Bacterial Growth and Division. Biochemistry and Regulation of Prokaryotic and Eukaryotic Division Cycles

509 Pages·1991·11.514 MB·English

by  Stephen Cooper (Auth.)

To Sandi, who has shared over half my life, and who
is now a part of me; to Sandi, who has kept my life
balanced; to Sandi, who has taught me how to live
life; to Sandi, whose presence makes each day a joy.
Bacterial Growth
and Division
Biochemistry and Regulation of
Prokaryotic and Eukaryotic Division Cycles
Stephen Cooper
Department of Microbiology and Immunology
University of Michigan Medical School
Ann Arbor, Michigan
ACADEMIC PRESS, INC.
Harcourt Brace Jovanovich, Publishers
San Diego New York Boston London Sydney Tokyo Toronto
This book is printed on acid-free paper. @
Copyright © 1991 by ACADEMIC PRESS, INC.
All Rights Reserved.
No part of this publication may be reproduced or transmitted in any
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without permission in writing from the publisher.
Academic Press, Inc.
San Diego, California 92101
United Kingdom Edition published by
Academic Press Limited
24-28 Oval Road, London NW1 7DX
Library of Congress Cataloging-in-Publication Data
Cooper, Stephen, date
Bacterial growth and division : biochemistry and regulation of
prokaryotic and eukaryotic division cycles / Stephen Cooper,
p. cm.
Includes bibliographical references.
Includes indexes.
ISBN 0-12-187905-4
1. Microbial differentiation. 2. Bacterial growth. I. Title.
[DNLM: 1. Baterial-growth & development. 2. Cell Cycle. 3.
Cell Division. 4. Cells. 5. Gene Expression Regulation, Bacterial. QW
51 C778b]
QR73.5.C66 1991
589.9'08761~dc20
DNLM/DLC
for Library of Congress 90-14426
CIP
PRINTED IN THE UNITED STATES OF AMERICA
91 92 93 94 9 8 7 6 5 4 3 2 1
Acknowledgments
A book does not come into being in the time it takes to write it. For me,
this book is the product of a scientific lifetime. During that lifetime I have
discussed these ideas with many people, and I have learned science from
many others.
One of my earliest teachers was Norton Zinder. I thank him for intro
ducing me to the excitement of science, and for setting high standards
that have guided my work.
Ole Maaloe is another teacher to whom I am indebted, but it took me
many years to understand the depth at which Ole thought about biologi
cal problems. His work is ever present in this volume, and his sug
gestions to look, and not touch, or to touch very gently, are some of the
lessons I wish to propagate.
Many people have discussed these ideas with me, and among them
I would note and thank Arthur Koch, Michael Savageau, Conrad
Woldringh, Nanne Nanninga, Olga Pierucci, Frederick Neidhardt, Arieh
Zaritzky, Robert Bender, Alan Leonard, Moselio Schaechter, Uli
Schwarz, Jochen Höltje, and Jay Keasling. In my laboratory over the last
25 years, a number of associates have worked beyond the call of duty
on various experiments, and I want to thank Therese Ruettinger, Sara
Scanlon, and Ming-Lin Hsieh for their efforts.
Some have been kind enough to read and comment on various chap
ters. Thanks for this go to Austin Newton, Bert Ely, Michael Higgins, and
David Dicker. Edward Birge read the entire manuscript, and I thank him
for his care and insight which have greatly improved this book. Chuck
Arthur, my editor at Academic Press, has been supportive and helpful
throughout the book's gestation.
I save a special paragraph for Chick (Charles E.) Helmstetter. We met
in Copenhagen in 1963, and through some divine intervention wound up
with jobs in Buffalo some years later. The ensuing collaboration was one
of the most exciting periods of my scientific career. For over a quarter of a
century Chick and I have talked, written, and discussed the ideas in this
book. I thank him for all of those phone calls and letters that he has
received, his comments on this book and on other ideas, and for his
friendship.
XIX
XX Acknowledgments
I thank Harold Winer for his help with the cover design.
But above all, I would note the special help of my wife, Sandi, who has
discussed words and syntax and ideas and communication and writing
for more hours than she would like to believe. Her help has been invalu
able, and I want her to know that she is the driving force behind this
creation.
