Tài liệu The biology of vibrios

The BIOLOGYof VIBRIOS This page intentionally left blank The BIOLOGYof VIBRIOS E D I T E D B Y Fabiano L. Thompson, Brian Austin, and Jean Swings W A S H I N G T O N , D . C . Copyright © 2006 ASM Press American Society for Microbiology 1752 N St., N.W. Washington, DC 20036-2904 Library of Congress Cataloging-in-Publication Data The biology of vibrios / edited by F. L. Thompson, B. Austin, and J. Swings. p. ; cm. Includes bibliographical references and index. ISBN 10: 1-55581-365-8 (alk. paper) ISBN-13: 978-1-55581-365-9 (alk. paper) 1. Vibrio. 2. Vibrio infections. I. Thompson, F. L. (Fabiano L.) II. Austin, B. (Brian), 1951– . III. Swings, J. G. IV. American Society for Microbiology. [DNLM: 1. Vibrio. 2. Vibrio—pathogenicity. 3. Vibrio Infections—etiology. QW 141 B615 2006] QR82.S6B56 2006 579.3'25—dc22 2005032511 All rights reserved Printed in the United States of America 10 9 8 7 6 5 4 3 2 1 Address editorial correspondence to ASM Press, 1752 N St., N.W., Washington, DC 20036-2904, U.S.A. Send orders to: ASM Press, P.O. Box 605, Herndon, VA 20172, U.S.A. Phone: 800-546-2416; 703-661-1593 Fax: 703-661-1501 E-mail: [email protected] Online: http://estore.asm.org Cover figure: Colonial morphology of vibrios in different media (courtesy of Gomez-Gil and Roque [see Chapter 2]). To Huai-Shu Xu This page intentionally left blank CONTENTS Contributors Preface • I. • xiii ix 7. The Roles of Lateral Gene Transfer and Vertical Descent in Vibrio Evolution • 84 Yan Boucher and Hatch W. Stokes Introduction 8. The Adaptive Genetic Arsenal of Pathogenic Vibrio Species: the Role of Integrons • 95 Dean A. Rowe-Magnus, Mohammed Zouine, and Didier Mazel 1. A Global and Historical Perspective of the Genus Vibrio • 3 R. R. Colwell II. V. Isolation, Enumeration, and Preservation 9. Motility and Chemotaxis Linda L. McCarter 2. Isolation, Enumeration, and Preservation of the Vibrionaceae • 15 Bruno Gomez-Gil and Ana Roque III. 4. Molecular Identification Mitsuaki Nishibuchi IV. • • 115 10. Adaptive Responses of Vibrios • 133 Diane McDougald and Staffan Kjelleberg Classification and Phylogeny 3. Taxonomy of the Vibrios • Fabiano L. Thompson and Jean Swings Physiology 11. Extremophilic Vibrionaceae Douglas H. Bartlett 29 44 VI. • 156 Habitat and Ecology 12. Aquatic Environment • 175 Hidetoshi Urakawa and Irma Nelly G. Rivera Genome Evolution 5. Comparative Genomics: Genome Configuration and the Driving Forces in the Evolution of Vibrios • 67 Tetsuya Iida and Ken Kurokawa 13. Dynamics of Vibrio Populations and Their Role in Environmental Nutrient Cycling • 190 Janelle R. Thompson and Martin F. Polz 6. Gene Duplicates in Vibrio Genomes • 76 Dirk Gevers and Yves Van de Peer 14. The Vibrio fischeri–Euprymna scolopes Light Organ Symbiosis • 204 Eric V. Stabb vii viii CONTENTS 15. The Mutual Partnership between Vibrio halioticoli and Abalones • 219 Tomoo Sawabe 16. Vibrios in Coral Health and Disease • 231 Eugene Rosenberg and Omry Koren 17. Vibrio cholerae Populations and Their Role in South America • 239 Ana Carolina P. Vicente, Irma Nelly G. Rivera, Michelle D. Vieira, and Ana Coelho VII. 23. Vibrio cholerae: the Genetics of Pathogenesis and Environmental Persistence • 311 Michael G. Prouty and Karl E. Klose 24. Vibrio parahaemolyticus • 340 Tetsuya Iida, Kwan-Sam Park, and Takeshi Honda 25. Vibrio vulnificus James D. Oliver • 349 26. Miscellaneous Human Pathogens • 367 Mitsuaki Nishibuchi Animal Pathogens 18. The Biology and Pathogenicity of Vibrio anguillarum