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University of Oklahoma Graduate College Microbial Ecology of Coastal Ecosystems: Investigations of the Genetic Potential For UNIVERSITY OF OKLAHOMA GRADUATE COLLEGE MICROBIAL ECOLOGY OF COASTAL ECOSYSTEMS: INVESTIGATIONS OF THE GENETIC POTENTIAL FOR ANAEROBIC HYDROCARBON TRANSFORMATION AND THE RESPONSE TO HYDROCARBON EXPOSURE A DISSERTATION SUBMITTED TO THE GRADUATE FACULTY in partial fulfillment of the requirements of the Degree of DOCTOR OF PHILOSOPHY By JAMIE M. JOHNSON DUFFNER Norman, Oklahoma 2017 MICROBIAL ECOLOGY OF COASTAL ECOSYSTEMS: INVESTIGATIONS OF THE GENETIC POTENTIAL FOR ANAEROBIC HYDROCARBON TRANSFORMATION AND THE RESPONSE TO HYDROCARBON EXPOSURE A DISSERTATION APPROVED FOR THE DEPARTMENT OF MICROBIOLOGY AND PLANT BIOLOGY BY ______________________________ Dr. Amy V. Callaghan, Chair ______________________________ Dr. Lee R. Krumholz ______________________________ Dr. Michael J. McInerney ______________________________ Dr. Mark A. Nanny ______________________________ Dr. Boris Wawrik © Copyright by JAMIE M. JOHNSON DUFFNER 2017 All Rights Reserved. This dissertation is dedicated to my husband, Derick, for his unwavering love and support. Acknowledgements I would like to thank my advisor, Dr. Amy Callaghan, for her guidance and support during my time as a graduate student, as well as for her commitment to my success as a scientist. I would also like to thank the members of my doctoral committee for their guidance over the years, particularly that of Dr. Boris Wawrik. I would like to also thank Drs. Josh Cooper, Chris Lyles, and Chris Marks for their friendship and support during my time at OU, both in and outside the lab. iv Table of Contents Acknowledgements………………………………………………………………….iv List of Tables………………………………………………………………………....vii List of Figures………………………………………………………………………....x Abstract……………………………………………………………………...............xiii Preface…………………………………………………………………………………1 Chapter 1: Interrogation of Chesapeake Bay Sediment Microbial Communities for Intrinsic Alkane-Utilizing Potential Under Anaerobic Conditions Abstract…………………………………………………………………………3 Introduction……………………………………………………………….........4 Materials & Methods…………………………………………………………...8 Results………………………………………………………………………...19 Discussion…………………………………………………………................27 Figures………………………………………………………………………...37 References……………………………………………………………………43 Chapter 2: Impact of Photolyzed Macondo (MC252) Crude Oil and Polycyclic Aromatic Hydrocarbons (PAHs) on Indigenous Sulfate-Reducing Microorganisms in Coastal Gulf of Mexico Sediments Abstract………………………………………………………………………..51 Introduction……………………………………………………………………52 Materials & Methods………………………………………………………….55 Results………………………………………………………………………...63 Discussion……………………………………………………………............67 Figures………………………………………………………………………...76 References……………………………………………………………………78 Chapter 3: Meta-Omic Analysis of Tar Balls: Remnants of the Deepwater Horizon Oil Spill Abstract………………………………………………………………………..86 Introduction……………………………………………………………………87 Materials & Methods…………………………………………………….……93 Results……………………………………………………………………….103 Discussion…………………………………………………………………...120 Figures…………………………………………………………………..…...135 References…………………………………………………………………..148 Appendix I: Chapter 1 Supplemental Materials……………………………….159 Appendix II: Chapter 2 Supplemental Materials………………………………190 v Appendix III: Chapter 3 Supplemental Materials……………………………..226 vi List of Tables Appendix I Table S1: Latitude & longitude coordinates of stations in Chesapeake Bay……………………………………………………………………………….…..159 Table S2: Primer sets used in assA and bssA clone generation…………..160 Table S3: Parameters of sediment microcosm set-up………………………161 Table S4: Percentage of bacterial 16S rRNA genes at the family level…….162 Table S5: Percentage of archaeal 16S rRNA genes at the family level……170 Table S6: Permutational-based multivariate analysis of variance (PerMANOVA) and multi-response permutation procedure (MRPP) of core bacterial and archaeal sediment communities…………………………………...172 Table S7: Diversity indices and descriptive information of core bacterial and archaeal sediment communites……………………………………………………173 Table S8: Copy numbers of dsrA and bacterial 16S rRNA gene sequences........................................................................................................174 Table S9: Copy numbers of mcrA and archaeal 16S rRNA gene sequences…………………………………………………………………………...175 Table S10: Detection of assA and bssA operational taxonomic units (OTUs) in sediment……………………………………………………………………………..176 Table S11: Sulfate concentrations in microcosms after 672 days of incubation……………………………………………………………………………177 Table S12: Methane production in microcosms after 672 days of incubation……………………………………………………………………………179 Appendix II Table S1: Site descriptions and latitude & longitude coordinates of sampling sites on the