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ANAEROBIC HALOPHILIC ALKALITHERMOPHILES: DIVERSITY and PHYSIOLOGICAL ADAPTATIONS to MULTIPLE EXTREME CONDITIONS by NOHA MOSTAFA

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ANAEROBIC HALOPHILIC ALKALITHERMOPHILES: DIVERSITY and PHYSIOLOGICAL ADAPTATIONS to MULTIPLE EXTREME CONDITIONS by NOHA MOSTAFA ANAEROBIC HALOPHILIC ALKALITHERMOPHILES: DIVERSITY AND PHYSIOLOGICAL ADAPTATIONS TO MULTIPLE EXTREME CONDITIONS by NOHA MOSTAFA MESBAH (Under the Direction of Juergen Wiegel) ABSTRACT Halophilic alkalithermophiles are poly-extremophiles adapted to grow at high salt concentrations, alkaline pH values and temperatures greater than 50ºC. Halophilic alkalithermophiles are of interest from physiological perspectives as they combine unique adaptive mechanisms and cellular features that enable them to grow under extreme conditions. The alkaline, hypersaline lakes of the Wadi An Natrun, Egypt were chosen as sources for isolation of novel halophilic alkalithermophiles. These lakes are characterized by saturating concentrations of NaCl (5.6 M), alkaline pH (8.5-11) and temperatures of 50ºC due to intense solar irradiation. The prokaryotic communities of three large lakes of the Wadi An Natrun were assessed using 16S rRNA clone libraries. The Wadi An Natrun lakes are dominated by three phylogenetic groups of Bacteria (Firmicutes, Bacteroidetes, α- and γ-proteobacteria) and two groups of Archaea (Halobacteriales and Methanosarcinales). Extensive diversity exists within each phylogenetic group; half of the clones analyzed did not have close cultured or uncultured relatives. Three novel halophilic alkalithermophiles were isolated from the Wadi An Natrun. A novel order, Natranaerobiales, was proposed to encompass these novel isolates. Natranaerobius thermophilus was chosen as a model for more detailed physiological studies. Analysis of the bioenergetic characteristics of N.thermophilus revealed the absence of cytoplasmic pH homeostasis. Rather, N.thermophilus has the novel feature of maintaining the cytoplasmic pH at a constant 1 unit below that of the extracellular pH, the cytoplasmic pH continuously changed with the extracellular pH. To investigate the mechanism of this dynamic cytoplasmic pH regulation, genes encoding putative cation/proton antiporter proteins were functionally characterized. The physiological characteristics of these cation/proton antiporters were well suited to the intracellular conditions of N.thermophilus. Collectively, antiporter proteins function over the whole pH range for growth of N.thermophilus and display antiport activity over a wide range of Na+ ion concentrations. Thus, they are capable of providing active cytoplasmic acidification even if the intracellular environment of N.thermophilus changes. Most of the antiporter proteins belong to the NhaC family of cation/proton antiporters; a group that is primarily involved in expulsion of intracellular Na+. These results indicate that these antiporters provide N.thermophilus tolerance to both alkaline pH and high salt concentrations. INDEX WORDS: Halophile, Alkaliphile, Thermophile, Extremophile, Alkalithermophile, Natranaerobiales, Natranaerobius thermophilus, Natronovirga, Wadi An Natrun, Microbial diversity, Antiporter, Intracellular pH, Proton motive force, Membrane potential, Phosphorylation potential ANAEROBIC HALOPHILIC ALKALITHERMOPHILES: DIVERSITY AND PHYSIOLOGICAL ADAPTATIONS TO MULTIPLE EXTREME CONDITIONS by NOHA MOSTAFA MESBAH B. Pharm. Sci., Suez Canal University, Egypt, 2002 A Dissertation Submitted to the Graduate Faculty of The University of Georgia in Partial Fulfillment of the Requirements for the Degree DOCTOR OF PHILOSOPHY ATHENS, GEORGIA 2008 © 2008 Noha Mostafa Mesbah All Rights Reserved ANAEROBIC HALOPHILIC ALKALITHERMOPHILES: DIVERSITY AND PHYSIOLOGICAL ADAPTATIONS TO MULTIPLE EXTREME CONDITIONS by NOHA MOSTAFA MESBAH Major Professor: Juergen Wiegel Committee: James T. Hollibaugh Joy B. Doran Peterson William B. Whitman Electronic Version Approved: Maureen Grasso Dean of the Graduate School The University of Georgia December 2008 ACKNOWLEDGEMENTS There are many people I would like to thank for helping make this dissertation possible, either for helping me with my work, offering support, encouragement or both. I am thankful for my advisor, Juergen Wiegel for his guidance and support. Juergen’s sustained encouragement over the years has enabled me to reach my goals. I also appreciate the assistance of my committee members, Tim Hollibaugh, Joy Peterson, and Barny Whitman. Many thanks to my labmates, past and present: Boguslaw Lupa, Mohammed Salameh, Rob Onyenwoke, Yong Jin Lee, Isaac Wagner, Elizabeth Burgess, and Karen Bowers, for keeping the energy level and morale high. There are others at the University of Georgia who have helped me along the way that I would like to thank – Lyla Lipscomb, James and Emily Henriksen, Magda Lupa, Dana Cook, Susmitha Seshadri and Bijal Patel. I would like to thank