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Spatial and Temporal Dynamics of Microorganisms Living Along Steep Energy Gradients and Implications for Ecology and Geologic Preservation in the Deep Biosphere

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Spatial and Temporal Dynamics of Microorganisms Living Along Steep Energy Gradients and Implications for Ecology and Geologic Preservation in the Deep Biosphere Spatial and Temporal Dynamics of Microorganisms Living Along Steep Energy Gradients and Implications for Ecology and Geologic Preservation in the Deep Biosphere Thesis by Sean William Alexander Mullin In Partial Fulfillment of the Requirements for the degree of Doctor of Philosophy CALIFORNIA INSTITUTE OF TECHNOLOGY Pasadena, California 2020 (Defended 8 June 2020) ii ã 2020 Sean W. A. Mullin ORCID: 0000-0002-6225-3279 iii What is any man’s discourse to me, if I am not sensible of something in it as steady and cheery as the creak of crickets? In it the woods must be relieved against the sky. Men tire me when I am not constantly greeted and refreshed as by the flux of sparkling streams. Surely joy is the condition of life. Think of the young fry that leap in ponds, the myriads of insects ushered into being on a summer evening, the incessant note of the hyla with which the woods ring in the spring, the nonchalance of the butterfly carrying accident and change painted in a thousand hues upon its wings… —Henry David Thoreau, “Natural History of Massachusetts” iv ACKNOWLEDGEMENTS Seven years is a long time. Beyond four years, the collective memory of a university is misty and gray, and if it were a medieval map, would be marked simply, “Here be dragons.” The number of times I have been mistaken this past year for an aged staff scientist or long-suffering post-doc would be amusing if not for my deepening wrinkles serving to confirm my status as a relative dinosaur. Wrinkles aside, I can happily say that my time spent in the Orphan Lab has been one of tremendous growth and exploration. I am extremely fortunate to have enjoyed the company of brilliant people who have inspired, challenged, amused, supported, and comforted me through it all. I have grown in grad school as both a scientist and a person, in no small part due to their impact on my life. First, I want to thank Victoria. I already appreciate the amount of work you do behind the scenes to keep the lab running, obtain opportunities for students, and maintain connections with the outside world, but I suspect that as time passes, I will appreciate those things even more. I have learned a tremendous amount from you, not least of which are the ways to communicate my science to the outside world to spark their interest. In a world of increasingly chaotic noise, I suspect these skills will be invaluable for the rest of my life. Getting to know you better on cruises has been a real joy and your passion for science has been infective — a real boon whenever my pessimism threatens. I also need to thank my fellow geobiology students and post-docs, both former and current, for being a tremendous support network. I still vividly recall starting out at Caltech. Coming from a large school, I expected to feel alone, particularly once I found out that I was the only geobiology student of the year. The warmth with which the older students so thoroughly accepted me took me aback but has since become aspirational as I have aged into the role of elder grad student. In particular, I want to thank Jena Johnson, Sarah Slotznick, Elizabeth Trembath-Reichert, and Lewis Ward for their welcome and friendship. Y’all are amazing. Of course, those students have since graduated, but the new geobiology crew has never ceased to impress, especially my officemates in 102. Special thanks to John Magyar, Usha Lingappa, Gray Chadwick, Kyle Metcalfe, Cecilia Sanders, Aditi Narayanan, and Alon Philosof for their friendship and willingness to celebrate each other’s successes and commiserate with the setbacks. A few scientific thanks are also deeply required here, in particular to a handful of postdocs who helped teach me the ways. Thank you to Greg Wanger, who was a driving force behind getting the v BLM-1 project off the ground, and to Brittany Kruger, who helped see it to completion. Thank you also to Kat Dawson, who I had met in lab but really got to know in Costa Rica. Seventy cores was a tall order for a two-person team, but we managed. I am glad to call you a friend and collaborator (plus somehow you are able to hear me perfectly even when I mumble and it honestly surprises me every time). Haley Sapers has also been a constant scientific sounding board for the past several years, someone with a seemingly boundless capacity to give and think, as well as a great travel companion. Your desire to do everything to the maximum degree and my tendency to efficiency (perhaps born of laziness) has been a potent combination. I absolutely must thank Stephanie Connon, the Orphan Lab Manger, as well. I honestly do not understand how you keep everything straight in the lab will all the projects