coast of Biloxi, Mississippi……………………………………………190 Table S2: Physical measurements of surface water at sampling sites…….191 Table S3: Ion concentrations in surface waters and overlying sediment waters………………………………………………………………………………..192 vii Table S4: Average percentage of Deltaproteobacteria sequences in T-0 sediment samples…………………………………………………………………..193 Table S5: MRPP of T-0 sediment Deltaproteobacteria communities………194 Table S6: Diversity indices and descriptive information of Deltaproteobacteria in T-0 sediment samples……………………………………………………………195 Table S7: Abundant taxa as a percentage of total Deltaproteobacteria at Site 1.......................................................................................................................196 Table S8: Abundant taxa as a percentage of total Deltaproteobacteria at Site 2………………………………………………………………………………………197 Table S9: Abundant taxa as a percentage of total Deltaproteobacteria at Site 3.......................................................................................................................198 Table S10: Changes in relative abundances of Deltaproteobacteria in T-0 and SRA sediment samples…………………………………………………………….199 Table S11: Relative abundances of deltaproteobacterial taxa in T-0 and SRA sediment samples…………………………………………………………………..201 Table S12: Sulfate reduction rates (SRRs) measured via sulfate reduction assays (SRAs) for Site 1……………………………………………………………213 Table S13: SRRs measured via SRAs for Site 2………………………………216 Table S14: SRRs measured via SRAs for Site 3. ……………………………..219 Appendix III Table S1: Relative abundance of core community taxa in preliminary sand patty samples………………………………………………………………………..226 Table S2: Latitude & longitude coordinates of sand patties collected from Fort Morgan (FM), Gulf Shores Site 1 (GS-1), and Gulf Shores Site 2 (GS-2)…….228 Table S3: Approximate weights of sand patties……………………………...229 Table S4: KEGG orthology numbers of functional marker genes………….230 Table S5: Physical measurements of surface water at sampling sites…….233 Table S6: Biomarker ratios of oil extracted from sand patties……………....233 Table S7: Number of sequences in 16S rRNA gene libraries……………….234 viii Table S8: Average relative abundances of phyla detected in sand patties, beach sand, and seawater samples………………………………………………235 Table S9: Average relative abundances of Proteobacteria from sand patties, beach sand, and seawater samples………………………………………………238 Table S10: Diversity indices of sand patties, beach sand, and seawater samples………………………………………………………………………………240 Table S11: MRPP of core microbial communities of samples collected from FM, GS-1, and GS2………………………………………………….…………………..245 ix List of Figures Chapter 1 Figure 1: Sulfate and methane depth profiles in Chesapeake Bay sediment pore water……………………………………………………………………………..37 Figure 2: Community composition of Bacteria and Archaea from Chesapeake Bay sediments based on 16S rRNA sequences…………………………………...38 Figure 3: Phylogenetic analysis of assA and bssA clones detected in Chesapeake Bay sediments………………………………………………………...39 Figure 4: Methane production in microcosms established under sulfate- reducing and methanogenic conditions……………………………………............41 Chapter 2 Figure 1: Non-metric multidimensional scaling (NMDS) ordination of Deltaproteobacteria in sediments collected from Biloxi, Mississippi…………….76 Figure 2: Sulfate reduction rates (SRRs) measured from sulfate reduction assays (SRAs) established with photolyzed or non-photolyzed MC252 source oil and PAHs……………………………………………………………………………..77 Chapter 3 Figure 1: Relative abundances of saturate, aromatic, and oxygenated fractions in oil extracted from Gulf of Mexico (GoM) sand patties………..…….135 Figure 2: Microbial communities associated with GoM sand patties, beach sand, and seawater based on 16S rRNA sequences……………………………136 Figure 3: NMDS ordination of core microbial communities sequenced from sand patties, beach sand, and seawater………………………………………….142 Figure 4: Heatmap of functional marker genes involved in nutrient cycling, aerobic hydrocarbon transformation, and anaerobic hydrocarbon transformation pathways from sand patties, beach sand, and seawater……………………….143 Appendix I Figure S1: Map of Chesapeake Bay sampling sites……………………….…180 Figure S2: Dissolved oxygen (DO) depth profiles of Chesapeake Bay from 2009.................................................................................................................181 Figure S3: DO depth profiles of Chesapeake Bay from 2010………………..181 x Figure S4: NMDS ordination of core bacterial and archaeal communities…………………………………………………………………………182 Figure S5: Distribution of sulfate-reducing microorganisms and methanogens in sediment horizons………………………………………………………………..183 Figure S6: Microcosm sulfate loss……………………………………………..185 Appendix II Figure S1: NMDS ordination of T-0
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