The microbial ecology and biogeochemistry of cyanobacteria in the arsenic-rich and inorganic carbon-limited geothermal waters of El Tatio Geyser Field, Chile

Geothermal settings are some of the best-known analogs for early earth environments and among the best places to investigate the impact of extreme conditions on microbial life. El Tatio Geyser Field (ETGF) is a geothermal setting located at 4,300m in the Atacama Desert region of Chile. Its high-elevation desert position leads to high UV-flux, rapid evaporation, and mineral precipitation. El Tatio geothermal waters also possess extremely limited concentrations of life-essential nutrients, such as dissolved inorganic carbon (DIC as CO2(aq) + HCO3-), contain among the highest naturally occurring concentrations of the toxic element arsenic (As as H3AsO30 + HXAsO43-X), and are buffered to circumneutral pH by arsenate (H2AsO4-/HAsO42-; pKa ~ 6.9 at 25°C). Cyanobacteria were found to be the most important primary producers supporting microbial communities in El Tatio geothermal waters. The objective of this dissertation work was to characterize the role of cyanobacteria in the ETGF microbial ecosystem, and determine the response of cyanobacteria to the high-As and low-DIC conditions present at ETGF. Field observations, geochemical analyses, and next-generation 16S rRNA gene sequencing approaches were used to determine the geochemical controls on cyanobacterial distribution, the phylogenetic diversity of El Tatio cyanobacteria, and the corresponding microbial community structure at sites with and without cyanobacteria. Four cultured cyanobacterial strains were isolated from ETGF mat material, and experiments were performed to assess the growth and carbon-uptake response of these strains to low DIC, AsIII, and AsV. AsIII and temperature negatively controlled the abundance and distribution of cyanobacteria in geothermal outflows throughout ETGF, whereas AsV positively influenced these factors. In the laboratory, AsIII inhibited the growth of cultured strains, while AsV stimulated growth. Closed-system experiments showed significantly increased carbon uptake and growth in the presence of AsV, due to the ability of arsenate to offset the rapid upward pH shift that often occurs in mats during photosynthesis, thereby maintaining DIC in the preferred forms for cyanobacterial uptake. These results showed that AsV plays a positive role in the ETGF microbial ecosystem by increasing the productivity of cyanobacterial mats under low DIC and arsenate-buffered conditions.