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Copyright by Marguerite Viola Langwig 2019 Copyright by Marguerite Viola Langwig 2019 The Thesis Committee for Marguerite Viola Langwig Certifies that this is the approved version of the following Thesis: Expansion of Deltaproteobacteria diversity from marine sediments reveals unique metabolic features APPROVED BY SUPERVISING COMMITTEE: Brett J. Baker, Supervisor Deana Erdner Brandi Kiel Reese Expansion of Deltaproteobacteria diversity from marine sediment reveals unique metabolic features by Marguerite Viola Langwig Thesis Presented to the Faculty of the Graduate School of The University of Texas at Austin in Partial Fulfillment of the Requirements for the Degree of Master of Science in Marine Science The University of Texas at Austin December 2019 Dedication This work is dedicated to my mom, Ann Langwig. You are in my heart forever. Acknowledgements I would like to thank Dr. Brett Baker for guiding me through this project and allowing me to grow immensely as a scientist. You have been an amazing and supportive mentor. Thank you to Valerie De Anda, your help was crucial for this work and without you I would be lost. Your questions and thinking inspire me every day. Thank you to the brohort for keeping me sane and being the most supportive and loving group of friends I could have imagined. Thank you to Lucas for a lifetime of love, laughter, and friendship. Thank you dad, Gen, and Celia, your love and phone calls helped me get through to the finish. Thank you Nina and Kiley, your training and guidance helped me build the foundation I needed to complete this project. And finally, thank you to my mom, I am here because of you and I will keep pushing to make you proud. v Abstract Expansion of Deltaproteobacteria diversity from marine sediment reveals unique metabolic features Marguerite Viola Langwig, M.S. Marine Sci The University of Texas at Austin, 2019 Supervisor: Brett J. Baker Deltaproteobacteria are a ubiquitous class of bacteria that play a substantial role in carbon and nutrient cycling. However, our understanding of Deltaproteobacteria is biased towards cultured exemplars. To better understand the biodiversity and ecology of the Deltaproteobacteria, we obtained hundreds of unique, uncultured metagenome-assembled genomes (MAGs) from a variety of coastal and deep-sea sediments. These 402 Deltaproteobacteria MAGs represent a 28% increase in Deltaproteobacteria genomes. Phylogenomic analyses revealed 12 novel lineages which consist entirely of uncultured representatives. Among these are two lineages that appear to represent a new order, which are capable of denitrification and dissimilatory nitrate reduction to ammonia (DNRA). Metabolic inference of Deltaproteobacteria MAGs reveals extensive versatility, central carbon metabolism, and a broad distribution of the Wood-Ljungdahl pathway for CO2 fixation. 54% of Deltaproteobacteria MAGs encode dissimilatory sulfite reductases (DsrAB), and for those with the ability to reduce sulfate, several dsr genes are related to those from thermophiles. This study expands the genetic catalog of Deltaproteobacteria vi and provides a better ecological context for Deltaproteobacteria worldwide. The description of these new lineages highlights that there is much to be learned about this globally distributed proteobacteria. vii Table of Contents List of Tables .......................................................................................................................x List of Figures .................................................................................................................... xi Introduction ..........................................................................................................................1 Results and Discussion ........................................................................................................3 Deltaproteobacteria phylogeny ...................................................................................3 Multigenomic entropy-based scores ...........................................................................4 Central metabolism and metabolic clustering .............................................................5 Group 0 .......................................................................................................................6 Group 1 .......................................................................................................................7 Group 2 .......................................................................................................................8 Group 3 .....................................................................................................................11 Dissimilatory sulfite reductases ................................................................................13 Conclusions ...............................................................................................................14 Methods..............................................................................................................................15 Sampling ...................................................................................................................15 Metagenomic sequencing and assembly ...................................................................15 Genome binning ........................................................................................................18 Phylogenetic analyses ...............................................................................................19 Clustering Analysis ...................................................................................................20 Dissimilatory sulfite reductases ................................................................................21 Hydrogenases ............................................................................................................22 Functional characterization of genomes ...................................................................23 viii Appendix ............................................................................................................................29 References ..........................................................................................................................42 ix List of Tables Table 1: Geochemical data taken at Guaymas Basin .........................................................35 Table 2: Oxygen profile for Mesquite Bay, Texas ............................................................36 Table 3: KEGG modules, pathways, and KO numbers used to determined completeness of pathways shown in Figure 2 ...............................................37 x List of Figures Figure 1: Updated phylogeny of Deltaproteobacteria based on a concatenation of 37 single-copy marker genes .............................................................................24 Figure 2: Percent completeness of KEGG modules for the 402 reconstructed Deltaproteobacteria genomes analyzed in this study ....................................26 Figure 3: Phylogeny of nearly 300 new NiFe Deltaproteobacteria hydrogenases .............27 Figure 4: Dissimilatory sulfite reductase (DsrA) tree ........................................................28 Figure 5: 16S rRNA maximum likelihood tree of 55 MAGs from this analysis and 94 references obtained from the ARB database. ................................................30 Figure 6: Principal component analysis of MEBS entropy scores for 1,778 Deltaproteobacteria genomes ........................................................................30 Figure 7: Dissimilatory sulfite reductase (DsrB) tree ........................................................31 Figure 8: Phylogeny of FeFe hydrogenases compared to characterized hydrogenase groups ............................................................................................................32 Figure 9: Low-dimension projection and clustering of the entropy scores for 1,778 Deltaproteobacteria genomes ........................................................................33 Figure 10: Principal component projection of a k means clustering analysis of entropy scores for 1,778 Deltaproteobacteria genomes .............................................34 xi Introduction Deltaproteobacteria are a functionally and phylogenetically diverse class of Proteobacteria with several cultured representatives (DeLong et al., 2014). These cultured organisms are capable of dissimilatory sulfate and sulfur-reduction, elemental sulfur disproportionation, aromatic hydrocarbon degradation, nitrogen fixation, dissimilatory iron-reduction, and predation (Burnham, Collart, & Highison, 1981; Schnell et al., 1989; Slobodkin et al., 2013). More recently, omics methods such as single cell genomics, de novo metagenomic assembly, and metatranscriptomics have been employed to understand the ecophysiology of uncultured Deltaproteobacteria (Jochum et al., 2018; Sheik, Jain, & Dick, 2014). These methods have been especially crucial for understanding Deltaproteobacteria in extreme environments, such as hydrothermal vents, where conditions are difficult to recreate in a laboratory setting (Anantharaman, Breier, & Dick, 2016). Hydrothermal vents are an ideal environment in which Deltaproteobacteria, and microbial physiology in general, can be studied; these systems contain a diversity of electron donors, and thus are able to support the array of metabolic pathways Deltaproteobacteria are known to utilize (Kato & Yamagishi, 2016; Martin et al., 2008) Novel Deltaproteobacteria have been
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