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Electron Donors and Acceptors for Members of the Family Beggiatoaceae

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Electron Donors and Acceptors for Members of the Family Beggiatoaceae Electron donors and acceptors for members of the family Beggiatoaceae Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften - Dr. rer. nat. - dem Fachbereich Biologie/Chemie der Universit¨at Bremen vorgelegt von Anne-Christin Kreutzmann aus Hildesheim Bremen, November 2013 Die vorliegende Doktorarbeit wurde in der Zeit von Februar 2009 bis November 2013 am Max-Planck-Institut f¨ur marine Mikrobiologie in Bremen angefertigt. 1. Gutachterin: Prof. Dr. Heide N. Schulz-Vogt 2. Gutachter: Prof. Dr. Ulrich Fischer 3. Pr¨uferin: Prof. Dr. Nicole Dubilier 4. Pr¨ufer: Dr. Timothy G. Ferdelman Tag des Promotionskolloquiums: 16.12.2013 To Finn Summary The family Beggiatoaceae comprises large, colorless sulfur bacteria, which are best known for their chemolithotrophic metabolism, in particular the oxidation of re- duced sulfur compounds with oxygen or nitrate. This thesis contributes to a more comprehensive understanding of the physiology and ecology of these organisms with several studies on different aspects of their dissimilatory metabolism. Even though the importance of inorganic sulfur substrates as electron donors for the Beggiatoaceae has long been recognized, it was not possible to derive a general model of sulfur compound oxidation in this family, owing to the fact that most of its members can currently not be cultured. Such a model has now been developed by integrating information from six Beggiatoaceae draft genomes with available literature data (Section 2). This model proposes common metabolic pathways of sulfur compound oxidation and evaluates whether the involved enzymes are likely to be of ancestral origin for the family. In Section 3 the sulfur metabolism of the Beggiatoaceae is explored from a dif- ferent perspective. Besides oxidizing stored elemental sulfur further to sulfate, members of this family can use sulfur as a terminal electron acceptor under anoxic conditions. So far, sulfur respiration in the Beggiatoaceae has only been discussed in the context of energy acquisition, but the here presented data suggest that this reaction could also be employed to dispose of stored sulfur when sulfide is oxidized at high rates. If strongly sulfidic conditions and high sulfide oxidation rates per- sist, sulfur can accumulate in such an excessive manner that the cell integrity can eventually not be maintained. Reduced sulfur compounds are surely the most important electron donors for chemolithoautotrophically growing Beggiatoaceae, but the traditional focus on this topic has left other possible inorganic electron donors largely unexplored. Hence, a major part of this thesis is dedicated to investigating the capacity of Beggiatoaceae I to use molecular hydrogen as an electron donor. Physiological experiments have shown that a chemolithoautotrophic Beggiatoa strain oxidizes hydrogen at high rates and under various conditions, indicating that hydrogen could play an impor- tant role in the metabolism of the Beggiatoaceae (Section 4.1). The physiological studies on hydrogen oxidation have been complemented by screening all avail- able Beggiatoaceae draft genomes and several cultured members of the family for hydrogenase-encoding genes (Section 4.2). [NiFe]-hydrogenase genes from four phylogentically and functionally distinct clades have been identified repeatedly, illustrating that the capacity for hydrogen oxidation in the Beggiatoaceae is likely both, widespread and versatile. The possible influence of hydrogen oxidation on the metabolic plasticity of the Beggiatoaceae is discussed and environmental set- tings are pointed out, in which hydrogen oxidation could be important for members of the family. In recent years, it became