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The Lure of
Bacterial
Genetics
A Tribute to John Roth
This page intentionally left blank
The Lure of
Bacterial
Genetics
A Tribute to John Roth

Edited by
Stanley Maloy
San Diego State University
San Diego, California

Kelly T. Hughes
University of Utah
Salt Lake City, Utah

Josep Casadesús
University of Seville
Seville, Spain

Washington, DC
Address editorial correspondence to ASM Press, 1752 N St. NW, Washington, DC
20036-2904, USA

Send orders to ASM Press, P.O. Box 605, Herndon,VA 20172, USA
Phone: 800-546-2416; 703-661-1593
Fax: 703-661-1501
E-mail: [email protected]
Online: estore.asm.org

Copyright © 2011 ASM Press

American Society for Microbiology
1752 N St. NW
Washington, DC 20036-2904

Library of Congress Cataloging-in-Publication Data

The lure of bacterial genetics : a tribute to John Roth / editors, Stanley Maloy, Kelly T.
Hughes, Josep Casadesús.
p. ; cm.
Includes bibliographical references and index.
ISBN 978-1-55581-538-7 (hardcover : alk. paper) 1. Bacterial genetics. 2. Roth, John
R., 1939- I. Roth, John R., 1939- II. Maloy, Stanley R. III. Hughes, Kelly Thomas.
IV. Casadesús, Josep, 1951- V. American Society for Microbiology.
[DNLM: 1. Bacteria—genetics—Festschrift. 2. Bacterial Physiological Phenomena—
genetics—Festschrift. 3. DNA, Bacterial—Festschrift. 4. Gene Expression Regulation—
Festschrift. 5. RNA, Bacterial—Festschrift. QW 51]
QH434.L87 2011
572.8293—dc22
2010029291

Current printing (last digit)

10 9 8 7 6 5 4 3 2 1

All Rights Reserved

Printed in the United States of America
 CONTENTS

Contributors ix
Preface xiii

I. INTRODUCTION / 1
1. John Roth’s Paths and Pathways / 3
Kelly T. Hughes and Stanley Maloy
2. Giving a Seminar: Suggestions for Graduate Students / 9
John Roth
3. Phage and Bacterial Genetics at Cold Spring
Harbor Laboratory / 23
Stanley Maloy and Kelly T. Hughes
4. Reflections of a Beer Auxotroph / 27
Thomas J. Silhavy

II. GENE EXPRESSION AND GENETIC

REGULATION / 33
5. The Biotin Operon of Escherichia coli / 35
Allan Campbell and Alice del Campillo-Campbell
6. Why Galactose? The Early Curiosities and
the Consequences / 43
Sankar Adhya
7. Control of Gene Expression by Compartmentalization:
the put Operon / 55
Stanley Maloy
8. Genetics of the Heme Pathway and Its Regulation / 65
Thomas Elliott

v
vi 䡵 CONTENTS

9. Regulation of NAD(P) Metabolism in Salmonella / 75

Julianne House Grose
10. Ethanolamine Utilization in Salmonella / 87
David Roof and David Sheppard
11. Fishing for Fluke: the Genetics of Flk and the Flagellar
Type 3 Secretion Specificity Switch / 99
Kelly T. Hughes

III. tRNA AND SUPPRESSORS / 115

12. Souvenirs from My Genetic Initiation / 117
Lionello Bossi
13. Complementary Studies in the Histidine Operon
and on Frameshifting: a Compliment to What Roth
Has Wrought / 123
John F. Atkins
14. Adventures with Frameshift Suppressor tRNAs / 131
Glenn R. Björk

IV. PHYSIOLOGY AND METABOLISM / 141

15. Microbial Channels: Forbidden Fruit from Missense
Rather than Nonsense / 143
Ian R. Booth
16. Of Bacteria and Bile / 153
Josep Casadesús, Sara B. Hernández, Ignacio Cota, and Francisco
Ramos-Morales
17. Swarming Adventures / 163
Rasika M. Harshey
18. Using Genetic Approaches To Delineate the Pathway
of Contact-Dependent Growth Inhibition / 173
Stephanie K. Aoki and David A. Low
19. Covert Operations: the Adaptable Plan of Attack Deployed by
Pathogenic Bacteria / 185
Michael J. Mahan, Robert L. Sinsheimer,William R. Shimp, and
Douglas M. Heithoff
20. Phenotypic Variation and Gene Regulation in the
Pathogenesis of Salmonella Infection / 201
Brad T. Cookson

