Varied physiological responses of the facultative gamma-proteobacterium, Shewanella oneidensis MR-1, and the delta-proteobacterium Desulfovibrio vulgaris hildenborough to oxygen

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2011

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Montana State University - Bozeman, College of Letters & Science

Abstract

Evolution of molecular oxygen and accumulation in Earth's atmosphere is considered to be the one of the most significant changes on Earth that impacted the evolution of life. Over the past 600 million years, there have been fluctuations in atmospheric oxygen concentrations that have driven the evolution of species in all three domains of life. Over the years, microbes and other life acquired different strategies to survive efficiently in the presence of oxygen through mutagenic evolutionary mechanisms. This dissertation demonstrates how a facultative bacterium, Shewanella oneidenisis MR-1, through signaling mechanisms, senses oxygen as an external stimulus and regulates metabolism accordingly. These signaling molecules reside within open reading frames as small domains that sense/transmit signals based on stimulus and subsequently trigger a response within the cell. One such open reading frame, SO3389, containing multiple domains was characterized in the first two chapters of this dissertation. Physiology and genetics based experiments were employed to address hypotheses that a putative sensory-box protein was involved in oxygen sensing. It was elucidated that this protein plays a role in sensing dissolved oxygen (DO) levels that affected both aerobic biofilm formation and transitions to anoxia. While oxygen can be an attractant in aerobic growth mode, it is considered to be toxic to strict anaerobes, such as Desulfovibrio vulgaris Hildenborough, a sulfate-reducing bacterium. Recent studies, however, reveal that even strict anaerobes can tolerate micromolar concentrations of oxygen. These organisms have evolved several protective mechanisms to combat oxidative stress and some may even possess oxygen-utilization machinery. Chapters 3 and 4 address the phenomenon of oxygen tolerance in D.vulgaris planktonic and biofilm cells and the variation in this response based on available carbon and energy sources. Physiology- and genetic-based approaches revealed that D.vulgaris cells grown on pyruvate exhibit increased tolerance towards DO but lactate-grown cells utilized oxygen for energy production at intermediate levels of DO. The substrate-dependent nature of oxygen response in D. vulgaris has not been previously reported, and could impact remediation strategies as well as possible implications for community interactions. The results demonstrated in this dissertation underscore two major findings with respect to oxygen responses: (i) the elucidation of unknown function for a conserved hypothetical protein, and (ii) the substrate-dependent nature of oxygen utilization in a "strict" anaerobe. The elucidation of function for these genes/proteins/organisms will further our fundamental understanding of microbial physiology, of the versatility that allows adaptation to constantly changing environments, and help improve future remediation strategies.

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