Project: Microbial Activity and Chemoautotrophy in the Deep Sea: Who, How, and How Much?

NSF Award Abstract:
The deep sea, defined as deeper than 200 m, is the largest and least explored habitat on the surface of our planet. It covers nearly two-thirds of the Earth's surface, contains approximately 75% of marine water by volume, and is home to about 55% of all marine microorganisms. Deep-sea microorganisms can play important roles in shaping global chemistry and climate, for example producing and consuming greenhouse gases (e.g., carbon dioxide and nitrous oxide). However, the microbiology of deep-sea waters is understudied relative to that of the surface ocean. Recent data suggests a much more diverse and active microbial community at depth than previously thought, but much remains to be known. For instance, recent estimates suggest that approximately 60% of the microbial species in the deep sea are novel. This project investigates the metabolic activity of deep-sea microorganisms, focusing on chemoautotrophy and the carbon cycle. Chemoautotrophy is a microbial metabolism in which inorganic carbon (e.g., carbon dioxide) is converted to sugar and biomass using chemical energy. This project uses several state-of-the-art sampling and analyses techniques to determine which species conduct chemoautotrophy (who?), what types of chemical energy support it (how?), and at what rate it occurs (how much?) throughout the deep sea. Answering these questions provides insight into deep-sea microbial ecology and quantitative data on the sources and sinks of carbon in deep waters. Results will advance our understanding of the ability of our oceans to sequester carbon over long timescales. This work benefits society through the implications of its findings for our ability to predict and mitigate climate change, as well as its educational mission, which includes training diverse high school, undergraduate, and graduate students in interdisciplinary, climate-relevant science through one-on-one mentorship, hands-on coursework, and the initiation of an annual regional symposium featuring student research.

This project investigates uncultured microorganisms' genetic potential and activity in the mesopelagic and bathypelagic oceanographic layers (200 to 4000 m water depth) to characterize deep-sea microbiology and address a discrepancy in the marine carbon cycle, namely, that respiration rates consistently exceed estimates of vertical inputs of carbon to the dark ocean. Chemoautotrophy may explain at least part of this discrepancy, but known types of chemoautotrophy (e.g., coupled to ammonia and nitrite oxidation) are insufficient to bridge the gap, suggesting novel chemoautotrophs and diverse coupled catabolisms. The overarching hypotheses are that (1) deep-sea microorganisms are more active than currently appreciated, (2) the organic carbon required to support this activity is provided, at least in part, by higher rates of endogenous inorganic carbon fixation, and (3) carbon fixation is performed by more phylogenetically and metabolically diverse chemoautotrophs/mixotrophs than currently known. This study uses high-pressure sampling containers during two deep-sea oceanographic expeditions, metagenomics, metatranscriptomics, and stable-isotope experiments coupled to single-cell isotope analyses via nanoSIMS to (1) quantify microbial anabolic activity in general and chemoautotrophy, mixotrophy, and heterotrophy specifically at bulk and single-cell levels, (2) characterize the diversity and distribution of genes and transcripts involved in chemoautotrophy and heterotrophy, (3) identify novel chemoautotrophs and mixotrophs and quantify their contribution to carbon cycling, and (4) investigate the ability of a major chemoautotrophic deep-sea lineage, the Marine Group I Thaumarchaeota, to utilize organic matter. The results have the potential to reveal novel functions in uncultured microbes and change our understanding of marine carbon cycling.

This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.