterially-dominated mat (‘flat’), conical purple mat (‘fingers’), white-pigmented mat (‘white’), and a mottled purple/brown pigmented mat (‘giraffe’). The cyanobacterial community shifted from Phormidium and Planktothrix in fingers and some flat mat, to Pseudanabaena and Spirulina in giraffe and white mats. Sulfide-oxidizing bacteria and sulfate-reducing bacteria were widely observed in all mat types. The genomes and proteins suggest functional niche similarity with regard to sulfide and oxygen cycling between abundant cyanobacteria in different mats. Understanding the role of cyanobacteria in shaping the function and appearance of modern microbial mats informs the interpretation of the chemical environment, metabolisms, and biogeochemical impact of microbial mats through Earth history.