Stephen Cooper
Illustrations
Figure
1 -1. Balanced Growth of a Bacterial Culture 8
1-2. Age Distribution during Balanced Growth 10
1 -3. Graphic Proof of the Age Distribution 11
1 -4. Life Cycle of a Bacterial Culture 12
1-5. The Schaechter-Maal0e-Kjeldgaard Experiment: The Fundamental
Experiment of Bacterial Physiology 14
1-6. The Shift-Up 15
2-1. Icon for Regulation of Growth and Division 23
3-1. Comparison of Differential and Integral Methods of Cell-Cycle Analysis 31
3-2. Selective and Nonselective (Batch) Methods for Synchronization 32
3-3. Size Distribution of a Bacterial Culture 39
3-4. The Membrane-Elution Apparatus 42
3-5. Synchronized Culture Produced by Membrane-Elution 43
3-6. The Technique of Flow Cytometry 47
3-7. Theory of Backwards Methods of Cell-Cycle Analysis 50
3-8. The Membrane-Elution Method for Backwards Analysis of the Division Cycle 51
3-9. Cell-Elution Pattern of a Membrane-Elution Experiment 53
3-10. Analysis of Biosynthetic Patterns from a Membrane-Elution Experiment 54
4-1. Protein Synthesis during the Division Cycle Using the Membrane-Elution
Method 70
4-2. Growth during the Division Cycle Determined from the Size Distribution 73
4-3. Linear or Exponential Accumulation of Mass during the Division Cycle 78
4-4. Proposed Patterns of Enzyme Synthesis during the Division Cycle 81
4-5. Semilogarithmic Plots and Cell-Cycle-Specific Protein Synthesis 85
4-6. Variation in Rate of Mass Synthesis by Repression of Auxiliary Proteins 87
4-7. Icon for Mass Synthesis during the Division Cycle 90
5-1. DNA Replication during the Division Cycle 96
5-2. Continuous Variation of Cell Age at Initiation and Termination 102
5-3. Continuous Variation in Times of Initiation and Termination Related to Cell
Division 103
5-4. Rate of DNA Synthesis during the Division Cycle Determined with the
Membrane-Elution Apparatus 108
5-5. Values of C and D at Different Growth Rates 110
5-6. DNA Contents of Bacteria by Flow Cytometry 112
5-7. Icon for DNA Replication during the Division Cycle 114
5-8. Derivation of Cell Size at Different Growth Rates 116
5-9. I + C + D Model of Chromosome Replication 120
5-10. DNA Synthesis and Cell Division during Inhibition of Mass Synthesis 122
5-11. Growth and Cell Division during Inhibition of DNA Synthesis 123
5-12. The Maal0e-Hanawalt Experiment 126
XX11 Illustrations
5-13. Chromosome Patterns following a Shift-Up 128
5-14. Deviations from Rate Maintenance 131
5-15. Icon for Regulation of DNA Replication 133
5-16. Gene-Frequency Analysis of DNA Replication 138
5-17. Nucleoid Separation and Production 141
5-18. DNA Replication in Slow-Growing Cells 145
5-19. Minichromosome and Plasmid Replication during the Division Cycle Using
the Membrane-Elution Method 168
6-1. Cellular and Molecular Structure of the Gram-Negative Bacterial Cell Wall 178
6-2. Three-Dimensional Representation of Peptidoglycan Structure 181
6-3. Growth of Peptidoglycan Area by Cutting of Stretched Bonds 182
6-4. Zonal and Diffuse Cell-Wall Synthesis 188
6-5. Rate and Topography of Peptidoglycan Synthesis during the Division Cycle 193
6-6. Membrane-Elution Analysis of Surface and Mass Synthesis during the
Division Cycle 198
6-7. Why Peaks in the Ratio of Peptidoglycan-to-Cytoplasm Synthesis Occur
Only Twice 199
6-8. Increase in Cross-Linking by Natural Selection 208
6-9. Definition of Cell Shape 214
6-10. Constant Shape of Rod-Shaped Cells of Varying Size 216
6-11. Development of Variable Widths during Bacterial Growth 221
6-12. Length and Width Distribution in a Cell Population 223
6-13. Peptidoglycan Synthesis in Septate and Nonseptate Cells of the Same Length 226
6-14. Membrane-Peptidoglycan Interaction for Shape Maintenance 229
6-15. Volume, Surface Area, and Length of Cells at Different Growth Rates 231
6-16. The Constrained-Hoop Model 233
6-17. Surface Synthesis during a Shift-Up 234
6-18. Icon for Surface Synthesis 240
8-1. Elements of Variation during the Division Cycle 256
8-2. Size Homeostasis 260
8-3. Cumulative and Noncumulative Variation 261
8-4. DNA Synthesis as a Function of Cell Length 267
8-5. Comparison of Classical and Inverse Age Distributions 268
8-6. Comparison of Division-Cycle Analysis by Forward and Backwards Methods 272
8-7. Age-Size Structure of a Bacterial Culture 274
9-1. Formal Analysis of DNA Segregation 282
9-2. The Methocel Method 287
9-3. Advantages of Presegregation with the Methocel Method 291
9-4. Comparison of Segregation Determined by the Membrane-Elution Method
and the Methocel Method 293
9-5. The Helmstetter-Leonard Surface-Area Model for Nonrandom DNA
Segregation 294
9-6. Why Segregation Randomness Varies with Growth Rate Using Methocel and
Does Not Vary Using the Membrane-Elution Technique 295
9-7. Analysis of Segregation by the Membrane-Elution Method 296
