Table Of ContentStarvation 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 Nitrogen and Phosphorus ............. 32
3. Marine Environments .............................. 34
3.1. Pelagic Bacterial Growth ...................... 34
3.2. Bacterial Growth and Survival in Sediments ...... 37
4. Freshwater Environments ........................... 40
4.1. Seasonal Dynamics of Bacterioplankton in Lakes 40
4.2. The Microbial Landscape in Lakes-Importance
of Microenvironments ........................ 44
4.3. Bacterial Productivity in the Surface Sediment
of Lakes ................................... 46
5. Concluding Comment .............................. 47
References ....................................... 48
Chapter 3
Bacterial Responses to SoU Stimuli
J. D. van Elsas and L. S. van Overbeek
1. Introduction...................................... 55
2. The Soil Environment. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 56
2.1. Observations on Bacterial Populations in Soil ..... 56
3. Stimuli in the Soil Environment . . . . . . . . . . . . . . . . . . . . . . 64
3.1. Responses to Stimuli of Bulk Soil .............. 66
3.2. Responses to Stimuli of Rhizosphere Soil ........ 70
4. Concluding Remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73
References ....................................... 74
