This page intentionally left blank 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 (cid:2) 2010 ASM Press American Society for Microbiology 1752 N St. NW Washington, DC 20036-2904 Library of Congress Cataloging-in-Publication Data The second messenger cyclic di-GMP / edited by Alan J. Wolfe and Karen L. Visick. p. ; cm. Includes bibliographical references and index. ISBN 978-1-55581-499-1 (hard cover) 1. Cyclic guanylic acid. 2. Second messengers (Biochemistry) I. Wolfe, Alan J. II. Visick, Karen L. III. American Society for Microbiology. [DNLM: 1. Cyclic GMP—physiology. 2. Bacterial Physiological Phenomena. 3. Cyclic GMP—analogs & derivatives. 4. Genome, Bacterial. 5. Signal Transduction—physiology. QU 58 S445 2010] QP625.N89S43 2010 572.8’6293—dc22 2009036432 Current printing (last digit) 10 9 8 7 6 5 4 3 2 1 All Rights Reserved Printed in the United States of America Coverillustration:AwrinkledcolonyformedbyamutantofVibriocholerae.Thephenotypeisassociatedwith cyclic di-GMP production. (Courtesy of Nicholas J. Shikuma and Fitnat H. Yildiz.) CONTENTS Contributors • vii 7. Making, Breaking, and Sensing of Cyclic Preface • xi Di-GMP: Structural, Thermodynamic, and Evolutionary Principles • 76 Dorothy Kim, John F. Hunt, and Tilman Schirmer I. Second Messengers: an Overview III. Cyclic Di-GMP and Lifestyle Choices 1. Introduction to Second Messengers: Lessons from Cyclic AMP • 3 8. Choosing the Right Lifestyle: Regulation Alan J. Wolfe of Developmental Pathways by Cyclic Di-GMP • 99 Matthew Parsek and Phillip Aldridge II. General Principles: the Core 9. Role of Cyclic Di-GMP in Caulobacter 2. Moshe Benziman and the Discovery of Cyclic crescentus Development and Cell Cycle Di-GMP • 11 Control • 120 Dorit Amikam, Haim Weinhouse, and Michael Y. So¨ren Abel and Urs Jenal Galperin 10. Hierarchical Control of rdar Morphotype 3. Ubiquity of Cyclic Di-GMP Pathways: a Development of Salmonella enterica by Cyclic Bioinformatic Analysis • 24 Di-GMP • 137 Michael Y. Galperin Ute Ro¨mling, Kristina Jonas, O¨jar Melefors, Nina Grantcharova, and Agaristi Lamprokostopoulou 4. The Core Pathway: Diguanylate Cyclases, Cyclic Di-GMP-Specific Phosphodiesterases, and 11. Role of Cyclic Di-GMP in Pseudomonas Cyclic Di-GMP-Binding Proteins • 37 aeruginosa Biofilm Development • 156 Mark Gomelsky Caroline S. Harwood 5. The HD-GYP Domain and Cyclic Di-GMP 12. The Scr Circuit in Vibrio parahaemolyticus Signaling • 57 Modulates Swarming and Sticking • 173 Robert P. Ryan, Yvonne McCarthy, and J. Maxwell Linda L. McCarter Dow 13. Roles of Diguanylate Cyclases and 6. Methods for Cyclic Di-GMP Phosphodiesterases in Motility and Biofilm Detection • 68 Formation in Vibrio fischeri • 186 Christopher M. Waters Alan J. Wolfe and Karen L. Visick v vi CONTENTS 14. Csr (Rsm) System and Its Overlap and IV. Cyclic Di-GMP, Pathogenesis, and Host Interplay with Cyclic Di-GMP Regulatory Immunity Systems • 201 Tony Romeo and Paul Babitzke 20. Role of Cyclic Di-GMP in Vibrio cholerae Virulence • 293 15. Riboswitches That Sense Cyclic Di-GMP • 215 Jason T. Pratt, Rita Tamayo, and Andrew Camilli Elaine R. Lee, Narasimhan Sudarsan, and Ronald R. Breaker 21. Cyclic Di-GMP Signaling and Host Immunity • 304 16. Role of Cyclic Di-GMP in the Regulatory David K. R. Karaolis and Theodore J. Standiford Networks of Escherichia coli • 230 Regine Hengge 22. Bis-(3(cid:2),5(cid:2))-Cyclic Di-GMP: Promising Adjuvant for Vaccine Design • 311 17. Cyclic Di-GMP Signaling in Vibrio Thomas Ebensen, Rimma Libanova, and Carlos A. cholerae • 253 Guzm´an Sinem Beyhan and Fitnat H. Yildiz 18. Role of Cyclic Di-GMP in Biofilm V. Conclusions Development and Signaling in Yersinia pestis • 270 23. Cyclic Di-GMP: Using the Past To Peer into Robert D. Perry and Alexander G. Bobrov the Future • 323 Karen L. Visick and Alan J. Wolfe 19. Environmental Control of Cyclic Di-GMP Signaling in Pseudomonas fluorescens: from Signal to Output • 282 Peter D. Newell and George A. O’Toole Index • 333 CONTRIBUTORS So¨ren Abel J. Maxwell Dow Biozentrum, University of Basel, CH-4056 Basel, BIOMERIT Research Centre, Department of Switzerland Microbiology, BioSciences Institute, University College Cork, Cork, Ireland Phillip Aldridge Centre for Bacterial Cell Biology and Institute for Thomas Ebensen Cell and Molecular Biosciences, Newcastle Department of Vaccinology and Applied University, Newcastle upon Tyne, NE2 4HH, Microbiology, Helmholtz Centre for Infection United Kingdom Research, 38124 Braunschweig, Germany Dorit Amikam Michael Y. Galperin P.O. Box 10356, Zichron Yakov 30900, Israel National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894 