V. GENES, CHROMOSOMES, AND

REARRANGEMENTS / 209
21. DNA Methylation and Mismatch Repair / 211
Martin G. Marinus
 CONTENTS 䡵 vii

22. Salmonella Genetics / 219

Kenneth E. Sanderson
23. Finding Inversions / 227
Molly Schmid
24. Barriers to the Formation of Inversion Rearrangements
in Salmonella / 233
Lynn Miesel
25. Adventures with Mutation and Selection in Beehive and
Cow Country / 245
Diarmaid Hughes and Dan I. Andersson

VI. GENOMES AND EVOLUTION / 255

26. From Genetics to Genomics / 257
Garret Suen, Frank O. Aylward, Steven C. Slater, and Barry S. Goldman
27. Baltimore and Beyond: from Gene Action to the
Postgenomic Era / 267
Robert A. LaRossa
28. Three Histories of Competence and Transformation / 277
Rosemary J. Redfield
29. A Plethora of Putative Phages and Prophages / 291
Sherwood R. Casjens
30. Impact of Horizontal Genetic Transfer on the Evolution
of Bacterial Genomes / 307
Jeffrey G. Lawrence
31. Germ Line DNA Parasites That Have Converged on an
Altruistic Somatic Excision Strategy / 325
Glenn Herrick
32. Recombineering: Advanced-Advanced
Bacterial Genetics / 333
James A. Sawitzke

VII. Epilogue / 341

33. Predicting the Future: a Fish Story / 343
John Roth
Index / 349
This page intentionally left blank
 CONTRIBUTORS

Sankar Adhya
Laboratory of Molecular Biology, Center for Cancer Research, National Cancer Institute,
National Institutes of Health, Bethesda, MD 20892-4264
Dan I. Andersson
Department of Medical Microbiology and Biochemistry, Biomedical Center, Uppsala
University, S-75124 Uppsala, Sweden
Stephanie K. Aoki
Department of Molecular, Cellular and Developmental Biology, University of California,
Santa Barbara, CA 93106
John F. Atkins
Department of Human Genetics, University of Utah, Salt Lake City, UT 84112-5330, and
BioSciences Institute, University College Cork, Cork, Ireland
Frank O. Aylward
Department of Bacteriology, University of Wisconsin, Madison, WI 53706
Glenn R. Björk
Department of Molecular Biology, Umeå University, SE-90187 Umeå, Sweden
Ian R. Booth
Institute of Medical Sciences, University of Aberdeen, Aberdeen, Scotland AB25 2ZD
Lionello Bossi
Centre de Génétique Moléculaire, CNRS, Gif-sur-Yvette, France
Allan Campbell
Department of Biology, Stanford University, Stanford, CA 94305
Josep Casadesús
Departamento de Genética, Universidad de Sevilla, E-41080 Sevilla, Spain
Sherwood R. Casjens
Pathology Department, University of Utah, Salt Lake City, UT 84112

ix
x 䡵 CONTRIBUTORS

Brad T. Cookson
Departments of Laboratory Medicine and Microbiology, University of Washington,
Seattle, WA 98195-7110
Ignacio Cota
Departamento de Genética, Universidad de Sevilla, E-41080 Sevilla, Spain
Alice del Campillo-Campbell
Department of Biology, Stanford University, Stanford, CA 94305
Thomas Elliott
Department of Microbiology and Immunology, West Virginia University, Morgantown,
WV 26506
Barry S. Goldman
Monsanto Company, 800 North Lindbergh Blvd., St. Louis, MO 63167
Julianne House Grose
Department of Microbiology and Molecular Biology, Brigham Young University, Provo,
UT 84602
Rasika M. Harshey
Department of Microbiology and Molecular Genetics, University of Texas, Austin,TX 78712
Douglas M. Heithoff
Department of Molecular, Cellular and Developmental Biology, University of California,
Santa Barbara, CA 93106
Sara B. Hernández
Departamento de Genética, Universidad de Sevilla, E-41080 Sevilla, Spain
Glenn Herrick
Department of Biology, University of Utah, Salt Lake City, UT 84112
Diarmaid Hughes
Department of Cell & Molecular Biology, Biomedical Center, Uppsala University, S-75124
Uppsala, Sweden
Kelly T. Hughes
Biology Department, University of Utah, Salt Lake City, UT 84112
Robert A. LaRossa
E. I. DuPont Co., Wilmington, DE 19880-0173
Jeffrey G. Lawrence
Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260
David A. Low
Department of Molecular, Cellular and Developmental Biology, University of California,
Santa Barbara, CA 93106
Michael J. Mahan
Department of Molecular, Cellular and Developmental Biology, University of California,
Santa Barbara, CA 93106
Stanley Maloy
Department of Biology, San Diego State University, San Diego, CA 92182-4614
Martin G. Marinus
Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School,
Worcester, MA 01605
 CONTRIBUTORS 䡵 xi