running. Somehow, though, you handle it all with both diligence and grace. I have been lucky to have made many friends outside of the Orphan Lab, too, and I cannot imagine what my life would have been like without their personal support. Giuliana Viglione, Kelvin Bates, Elle Chimiak, Al Chan, and Ollie Stephenson — thank you. You mean the world to me. Nancy Sulahian of the Glee Club and Taso Dimitriadis of the Center for Diversity have also been critical parts of my life here, giving me the opportunity to use some different parts of my brain and good friends besides. I want to thank my friends outside of Caltech too, for when I just need a break: Andrew Chen, Matt Franscioni, David Binsacca, Katie Papoe and Erik Wong, and Martín Hernandez. Thank you for reminding of the world abroad. To my parents and my family in general, thank you. I am fortunate to have you so close and your support has never stopped. My cousins Ken and Nick showed me around LA when I first visited to convince me to come here, and it worked! Aunt Donna and Bennet — I have so appreciated your interest in my life and my science. And of course to my parents, I cannot express enough thanks. I wrote in my application for Caltech that my scientific curiosity came from you, and that remains true. You have been patient, interested, supportive, and kind. Problems never feel unsurmountable when I talk to you. Lastly, I want to thank James. The past four years with you have been a delight, truly, and I cannot imagine them any differently. You are the rarified air keeping me afloat, and I keep thoughts of you close at hand at all times as a little source of joy and light my life. I look forward to our future. vi ABSTRACT The deep biosphere represents a massive repository of life with unknown effects on global biogeochemical cycles. Even the fundamental life strategies of the endemic microorganisms that inhabit this biome remain enigmatic; some studies have indicated that subsurface organisms subsist in energetic regimes below the theoretical lower limit for life. A boom-bust life cycle, mediated by tectonic disturbances and subsurface fractures, may help explain these phenomena. This work addresses and expands on this question, first by exploring the response of continental deep biosphere microorganisms to an in situ organic matter amendment, then by analyzing the microbial community dynamics of the sediments and carbonate along a naturally-occurring energy gradient at a methane seep. Our experiments in the continental deep biosphere confirmed that mineralogical heterogeneity can drive differential colonization of the native microorganisms, implying that selection and adaptation to in situ conditions occurs, differentiating individual microbial niches. We also observed the formation of secondary framboidal iron sulfide minerals, a well-known phenomenon in marine sediments but not extensively observed in the deep subsurface, that were correlated to the presence of abundant sulfur-metabolizing microorganisms. Chapters 2 and 3 are instead focused on the microbial ecology of a methane seep on the Pacific margin of Costa Rica. Cold methane seeps themselves represent sharp boundaries between the generally low-energy background seafloor and abundant chemical energy in the form of methane. Chapter 2 describes that the microorganisms living at these seeps occupy a significantly narrower spatial scale than the endemic megafauna. In addition, by correlating community dissimilarity and geographic distance, the functional center of the seep was identified, allowing for insight into the ecological differentiation between clades of anaerobic methanotrophic archaea (ANME). Chapter 3 examines in greater detail the endolithic microbial community, principally composed of ANME-1. By conducting transplantation experiments of carbonates on the seafloor, we tested the response of the in situ endolithic communities and found that carbonates moved distinctly outside the active zone changed less than communities moved to regions of less activity. vii PUBLISHED CONTENT AND CONTRIBUTIONS Mullin, S.W. et al. (2020). “Patterns of In Situ Mineral Colonization by Microorganisms in a ~60°C Deep Continental Subsurface Aquifer”. Frontiers in Microbiology (accepted). S.W.M. participated in the conception of the project, gathered field data, extracted and analyzed the DNA, performed the microscopy, and wrote the manuscript. Mullin, S.W., et al. (2020). “Correlating the Microbial and Animal Communities with Biogeochemistry at a Cold Methane Seep in the Costa Rica Pacific Margin”. In prep S.W.M. participated in the conception of the project, participated in the cruise, participated in extracting DNA, analyzed all DNA data, geochemistry, and spatial mapping, and wrote the manuscript. Mullin, S.W., et al. (2020). “Microbial community dynamics and succession in methane seep carbonates”. In prep S.W.M. participated in the conception of the project, participated in the cruise, participated in extracting DNA, analyzed all DNA data, and wrote the manuscript.
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