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Starvation in Bacteria Starvation in Bacteria Starvation in Bacteria Starvation in Bacteria Edited by Staffan Kjelleberg University 0/ Göteborg Göteborg, Sweden and University 0/ New South Wales Sydney, Australia SPRINGER SCIENCE+BUSINESS MEDIA, LLC Library of Congress Cataloging-In-Publication Data Starvation 1n bacteria / edited by Staffan Kjeiieberg. p. cm. Includes bibliographical references and Index. 1. M1crob1al netaboHsn. 2. Starvation. I. Kjeileberg, Staffan. QR88.S7 1993 589.9" 0133—dc 20 93-21918 CIP This limited facsimile edition has been issued for the purpose of keeping this title available to the scientific community. 10 98765432 ISBN 978-0-306-44430-2 ISBN 978-1-4899-2439-1 (eBook) DOI 10.1007/978-1-4899-2439-1 © Springer Science+Business Media New York 1993 Originally published by Plenum Press, New York in 1993 Softcover reprint of the hardcover 1st edition 1993 All rights reserved No part of this book may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher Preface Concerted efforts to study starvation and survival of nondifferentiating vegeta­ tive heterotrophic bacteria have been made with various degrees of intensity, in different bacteria and contexts, over more than the last 30 years. As with bacterial growth in natural ecosystem conditions, these research efforts have been intermittent, with rather long periods of limited or no production in between. While several important and well-received reviews and proceedings on the topic of this monograph have been published during the last three to four decades, the last few years have seen a marked increase in reviews on starvation survival in non-spore-forming bacteria. This increase reflects a realization that the biology of bacteria in natural conditions is generally not that of logarithmic growth and that we have very limited information on the physiology of the energy- and nutrient-limited phases of the life cyde of the bacterial cello The growing interest in nongrowing bacteria also sterns from the more recent advances on the molecular basis of the starvation-induced nongrowing bacterial cello The identification of starvation-specific gene and protein re­ sponders in Escherichia coli as weIl as other bacterial species has provided molecular handles for our attempts to decipher the "differentiation-like" responses and programs that nondifferentiating bacteria exhibit on nutrient­ limited growth arrest. Severallaboratories have contributed greatly to the progress made in life­ after-log research. Of these it is pertinent to mention the strong pioneering work of Richard Morita and his collaborators, which predominantly studied marine Vibrio species, and Abdul Matin and co-workers, who in aseries of important publications introduced physiological and molecular aspects of starvation survival and the starvation-induced program in E. coli. Recently, the field has benefited greatly from the elegant and innovative series of studies reported by the research laboratories of Roberto Kolter and Regine Hengge­ Aronis. The detailed analysis of global control systems (for the regulation above the operon level) by, primarily, Fred Neidhardt and colleagues has been of prime importance for our understanding of the starvation-induced defense systems exhibited by prokaryotes. v vi Preface This monograph provides an up-to-date presentation of the means by which traditionally nondifferentiating bacteria adapt to starvation conditions. The genetic program and physiological features of adaptation to starvation by different bacteria are explored. This book also addresses prevailing ecosystem conditions that lead to intermittent growth or long-tenn starvation in bacteria. It is suggested that an improved understanding of starvation survival and nongrowth biology is an essential goal in microbiology, with far-reaching implications in bacterial physiology and ecology, as weIl as in applied bacteriol­ ogy and biotechnology. Public health microbiology and environmental bio­ technology are areas that greatly benefit from the advances recently made in research programs that deal with starvation in bacteria. This monograph serves as an overview and introduction also for those interested in further exploring such applications. 