Dr. Greg Cook and all the members of the Cook lab at the Univesity of Otago, New Zealand for helping me during my stay and for that very enjoyable cycling weekend in Clyde. Finally, I would like to thank my parents for encouraging me to pursue a career in science and for their continued support of me as I have progressed forward in my life. iv TABLE OF CONTENTS Page ACKNOWLEDGEMENTS ........................................................................................................... iv LIST OF TABLES ........................................................................................................................ vii LIST OF FIGURES ....................................................................................................................... ix CHAPTER 1 INTRODUCTION AND LITERATURE REVIEW .....................................................1 2 NOVEL AND UNEXPECTED PROKARYOTIC DIVERSITY IN WATER AND SEDIMENTS OF THE ALKALINE, HYPERSALINE LAKES OF THE WADI AN NATRUN, EGYPT ...........................................................................................51 3 NATRANAEROBIUS THERMOPHILUS GEN. NOV. SP. NOV., A HALOPHILIC, ALKALITHERMOPHILIC BACTERIUM FROM SODA LAKES OF THE WADI AN NATRUN, EGYPT, AND PROPOSAL OF NATRANAEROBIACEAE FAM. NOV. AND NATRANAEROBIALES ORD. NOV. .....................................104 4 NATRONOVIRGA WADINATRUNENSIS GEN. NOV. SP. NOV. AND NATRANAEROBIUS TRUEPERI SP. NOV., TWO HALOPHILIC, ALKALITHERMOPHILIC MICROORGANISMS FROM SODA LAKES OF THE WADI AN NATRUN, EGYPT ....................................................................126 5 BIOENERGETIC PROPERTIES AND INTRACELLULAR PH REGULATION IN NATRANAEROBIUS THERMOPHILUS, AN ANAEROBIC, HALOPHILIC ALKALITHERMOPHILIC BACTERIUM ..........................................................147 v 6 ACTIVITY PROFILES OF NA+ (K+)/H+ ANTIPORTERS FROM THE HALOPHILIC, ALKALITHERMOPHILIC NATRANAEROBIUS THERMOPHILUS ARE ADAPTIVE TO THE EXTREME ENVIRONMENT ..167 7 CONCLUSIONS........................................................................................................200 APPENDICES .............................................................................................................................204 A CALCULATION OF BIOENERGETIC PARAMETERS .......................................204 B DEPENDENCE OF SOLUTE TRANSPORT ON NA+ IN NATRANAEROBIUS THERMOPHILUS .................................................................................................210 C EFFECT OF PH ON PROTON PUMPING INTO INVERTED MEMBRANE VESICLES ............................................................................................................212 D IN VIVO EXPRESSION OF NATRANAEROBIUS THERMOPHILUS ANTIPORTER GENES ........................................................................................214 E EFFECT OF EXTRACELLULAR PH ON SOLUTE UPTAKE IN NATRANAEROBIUS THERMOPHILUS ..............................................................222 F EFFECT OF EXTRACELLULAR PH ON INTRACELLULAR PH IN ENERGIZED AND NON-ENERGIZED CELLS OF NATRANAEROBIUS THERMOPHILUS 225 vi LIST OF TABLES Page Table 1.1: Definitions of different extremophiles ..........................................................................47 Table 2.1: Physiochemical properties of the water of the Wadi An Natrun lakes under study .....83 Table 2.2: Diversity and richness indices for bacterial clone libraries ..........................................84 Table 2.3: Distribution of bacterial OTUs into phylogenetic groups ............................................85 Table 2.4: Summary of OTUs affiliated with the α-proteobacteria ...............................................86 Table 2.5: Summary of OTUs affiliated with the γ- proteobacteria ..............................................87 Table 2.6: Summary of OTUs affiliated with the δ- proteobacteria, Bacteroidetes, Firmicutes, and Spirochaetes ............................................................................................................88 Table 2.7: LIBSHUFF comparisons of bacterial clone libraries ...................................................89 Table 2.8: Diversity and richness indices for archaeal clone libraries ..........................................90 Table 2.9: LIBSHUFF comparisons of archaeal clone libraries ....................................................91 Table 3.1: Differential characteristics of strain JW/NM-WN-LFT and closely related species ..119 Table S3.1: PLFA composition of strain JW/NM-WN-LFT ........................................................122 Table 4.1: Selected characteristics that distinguish strains JW/NM-WN-LUT (and related strains) and JW/NM-WN-LH1T from Natranaerobius thermophilus ......................................142 Table 4.2: Polar and neutral fatty acid composition of strains JW/NM-WN-LUT and JW/NM- WN-LH1T ....................................................................................................................144
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