9-8. Analysis of Segregation by the Methocel Method 298
9-9. Nonequipartition Model of Minichromosome Segregation 304
10-1. The Life Cycle of a Culture as Shift-Ups and Shift-Downs 316
11-1. Classical Division Cycle of Caulobacter crescentus 320
11-2. Chromosome Pattern during the Division Cycle of Caulobacter crescentus 321
Illustrations
xxin
11-3. Alternative View of the Division Cycle of Caulobacter crescentus 328
11-4. Schematic Analysis of Caulobacter Growth and Division 331
11-5. Icon of the Caulobacter Division Cycle 333
11-6. Age Distribution for Cells with Unequal Interdivision Times in Unequal
Progeny 335
12-1. Growth of Streptococcus Cell Surface with Overlapping Rounds of Wall
Growth 341
12-2. Icon for Streptococcal Cell-Wall Growth 343
12-3. Chromosome Replication during the Division Cycle of Streptococcus 344
12-4. Concept of the Fundamental Cell 349
13-1. Inside-to-Outside Growth of Bacillus subtilis Cell Wall 359
13-2. Side Wall and Pole Growth of Bacillus subtilis 361
13-3. Presumed Chromosome Configuration in Growing Bacillus subtilis 367
13-4. Residual Division in a Culture with a Variable D Period 369
13-5. Cell Mass as a Function of Growth Rate in Bacillus subtilis 370
14-1. Synthesis of Cell Components during the Division Cycle 379
14-2. Calculation of Cell-Length Distribution with Variable Cell Widths 382
14-3. Microscale Pattern of Protein Synthesis during the Division Cycle 384
14-4. Idealization of the Schaechter, Maal0e, and Kjeldgaard Experiment 386
15-1. G1 Arrest 393
15-2. The Continuum Model 394
15-3. Icon for the Classical Eukaryotic Division Cycle 396
15-4. Comparison of the Eukaryotic and Prokaryotic Views of G1 -Phase Variability 398
15-5. Explanation of Complementation of G1 Mutants 399
15-6. G1 Arrest according to the Continuum Model 400
15-7. Schematic Description of the G(0) Model of Zetterberg and Larsson 403
15-8. Reanalysis of a G(0) Model 405
15-9. The Transition-Probability Model 415
15-10. External Conditions Induce DNA Synthesis by First Activating Mass Synthesis 418
15-11. The Frequency-of-Labeled-Mitoses Method: A Backwards Method for
Eukaryotic Cell-Cycle Analysis 425
15-12. Continuum-Model Icon for the Eukaryotic Division Cycle 426
Tables
Table
5-1. Replication Point Determination by Autoradiography (after Bird, Louarn,
Martuscelli, and Curo) 113
5-2. Mass and DNA Content of Cells Growing at Different Rates 117
6-1. Dimensions of Cells Growing at Different Rates 217
6-2. Classification of Morphogenes (according to Donachie, Begg, and Sullivan) 236
8-1. Cell Sizes and Their Variation at Particular Events during the Division Cycle 254
9-1. The Segregation Results of Pierucci-Zuchowski and Its Comparison with
Different Models 290
9-2. Selection for High Plasmid Copy Number 306
12-1. Cell Composition Expected for Streptococcus faecium at Different Growth
Rates 354
14-1. Rates of Chain Extension for Macromolecules 384
15-1. Terminology of Cell-Cycle Phases in Prokaryotes and Eukaryotes 425
xxv
Prologue
And since then, I have tended to class certain research procedures
with military operations: the will to conquer; applying a strategy and
a tactic; the necessity of choosing a terrain; developing a plan of
attack; concentrating one's forces on a particular sector, focusing and
modifying the initial plan according to the reactions obtained. In
short, going on the offensive on all fronts.
F. Jacob, The Statue Within, 1988.
I. THE FIELD OF DIVISION-CYCLE STUDIES
Growth of cells can be considered in two different but complementary
ways. We can consider the growth of any property of a population such
as the change in the total number or total weight of a group of individuals
or cells. Alternatively, we can study the growth of individual members of
the population. In the human population, an individual begins life
weighing about seven pounds and grows rapidly over the next decade.
The increase in weight then slows. There is no necessary relationship
between the growth pattern of a population and the growth pattern of its
individual members, as can be seen by our current population explosion.
The growth pattern of an individual could be different. We could remain
the same weight for 10 years, grow to 300 pounds by the age of 20, and
then drop to 150 pounds; this would have no effect on the growth of the
population.
This book deals primarily with bacterial growth at the individual cell
level, and only slightly at the population level. It is the study of the
bacterium during its cell cycle or division cycle. Though there have been
a number of excellent treatises on the growth of bacteria, such as the
text by Ingraham, Maaloe and Neidhardt,1 its successor by Ingraham,
Neidhardt and Schaechter,2 or the encyclopedic treatment of Escherichia
1