1 wish to thank the authors for providing their excellent contributions, Plenum Senior Editor Mary Phillips Born and other Plenum staff members for constructive support throughout the various stages of preparing this mono­ graph, and Kevin MarshalI for proposing that it is timely to publish a book on starvation in bacteria. Staffan Kjelleberg Göteborg anti Sydney Contributors MartaAlmir6n, Department ofMicrobiology and Molecular Genetics, Harvard Medical School, Boston, Massachusetts 02115 R. T. Bell, Institute of Limnology, Uppsala University, S-751 22 Uppsala, Sweden Thomas Egli, Swiss Federal Institute for Water Resources and Water Pollution Control (EAWAG), CH-8600 Dübendorf, Switzerland Klas Flärdh, Department of General and Marine Microbiology, University of Göteborg, S-413 19 Göteborg, Sweden lohn W. Foster, Department of Microbiology and Immunology, College of Medicine, University of South Alabama, Mobile, Alabama 36688 Regine Hengge-Aronis, Department of Biology, University of Konstanz, 7750 Konstanz, Germany Louise Holmquist, Department of General and Marine Microbiology, Univer­ sity of Göteborg, S-413 19 Göteborg, Sweden Asa louper-laan, Department of General and Marine Microbiology, University of Göteborg, S-413 19 Göteborg, Sweden Staffan Kjelleberg, Department of General and Marine Microbiology, Uni ver­ sity of Göteborg, S-413 19 Göteborg, Sweden. Present address: School of Microbiology and Immunology, University of New South Wales, Ken­ sington, New South Wales 2033, Australia Roberto Kolter, Department of Microbiology and Molecular Genetics, Harvard Medical School, Boston, Massachusetts 02115 C. G. Kurland, Department of Molecular Biology, Uppsala University, S-751 24 Uppsala, Sweden vii viii Contributors c. Anthony Mason, Swiss Federal Institute for Water Resources and Water Pollution Control (EAWAG), CH-8600 Dübendorf, Switzerland Riitta Mikkola, Department of Molecular Biology, Uppsala University, S-751 24 Uppsala, Sweden D. J. W Moriarty, Department of Marine Microbiology, University of Gothen­ burg, Gothenburg, Sweden. Present address: Department of Chemical Engineering, University of Queensland, St. Lucia, Queensland 4067, Aus­ tralia Richard Y. Morita, Department of Microbiology, College of Science and College of Oceanography, Oregon State University, Corvallis, Oregon 97330-3804 Thomas Nyström, Department ofMicrobiology and Immunology, University of Michigan Medical School, Ann Arbor, Michigan 48109-0620. Present address: Department of General and Marine Microbiology, University of Göteborg, S-413 19 Götcborg. Sweden James D. Oliver, Department of Biology, University of North Carolina at Charlotte, Charlotte, North Carolina 28223 Jörgen Östling, Department of General and Marine Microbiology, University of Göteborg, S-413 19 Göteborg, Sweden Deborah A. Siegele, Department of Microbiology and Molecular Genetics, Harvard Medical School, Boston, Massachusetts 02115. Present address: Department of Biology, Texas A&M University, College Station, Texas 77843 Michael P. Spector, Department of Biomedical Sciences, College of Allied Health, and Department of Microbiology and Immunology, College of Medicine, University of South Alabama, Mobile, Alabama 36688 Björn Svenblad, Department of General and Marine Microbiology, University of Göteborg, S-413 19 Göteborg, Sweden J. D. van Eisas, Institute for Soil Fertility Research, 6700AA Wageningen, The Netherlands L. S. van Overbeek, Institute for Soil Fertility Research, 6700AA Wageningen, The Netherlands Contents Chapter 1 Bioavailability of Energy and the Starvation State Richard Y. Morita 1. Introduetion...................................... 1 2. Survival of Baeteria in Natural and Artifieial Eeosystems 2 3. Organic Matter in Oligotrophie Systems. 2 3.1. Soil ....................................... 3 3.2. Aquatic Systems. 3 4. Bioavailability of Organie Matter in Oligotrophie Environments for Heterotrophie Baeteria .............. 4 4.1. Energy for Growth and/ or Reproduetion ......... 4 4.2. Bioavailability of Substrates and Generation Times 4 4.3. Syntrophy and Baeterial Aetivity ............... 7 4.4. Oligotrophie Bacteria . 8 5. The Starvation Proeess ............................. 8 5.1. Patterns of Starvation .. 10 5.2. Cell Size of Baeteria in Oligotrophie Environments and in Starvation Microeosms .................. 12 5.3. Cell Membrane Changes ...................... 13 5.4. ATP and Adenylate Energy Charge ............. 14 5.5. Protein, DNA, and RNA ...................... 14 5.6. Chemotaxis................................. 16 5.7. Resistance of Starved Cells to Various Environmental Faetors ........................ 16 5.8. Recovery from Starvation ..................... 16 6. Conclusions...................................... 17 References ....................................... 18 ix x Contents Chapter 2 Bacterial Growth and Starvation in Aquatic Environments D. 1. W. Moriarty and R. T. Bell 1. Introduction...................................... 25 2. Effects of Starvation on Natural Populations. 27 2.1. Specific Growth Rates and Productivity .......... 27 2.2. Factors Controlling Bacterial Growth ............ 28 2.3. Bacterial Cell Sizes in Natural Environments. 31 2.4. Effects of
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