Lynn Miesel
Merck Research Laboratories, 126 East Lincoln Avenue, Rahway, NJ 07065
Francisco Ramos-Morales
Departamento de Genética, Universidad de Sevilla, E-41080 Sevilla, Spain
Rosemary J. Redfield
Department of Zoology, University of British Columbia,Vancouver, BC V6T 1Z3, Canada
David Roof
Genentech, Inc., 1 DNA Way, South San Francisco, CA 94080-4990
John Roth
Department of Genetics, University of California, Davis, Davis, CA 95616
Kenneth E. Sanderson
Salmonella Genetic Stock Centre, Department of Biological Sciences, University of Calgary,
Calgary, Alberta T2N 1N4, Canada
James A. Sawitzke
Molecular Control and Genetics Section, Gene Regulation and Chromosome Biology
Laboratory, Center for Cancer Research, National Cancer Institute, Frederick, MD 21702
Molly Schmid
Keck Graduate Institute, 535 Watson Drive, Claremont, CA 91711
Anca Segall
Center for Microbial Sciences, Department of Biology, San Diego State University, San
Diego, CA 92182-4614
David Sheppard
Department of Biological Sciences, University of Delaware, Newark, DE 19716
William R. Shimp
Department of Molecular, Cellular and Developmental Biology, University of California,
Santa Barbara, CA 93106
Thomas J. Silhavy
Princeton University, Princeton, NJ 08544
Robert L. Sinsheimer
Department of Molecular, Cellular and Developmental Biology, University of California,
Santa Barbara, CA 93106
Steven C. Slater
Great Lakes Bioenergy Research, University of Wisconsin, Madison, WI 53706
Garret Suen
Department of Bacteriology, University of Wisconsin, Madison, WI 53706
This page intentionally left blank
 PREFACE

T his book is a tribute to the pleasures of bacterial genetics as taught by one

of the great gurus of this field, John Roth. Over the course of his career,
John has influenced a large number of scientists, propagating a unique scientific
philosophy that is emphasized in the many chapters of this book. He does not
approach science as simply a job or a race to beat other groups. Rather, for John,
science is clearly about the mental pleasure of solving a difficult puzzle, some-
thing that is not quite done until all of the pieces fit together. And solving
complex puzzles isn’t something you do on your own—thinking about the
problem with colleagues is part of the fun. The chalkboards in the hallway out-
side John’s lab have always been littered with diagrams of new ideas, often with
several people talking excitedly about what it all means and what to try next.
Each student has had his or her own unique project, so there have always been
a variety of research projects going on at the same time, providing an exciting
buffet of scientific discussions.
With John, thinking about a given topic begins with an idea, elaborated over
a piece of paper or more often at the blackboard or at the bar. Ideas easily de-
velop into models, which then evolve into experiments to test the model. It has
been instructive to observe his thinking, which takes deductive leaps over details
in which we have often been hopelessly mired. Ideas are molded and shaped by
data—as the data come out, everyone is back at the blackboard or around a piece
of paper to shape and redirect and design new tests for new models.Throughout,
John has displayed indomitable optimism and irrepressible curiosity. He
approaches science as a personal quest, an adventure to follow the story that
nature has written. While working out the story, he is absorbed in the joy and
the fun of it, to see where it takes us and whether we can second-guess nature
or whether nature has misled us, demanding a trickier experimental approach.
Elegant genetics takes precedence; brute force is looked down upon, to be used
only as a last resort, after the awesome power of genetics has simply run out of
steam. The adventure is the most important thing! John infects us with his own

xiii
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