Exploring the microbe-energy interface: Geochemical reaction energetics and microbial diversity in a shallow marine hydrothermal system

Modern hydrothermal systems host an incredible diversity of predominantly thermophilic microorganisms. Most thermophiles are chemotrophs, gaining energy from chemical disequilibria that result from fluid mixing and water-rock reactions. The connection between life and energy is inescapable; however, the relationship between thermophile diversity and hydrothermal geochemistry is poorly understood. I use the shallow marine hydrothermal system of Vulcano Island, Italy, to study the interface between fluid chemistry, metabolic reaction energetics and the diversity of thermophilic microorganisms. Detailed geochemical analyses of hydrothermal fluids establish the geochemical variability in the shallow marine vents, geothermal wells and onshore seeps throughout the Vulcano hydrothermal system. First order geochemical analyses reveal large variations in temperature, pH, salinity and reduced aqueous species that define metabolic niches throughout the system. In situ chemical compositions are combined with standard state reaction properties to evaluate the Gibbs free energy of 234 potential metabolic reactions at 9 sites across the Vulcano system. Respiration and fermentation of carboxylic acids, neutral aldoses and amino acids are considered alongside chemolithotrophic reactions in the H-O-N-C-S-Fe system. Lithotrophic and heterotrophic respiration reactions yield up to 120 kJ/mol e- and are generally more favorable than fermentation reactions. Energy yields are highly dependent on the electron acceptor and variations in pH and ferrous iron concentrations result in large energetic variations across the sites investigated. Within this geochemical context, diverse archaeal and bacterial communities were identified throughout the system using standard molecular techniques. While culture-independent methods identified a number of organisms previously isolated from this system, most of the observed diversity belonged to phylogenetic groups with no cultured representatives, including the ancient Korarchaeota. Variations in microbial community structure among different sites are interpreted within the established geochemical framework and are attributed to variations in environmental conditions, as well as geochemical compositions and metabolic energetics. Potential metabolisms of the uncultured organisms can be inferred by comparing energy profiles among the sites. For the first time, complete geochemical analyses and reaction energetics are determined simultaneously with the phylogenetic distribution of thermophilic microorganisms and the relationships between geochemical variability and microbial diversity in hydrothermal ecosystems are explored.