Theses and Dissertations at Montana State University (MSU)
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Item Evolutionary consequences of gene flow in the absence or inhibition of dispersal in microbial communities(Montana State University - Bozeman, College of Agriculture, 2023) Munro-Ehrlich, Robert Mason; Chairperson, Graduate Committee: Jovanka Voyich-Kane; This is a manuscript style paper that includes co-authored chapters.Much of our understanding of the evolutionary dynamics of microbial populations is derived from population level studies which focus on the immediately present populations and ignore the contributions of nearby communities. Microbial ecology studies typically do not distinguish between gene flow, i.e., the movement of genetic material between populations, and dispersal, i.e., the movement of those populations themselves. These two processes are indeed linked, but not identical. We have known for centuries that genetic material can be transferred between physically distant and taxonomically disparate microbial populations; molecular biology tools like cloning are dependent on this capability. In other words, gene flow can occur even without dispersal. However, our ecological and evolutionary studies of microbial populations typically fail to acknowledge the evolutionary impact and genetic contributions of outside populations. Unique evolutionary scenarios arise when dispersal between two or more populations is prevented or limited, but gene flow can still occur between them. We hypothesized that this scenario would impact microbial populations by facilitating speciation, selection, and local adaptation. We aimed to test this hypothesis by studying endemic Meiothermus populations inhabiting serpentinite rocks in the subsurface of the Samail ophiolite in Oman. Samail Ophiolite microbial communities, of which Meiothermus populations are a component, are dispersed across the subsurface and separated by meters of solid rock and by chemical and pH gradients spanning orders of magnitude. Despite barriers to dispersal that are significant enough to shape community structure, we found that gene flow still occurred between nearly all observed populations of Meiothermus. This gene flow is contributing to disruptive selection amongst cohabiting populations, and may also be contributing to local adaptation, both at the genetic and genomic level. We also identified potential mechanisms for this gene flow, including abundant viral elements. The sequence similarity of mobile genetic elements in these Meiothermus populations implies that this gene flow occurred after colonization by a common Meiothermus ancestor and that diversification is likely ongoing. To our knowledge, this is the first demonstration of gene flow across barriers to dispersal in an environmental microbial system. In conclusion, these results suggest that the capacity for microbial populations to undergo gene flow even in the absence or inhibition of dispersal is a natural process, has substantial consequences for the evolution of the effected population, and may also have consequences for the microbial and surrounding environment.Item Rock powered life in the Samail ophiolite: an analog for early Earth(Montana State University - Bozeman, College of Agriculture, 2021) Fones, Elizabeth Marie; Chairperson, Graduate Committee: Eric Boyd; Daniel R. Colman, Emily A. Kraus, Daniel B. Nothaft, Saroj Poudel, Kaitlin R. Rempfert, John R. Spear, Alexis S. Templeton and Eric S. Boyd were co-authors of the article, 'Physiological adaptations to serpentinization in the Samail ophiolite, Oman' in the journal 'The International Society for Microbial Ecology journal' which is contained within this dissertation.; Daniel R. Colman, Emily A. Kraus, Ramunas Stepanauskas, Alexis S. Templeton, John R. Spear and Eric S. Boyd were co-authors of the article, 'Diversification of methanogens into hyperalkaline serpentinizing environments through adaptations to minimize oxidant limitation' in the journal 'The International Society for Microbial Ecology journal' which is contained within this dissertation.; David W. Mogk, Alexis S. Templeton and Eric S. Boyd were co-authors of the article, 'Endolithic microbial carbon cycling activities in subsurface mafic and ultramafic igneous rock' which is contained within this dissertation.Serpentinization is a geochemical process wherein the oxidation of Fe(II)-bearing minerals in ultramafic rock couples with the reduction of water to generate H 2, which in turn can reduce inorganic carbon to biologically useful substrates such as carbon monoxide and formate. Serpentinization has been proposed to fuel a subsurface biosphere and may have promoted life's emergence on early Earth. However, highly reacted waters exhibit high pH and low concentrations of potential electron acceptors for microbial metabolism, including CO 2. To characterize how serpentinization shapes the distribution and diversity of microbial life, direct cell counts, microcosm-based activity assays, and genomic inferences were performed on environmental