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Hydrocarbon-Degrading Sulfate-Reducing Bacteria in Marine Hydrocarbon Seep Sediments

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Hydrocarbon-Degrading Sulfate-Reducing Bacteria in Marine Hydrocarbon Seep Sediments Hydrocarbon-degrading sulfate-reducing bacteria in marine hydrocarbon seep sediments Sara Kleindienst Cover: 13 C-mass images of alkane-degrading SRB from Amon Mud Volcano or Guaymas Basin marine seep sediments as determined by NanoSIMS analysis. Hydrocarbon-degrading sulfate-reducing bacteria in marine hydrocarbon seep sediments Dissertation zur Erlangung des Grades eines Doktors der Naturwissenschaften - Dr. rer. nat. - Dem Fachbereich Biologie/Chemie der Universität Bremen vorgelegt von Sara Kleindienst Bremen April 2012 Die vorliegende Arbeit wurde in der Zeit von September 2008 bis April 2012 im Rahmen der „International Max Planck Research School of Marine Microbiology (MarMic)“ in der Abteilung Molekulare Ökologie am Max-Planck-Institut für marine Mikrobiologie in Bremen angefertigt. 1. Gutachter: Prof. Dr. Rudolf Amann 2. Gutachter: Prof. Dr. Heribert Cypionka Tag des Promotionskolloquiums: 24. Mai 2012 Table of Contents Table of Contents Summary................................................................................................................................ III Zusammenfassung..................................................................................................................IV List of Abbreviations............................................................................................................... V Chapter I ................................................................................................................................... 1 General Introduction ........................................................................................................... 1 1. Hydrocarbons .............................................................................................................. 1 2. Hot spots of hydrocarbon sources in the ocean........................................................... 3 2.1. Hydrothermal vents............................................................................................ 3 2.2. Cold seeps .......................................................................................................... 4 2.3. Anthropogenic oil spills ..................................................................................... 8 3. Benthic communities at hydrocarbon seeps................................................................ 9 3.1. Chemosynthetic communities ............................................................................ 9 3.2. Microbial communities ...................................................................................... 9 4. Microbial non-methane hydrocarbon-degradation in anoxic seep sediments........... 11 4.1. Cultured non-methane hydrocarbon degrading SRB ....................................... 13 4.2. Metabolic pathways for anaerobic hydrocarbon degradation by SRB............. 14 5. Stable-isotope probing techniques in microbial ecology .......................................... 17 Objectives of this thesis...................................................................................................... 20 Contribution to manuscripts............................................................................................. 22 Chapter II................................................................................................................................ 24 Distribution and in situ abundance of sulfate-reducing bacteria in diverse marine hydrocarbon seep sediments ............................................................................................. 24 Chapter III.............................................................................................................................. 59 Specialists instead of generalists oxidize alkanes in anoxic marine hydrocarbon seep sediments..................................................................................................................... 59 Chapter IV .............................................................................................................................. 90 Activity and in situ abundance of alkane-degrading sulfate-reducing bacteria at marine hydrocarbon seeps................................................................................................. 90 Chapter V.............................................................................................................................. 127 Impact of natural oil and higher hydrocarbons on microbial diversity, distribution and activity in Gulf of Mexico cold seep sediments ................................ 127 Chapter VI ............................................................................................................................ 129 Synopsis of Results, General Discussion and Conclusions ........................................... 129 1. DSS hydrocarbon degraders at marine seeps .......................................................... 129 1.1. SCA-SRB1 are global key players involved in short-chain alkane degradation..................................................................................................... 131 1.2. SCA-SRB2 are Guaymas Basin-endemic short-chain alkane degraders ....... 135 1.3. LCA-SRB1 are long-chain alkane degraders................................................. 136 1.4. SEEP-SRB1 are globally abundant candidates for hydrocarbon degradation136 2. Non-DSS hydrocarbon degraders at marine seeps.................................................. 137 2.1. SEEP-SRB2 are novel ANME-partners involved in AOM ........................... 137 2.2. SEEP-SRB3 and SEEP-SRB4 are candidates for hydrocarbon degradation . 140 2.3. LCA-SRB2 are global key players involved in long-chain alkane degradation..................................................................................................... 140 2.4. Desulfobacterium anilini and relatives are involved in oil degradation ........ 141 3. Unexplored groups involved in hydrocarbon degradation at marine seeps ............ 142 4. Environmental impact of hydrocarbon-degrading SRB.......................................... 144 4.1. Cellular activities of alkane-degrading SRB.................................................. 144 4.2. SR rates coupled to alkane oxidation at hydrocarbon seeps .......................... 145 I Table of Contents 5. Future Perspectives ................................................................................................. 146 References ............................................................................................................................. 148 Acknowledgements............................................................................................................... 159 Appendix ............................................................................................................................... 161 Curriculum Vitae ................................................................................................................. 182 II Summary Summary Microorganisms are key players in our biosphere because of their ability to degrade various organic compounds including a wide range of hydrocarbons. At marine hydrocarbon seeps, more than 90% of sulfate reduction (SR) is potentially coupled to non-methane hydrocarbon oxidation. Several hydrocarbon-degrading sulfate-reducing bacteria (SRB) were enriched or isolated from marine sediments. However, in situ active SRB remained largely unknown. In the present thesis, the global distribution and abundance of SRB at diverse gas and hydrocarbon seeps was investigated by catalyzed-reporter deposition fluorescence in situ hybridization (CARD-FISH). The majority of Deltaproteobacteria was assigned to specific SRB groups, for instance on average 83% and 61% at gas and hydrocarbon seeps. Members of the Desulfosarcina/Desulfococcus (DSS) clade significantly dominated all sites, suggesting their important role in hydrocarbon degradation processes. Furthermore, butane- and dodecane-degrading SRB were identified from two contrasting marine hydrocarbon seeps using 13 C-stable-isotope probing techniques. The identified key players affiliated with four distinct groups, of which three belonged to the DSS clade. Specific groups were, according to their ability to oxidize short-chain alkanes (SCA) or long-chain alkanes (LCA), denoted as “SCA-SRB1” and “SCA-SRB2” as well as “LCA-SRB1” and “LCA-SRB2”. Based on the obtained data it is assumed that diverse and highly specialized DSS organisms are involved in hydrocarbon degradation at marine seeps rather than generalists of one dominant subgroup. At marine hydrocarbon seeps, groups SCA-SRB1 and SCA-SRB2 constituted up to 31 and 9% of all Deltaproteobacteria , respectively. In addition, LCA-SRB2 comprised up to 6% of all detected Deltaproteobacteria . Furthermore, activities for these groups were analyzed on the cellular level by Nanometer-scale Secondary Ion Mass Spectrometry (NanoSIMS). Alkane oxidation rates for specific groups were determined to be on average between 45 and 58 amol butane and 1 amol dodecane per cell and per day. Extrapolated data indicate that specific alkane-degrading SRB groups have the potential to contribute up to 100% of the total SR rates at seeps from the Gulf of Mexico. Therefore, alkane-degrading SRB groups may significantly impact sulfur and carbon cycles at marine hydrocarbon seeps. In addition, based on the obtained data, members of the uncultured group SEEP-SRB2 are hypothesized to be involved in hydrocarbon degradation. SEEP-SRB2 were visualized for the first time using CARD-FISH and were detected
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