evident that molecular hydrogen can indeed be an im- portant electron donor for sulfur bacteria of very different phylogenetic origin and lifestyle. The general discussion of this thesis therefore presents a comparison of how much energy members of the family Beggiatoaceae—and sulfur bacteria in general—could gain from the oxidation of reduced sulfur compounds and molec- ular hydrogen (Section 5). This comparison includes both, thermodynamic and biochemical considerations. II Zusammenfassung Die Familie Beggiatoaceae umfasst große, farblose Schwefelbakterien, die f¨ur ihren chemolithotrophen Stoffwechsel, im speziellen die Oxidation reduzierter Schwe- felverbindungen mit Sauerstoff und Nitrat, bekannt sind. Die vorliegende Ar- beit tr¨agt mit verschiedenen Studien zum dissimilatorischen Stoffwechsel zu einem tiefergehenden Verst¨andnis der Physiologie und Okologie¨ dieser Organismen bei. Obwohl anorganische Schwefelverbindungen seit jeher als wichtige Elektronendo- natoren f¨ur diese Familie angesehen werden, war es bis jetzt nicht m¨oglich ein allgemeines Modell f¨ur die Oxidation von Schwefelverbindungen innerhalb der Familie aufzustellen, da die meisten ihrer Mitglieder zur Zeit nicht kultivierbar sind. Ein solches Modell wurde jedoch jetzt entwickelt, indem Informationen aus sechs teilsequenzierten Genomen aus der Familie mit verf¨ugbaren Literatur- daten zusammengefasst wurden (Abschnitt 2). Im Rahmen dieses Modells wer- den gemeinsame Stoffwechselwege der Schwefeloxidation vorgeschlagen und die Urspr¨unglichkeit der betreffenden Enzyme f¨ur die Familie wird abgesch¨atzt. In Abschnitt 3 wird der Schwefelstoffwechsel der Familie Beggiatoaceae aus einer anderen Perspektive betrachtet. Neben der Oxidation zu Sulfat kann gespeicherter Elementarschwefel von Mitgliedern dieser Familie auch als termi- naler Elektronenakzeptor verwendet werden. Bis jetzt wurde Schwefeloxidation in den Beggiatoaceae nur aus Sicht des Energiegewinns betrachtet, aber die hier pr¨asentierten Daten weisen darauf hin, dass diese Reaktion auch bei hohen Sulfid- Oxidationsraten genutzt werden k¨onnte um gespeicherten Schwefel zu entsorgen. F¨ur den Fall dass stark sulfidische Bedingungen und hohe Sulfid-Oxidationsraten uber¨ l¨angere Zeit anhalten, kann Schwefel so ausgiebig eingelagert werden, dass schlussendlich die Zellintegrit¨at nicht mehr aufrecht erhalten werden kann. III Reduzierte Schwefelverbindingen sind mit Sicherheit die wichtigsten Elektronen- donatoren f¨ur chemolithoautotroph wachsende Beggiatoaceae, aber durch die lan- ganhaltende Fokussierung auf dieses Thema wurden andere m¨ogliche anorganische Elektronendonatoren kaum untersucht. Daher besch¨aftigt sich ein Hauptteil dieser Arbeit damit, die F¨ahigkeit der Beggiatoaceae molekularen Wasserstoff zu ox- idieren, zu untersuchen. Physiologische Experimente haben gezeigt, dass ein chemolithoautotropher Beggiatoa-Stamm Wasserstoff mit hohen Raten und unter verschiedensten Bedingungen oxidiert, so dass Wasserstoff im Metabolismus der Familie eine wichtige Rolle spielen k¨onnte (Abschnitt 4.1). Die physiologischen Studien zur Wasserstoffoxidation sind um eine Uberpr¨¨ ufung der verf¨ugbaren teilse- quenzierten Beggiatoaceae-Genome und verschiedener kultivierter Mitglieder der Familie auf Hydrogenase-Gene erg¨anzt worden (Abschnitt 4.2). Die wiederholte Identifizierung von [NiFe]-Hydrogenasen aus vier phylogenetisch und funktionell verschiedenen Gruppen weist darauf hin, dass die F¨ahigkeit zur Wasserstoffoxida- tion in der Familie Beggiatoaceae wahrscheinlich sowohl weit verbreitet als auch vielseitig ist. Der m¨oglich Einfluss von Wasserstoffoxidation auf die metabolische Anpassungsf¨ahigkeit der Beggiatoaceae wird diskutiert, genauso wie nat¨urliche Umgebungen, in denen Wasserstoffoxidation eine wichtige Funktion f¨ur Mitglieder der Familie erf¨ullen kann. In den letzten Jahren wurde vermehrt deutlich, dass molekularer Wasserstoff in der Tat ein wichtiger Elektronendonator f¨ur Schwefelbakterien von unterschiedlichstem phylogenetischen Ursprung und Lebensstil sein kann. Die Gesamtdiskussion dieser Arbeit (Abschnitt 5) widmet sich daher der Frage wie viel Energie Mitglieder der Familie Beggiatoaceae — und Schwefelbakterien im Allgemeinen — mit der Oxidation reduzierter Schwefelverbindungen gewinnen k¨onnen. Dieser Vergleich ber¨ucksichtigt sowohl thermodynamische als auch biochemische Uberlegungen.