Paul Babitzke Department of Biochemistry and Molecular Mark Gomelsky Biology, The Pennsylvania State University, Department of Molecular Biology, University of University Park, PA 16802 Wyoming, Laramie, WY 82071 Sinem Beyhan Nina Grantcharova Department of Microbiology and Environmental Department of Microbiology, Tumor and Cell Toxicology, University of California, Santa Cruz, Biology, Karolinska Institutet, SE-171 77 Santa Cruz, CA 95064 Stockholm, Sweden Alexander G. Bobrov Carlos A. Guzma´n Department of Microbiology, Immunology, and Department of Vaccinology and Applied Molecular Genetics, University of Kentucky, Microbiology, Helmholtz Centre for Infection Lexington, KY 40536-0298 Research, 38124 Braunschweig, Germany Ronald R. Breaker Caroline S. Harwood Department of Molecular, Cellular and Department of Microbiology, The University of Developmental Biology, Department of Molecular Washington, Seattle, WA 98195 Biophysics and Biochemistry, and Howard Hughes Medical Institute, Yale University, New Haven, CT Regine Hengge 06520 Institut fu¨r Biologie—Mikrobiologie, Freie Universit¨at Berlin, 14195 Berlin, Germany Andrew Camilli Howard Hughes Medical Institute and Department John F. Hunt of Molecular Biology and Microbiology, Tufts Department of Biological Sciences, Columbia University School of Medicine, Boston, MA 02111 University, New York, NY 10027 vii viii CONTRIBUTORS Urs Jenal Matthew Parsek Biozentrum, University of Basel, CH-4056 Basel, Department of Microbiology, University of Switzerland Washington, School of Medicine, Seattle, WA 98195-7242 Kristina Jonas Department of Microbiology, Tumor and Cell Robert D. Perry Biology, Karolinska Institutet, SE-171 77 Department of Microbiology, Immunology, and Stockholm, Sweden Molecular Genetics, University of Kentucky, Lexington, KY 40536-0298 David K. R. Karaolis Intragenics Research Institute, Havre de Grace, MD Jason T. Pratt 21078, and Karagen Pharmaceuticals, Baltimore, Howard Hughes Medical Institute and Department MD 21210 of Molecular Biology and Microbiology, Tufts University School of Medicine, Boston, MA 02111 Dorothy Kim Department of Biological Sciences, Columbia University, New York, NY 10027 Tony Romeo Department of Microbiology and Cell Science, Agaristi Lamprokostopoulou University of Florida, Gainesville, FL 32611 Department of Microbiology, Tumor and Cell Biology, Karolinska Institutet, SE-171 77 Ute Ro¨mling Stockholm, Sweden Department of Microbiology, Tumor and Cell Biology, Karolinska Institutet, SE-171 77 Elaine R. Lee Stockholm, Sweden Department of Molecular, Cellular and Developmental Biology, Yale University, New Robert P. Ryan Haven, CT 06520 BIOMERIT Research Centre, Department of Microbiology, BioSciences Institute, University Rimma Libanova College Cork, Cork, Ireland Department of Vaccinology and Applied Microbiology, Helmholtz Centre for Infection Tilman Schirmer Research, 38124 Braunschweig, Germany Core Program Structural Biology and Biophysics, Biozentrum, University of Basel, CH-4056, Basel, Linda L. McCarter Department of Microbiology, The University of Switzerland Iowa, Iowa City, IA 52242 Theodore J. Standiford Yvonne McCarthy Department of Internal Medicine, Division of BIOMERIT Research Centre, Department of Pulmonary and Critical Care Medicine, University Microbiology, BioSciences Institute, University of Michigan Medical Center, Ann Arbor, MI 48109 College Cork, Cork, Ireland Narasimhan Sudarsan O¨jar Melefors Howard Hughes Medical Institute, Yale University, Department of Microbiology, Tumor and Cell New Haven, CT 06520 Biology, Karolinska Institutet, SE-171 77 Stockholm, Sweden Rita Tamayo Department of Microbiology and Immunology, The Peter D. Newell University of North Carolina at Chapel Hill, Chapel Department of Microbiology and Immunology, Hill, NC 27599 Dartmouth Medical School, Hanover, NH 03755 George A. O’Toole Karen L. Visick Department of Microbiology and Immunology, Department of Microbiology and Immunology, Dartmouth Medical School, Hanover, NH 03755 Loyola University Chicago, Maywood, IL 60153 CONTRIBUTORS ix Christopher M. Waters Alan J. Wolfe Department of Microbiology and Molecular Department of Microbiology and Immunology, Genetics, Michigan State University, East Lansing, Loyola University Chicago, Maywood, IL 60153 MI 48824 Haim Weinhouse Fitnat H. Yildiz Department of Biological Chemistry, The Alexander Department of Microbiology and Environmental Silberman Institute for Life Sciences, Hebrew Toxicology, University of California, Santa Cruz, University of Jerusalem, Jerusalem 91904, Israel Santa Cruz, CA 95064