Molecular biogeochemistry of modern and ancient marine microbes

Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy at the Massachusetts Institute of Technology and the Woods Hole Oceanographic Institution February 2010Biological activity has shaped the surface of the earth in numerous ways, but life’s most pervasive and persistent global impact has been the secular oxidation of the surface environment. Through primary production – the biochemical reduction of carbon dioxide to synthesize biomass – large amounts of oxidants such as molecular oxygen, sulfate and ferric iron have accumulated in the ocean, atmosphere and crust, fundamentally altering the chemical environment of the earth’s surface. This thesis addresses aspects of the role of marine microorganisms in driving this process. In the first section of the thesis, biomarkers (hydrocarbon molecular fossils) are used to investigate the early history of microbial diversity and biogeochemistry. Molecular fossils from the Transvaal Supergroup, South Africa, document the presence in the oceans of a diverse microbiota, including eukaryotes, as well as oxygenic photosynthesis and aerobic biochemistry, by ca. 2.7Ga. Experimental study of the oxygen requirements of steroid biosynthesis suggests that sterane biomarkers in late Archean rocks are consistent with the persistence of microaerobic surface ocean environments long before the initial oxygenation of the atmosphere. In the second part, using Prochlorococcus (a marine cyanobacterium that is the most abundant primary producer on earth today) as a model system, we explored how microbes use the limited nutrient resources available in the marine environment to make the protein catalysts that enable primary production. Quantification of the Prochlorococcus proteome over the diel cell-division cycle reveals that protein abundances are distinct from transcript-level dynamics, and that small temporal shifts in enzyme levels can redirect metabolic fluxes. This thesis illustrates how molecular techniques can contribute to a systems-level understanding of biogeochemical processes, which will aid in reconstructing the past of, and predicting future change in, earth surface environments.Office of Naval Research National Defense Science & Engineering Graduate Fellowship (to JRW), National Science Foundation Graduate Research Fellowship (to JRW), NASA Exobiology Program Award NNG05GN62G (to RES), NASA Astrobiology Institute Award NNA08CN84A (to RES), National Science Foundation Award EAR0418619 (to RES), Agouron Institute Geobiology Award AI-GB4.02.3Extn06.2bMIT (to RES), Gordon and Betty Moore Foundation Marine Microbiology Award 495 (to SWC), National Science Foundation Award OCE0425602 (to SWC) National Science Foundation Award EF0424599 (to SWC), Department of Energy Award DE-FG02-07ER64506 (to SWC), Department of Energy Award DE-FG02-08ER64516 (to SWC