¨ IV Contents Summary I Zusammenfassung III List of Figures VII List of Tables IX List of Abbreviations X 1 Introduction 1 1.1 The family Beggiatoaceae .......................... 1 1.1.1 Members of the family Beggiatoaceae belong to the physio- logicalgroupofsulfurbacteria.................. 1 1.1.2 Morphologicalandphylogeneticdiversity............ 4 1.1.3 Physiology.............................. 7 1.2 Sulfur cycling ................................. 12 1.3 Enzymesofsulfurcompoundoxidation.................. 16 1.3.1 Oxidation of sulfide to elemental sulfur ............. 17 1.3.2 Oxidation of elemental sulfur to sulfite ............. 18 1.3.3 Oxidation of sulfite to sulfate ................... 20 1.3.4 Oxidationofthiosulfate...................... 22 1.3.5 Productionofreducingequivalents................ 24 1.4 Molecularhydrogeninthebiosphere................... 25 1.5 Enzymesofhydrogenmetabolism..................... 28 1.5.1 Hydrogenases............................. 28 V Contents 1.5.2 [NiFe]-hydrogenases......................... 30 1.5.3 Phylogeneticclustersof[NiFe]-hydrogenases.......... 31 1.5.4 Nitrogenaseisanhydrogen-evolvingprotein.......... 34 1.6 Objectives ................................... 36 2 Beggiatoaceae genomes 67 2.1 Oxidative sulfur metabolism in the family Beggiatoaceae ....... 69 3 Sulfur respiration in Beggiatoaceae 119 3.1 Sulfur respiration in a marine Beggiatoa strain.............121 4 Hydrogen oxidation by members of the family Beggiatoaceae 145 4.1 Hydrogen oxidation
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    University of Akureyri Department of Natural Resource Science 7. References Ammann, E. C., Reed, L. L., & Durichek, J. J. (1968). Gas consumptions and Growth Rate of Hydrogenomonas eutropha in Continuous Culture. Applied Microbiology , 16, (6), 822-826. Aguiar, P., Beveridge, T. J., & Reysenbach, A.-L. (2004). Sulfurihydrogenibium azorense, sp. nov., a thermophilic hydrogen oxidizing microaerophile from terrestrial hot springs in the Azores. International Journal of Systematic and Evolutionary Microbiology , 54, 33-39. Altschul, S., Gish, W., Miller, W., Myers, E., & Lipman, D. (1990). "Basic local alignment search tool.". J. Mol. Biol. , 215:403-410. Amend, J., & Shock, E. (2001). Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and Bacteria. FEMS Microbiology Reviews , 25, 175-243. Aragno, M. (1978). Enrichment, isolation and preliminary characterization of a thermophilic, endospore-forming hydrogen bacterium. FEMS Micobiol. Lett. , 3: 13-15. Aragno, M. (1992). The Thermophilic, Aerobic, Hydrogen-Oxidizing (Knallgas) Bacteria. In A. Balows, H. Trüper, M. Dworkin, W. Harder, & K. Schleifer, The Prokaryotes, a handbook on biology of bacteria. 2nd ed. vol. 4 (pp. 3917-3933.). New York: Springer Verlag. Aragno, M., & Schlegel, H. G. (1992). The mesophilic Hydrogen-Oxidizing (Knallgas) Bacteria. In A. Balows, H. Truper, M. Dworkin, W. Harder, & K.-H. Schleifer, The Prokaryotes 2nd. ed. (pp. 344-384). New York: Springer. Ármannson, H. (2002, May 30-31). Erindi á ráðstefnu um málefni veitufyrirtækja . Grænt bókhald í jarðhita- samanburður á útblæstri við aðra orkugjafa . Akureyri, Iceland: Samorka. Bae, S., Kwak, K., Kim, S., Chung, S., & Igarashi, Y. (2001). Isolation and Characterization of CO2-Fixing Hydrogen -Oxidizing Marine 109 University of Akureyri Department of Natural Resource Science Bacteria.
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