rock and water samples from the Samail Ophiolite, Oman. Microbial communities were shaped by water type with cell densities and activities generally declining with increasing pH. However, cells inhabiting highly reacted waters exhibited adaptations enabling them to minimize stresses imposed by serpentinization, including preferentially assimilating carbon substrates for biomolecule synthesis rather than dissimilating them for energy generation, maintaining small genomes, and synthesizing proteins comprised of more reduced amino acids to minimize energetic costs and maximize protein stability in highly reducing waters. Two distinct lineages of a genus of methanogens, Methanobacterium, were recovered from subsurface waters. One lineage was most abundant in high pH waters exhibiting millimolar concentrations of H2, yet lacked two key oxidative [NiFe]-hydrogenases whose functions were presumably replaced by formate dehydrogenases that oxidize formate to yield reductant and CO 2. This allows cells to overcome CO 2/oxidant limitation in high pH waters via a pathway that is unique among characterized Methanobacteria. Finally, gabbro cores from the Stillwater Mine (Montana, U.S.A) were used to develop methods for detecting the activities of cells inhabiting mafic to ultramafic igneous rocks while controlling for potential contaminants. Optimized protocols were applied to rock cores from the Samail Ophiolite, where rates of biological formate and acetate metabolism were higher in rocks interfacing less reacted waters as compared with more extensively reacted waters, and in some cases may greatly exceed activities previously measured in fracture waters. This dissertation provides new insights into the distribution, activities, and adaptations exhibited by life in a modern serpentinizing environment.Item Influence of lithogenic energy on subglacial microbial community composition(Montana State University - Bozeman, College of Agriculture, 2021) Dunham, Eric Corwin; Chairperson, Graduate Committee: Eric Boyd; John E. Dore, Mark L. Skidmore, Eric E. Roden and Eric S. Boyd were co-authors of the article, 'Lithogenic hydrogen supports microbial primary production in subglacial and proglacial environments' in the journal 'Proceedings of the National Academy of Sciences of the United States of America' which is contained within this dissertation.; K. Rebecca Mitchell, Mark L. Skidmore and Eric S. Boyd were co-authors of the article, 'Influence of ferric iron on community composition in a basaltic glacial catchment' which is contained within this dissertation.Chemosynthesis, the generation of biomass using chemical energy, supported life on early Earth and continues to sustain contemporary light-independent ecosystems. The mechanisms of nutrient release from the geosphere are critical to understanding the present and historical distribution and diversity of life. Glaciers release such nutrients through comminution of bedrock, continuously resurfacing reactive minerals that can be colonized and exploited by chemosynthetic microorganisms. Bedrock mineralogy influences the nutrients available in these environments, but little is known about which nutrients are most important or how they affect microbial community composition, particularly in catchments overlying igneous bedrock like basalt. Iron and silicate minerals, common in basalt, readily generate both reductants such as H 2 and oxidants such as Fe(III) through interactions with water. Abundant H 2 in meltwaters of the basalt-based Icelandic glacier Kotlujokull (KJ) were found to support sediment microbial communities better adapted to use H 2 in chemosynthetic metabolism than those found beneath the carbonate-based Robertson Glacier (RG), Canada. KJ communities exhibited shorter lag-times and faster rates of net H 2 oxidation and dark carbon dioxide (CO 2) fixation than those from RG. A KJ sediment enrichment culture provided with H 2, CO 2, and Fe(III) produced a chemolithoautotrophic population related to Rhodoferax ferrireducens, which was also detected using molecular techniques in sediments from Kaldalonsjokull (Kal), another basalt-based Icelandic glacier. The abundance and composition of microbial communities that colonized defined minerals incubated for 12 months in Kal meltwater streams were examined by extracting DNA and sequencing PCR-amplifiable 16S rRNA genes. DNA quantities and the composition of 16S rRNA genes recovered from Kal sediments were most similar to those recovered from incubated Fe(III)-bearing minerals hematite and magnetite, with putative Fe(III) reducers dominating all three communities. These findings point to the importance of bedrock mineral composition in influencing the supplies of nutrients like H 2 and Fe(III) that, in turn, influence the diversity, abundance, and activity of microbial communities in subglacial environments. They further indicate the potential for subglacial habitats to serve as refugia for microbial communities in the absence of sunlight, such as during Snowball Earth episodes, or on icy planets without photosynthetic life.