and V. ordalii • 251 Jorge H. Crosa, Luis A. Actis, and Marcelo E. Tolmasky 19. Vibrio harveyi: Pretty Problems in Paradise • 266 Leigh Owens and Nancy Busico-Salcedo 20. Vibrio salmonicida Brian Austin VIII. The Impact of Genomics and Proteomics in the Study of Human Pathogens • 281 IX. 27. Epidemiology • 385 Shah M. Faruque and G. Balakrish Nair X. 22. Miscellaneous Animal Pathogens • 297 Brian Austin Applications 28. Biotechnological Applications J. Grant Burgess XI. 21. Vibrio splendidus • 285 Frédérique Le Roux and Brian Austin Epidemiology • 401 Conclusions 29. Conclusions • 409 Fabiano L. Thompson, Brian Austin, and Jean Swings Index • 417 CONTRIBUTORS Luis A. Actis Department of Microbiology, Miami University, Oxford, Ohio 45056 Jorge H. Crosa Department of Molecular Microbiology and Immunology, School of Medicine, Oregon Health and Science University, Portland, Oregon 97201-3098 Brian Austin School of Life Sciences, John Muir Building, Heriot-Watt University, Riccarton, Edinburgh, EH14 4AS, Scotland, United Kingdom Shah M. Faruque Molecular Genetics Laboratory, International Centre for Diarrhoeal Disease Research, Bangladesh, Mohakhali, Dhaka-1212, Bangladesh Douglas H. Bartlett Marine Biology Research Division (0202), Scripps Institution of Oceanography, University of California, San Diego, La Jolla, California 92093-0202 Dirk Gevers Laboratory of Microbiology, Ghent University, K. L. Ledeganckstraat 35, B-9000 Ghent, Belgium Bruno Gomez-Gil CIAD, A.C. Mazatlán Unit for Aquaculture and Environmental Management, A.P. 711, Mazatlán, Sin. 82000, México Yan Boucher Department of Chemistry and Biomolecular Sciences, Macquarie University, Sydney, NSW 2109, Australia J. Grant Burgess School of Marine Science and Technology, Armstrong Building, University of Newcastle, Newcastle Upon Tyne NE1 7RU, United Kingdom Takeshi Honda Department of Bacterial Infections, Research Institute for Microbial Diseases, Osaka University, 3-1 Yamadaoka, Suita, Osaka 565-0871, Japan Nancy Busico-Salcedo College of Veterinary Medicine, University of Southern Mindanao, Kacacan, 9407 Cotabato, Philippines Tetsuya Iida Department of Bacterial Infections, Research Institute for Microbial Diseases, Osaka University, 3-1 Yamadaoka, Suita, Osaka 565-0871, Japan Ana Coelho Department of Genetics, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, CEP 21944-970, Brazil Staffan Kjelleberg School of Biotechnology and Biomolecular Sciences, Centre for Marine Biofouling and Bio-Innovation, University of New South Wales, Sydney 2052, Australia R. R. Colwell Center for Bioinformatics and Computational Biology (CBCB), Agriculture/Life Sciences Surge Bldg. #296, Room 3103, University of Maryland, College Park, Maryland 20740 Karl E. Klose South Texas Center for Emerging Infectious Diseases and Department of Biology, The University of Texas at San Antonio, San Antonio, Texas 78249 ix x CONTRIBUTORS Omry Koren Department of Molecular Microbiology and Biotechnology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Ramat Aviv 69978, Israel Martin F. Polz Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, Massachusetts 02139 Ken Kurokawa Laboratory of Comparative Genomics, Graduate School of Information Science, Nara Institute of Science and Technology, 8916-5 Takayamacho, Ikoma 630-0192, Japan Michael G. Prouty South Texas Center for Emerging Infectious Diseases and Department of Biology, The University of Texas at San Antonio, San Antonio, Texas 78249 Frédérique Le Roux Laboratoire de Génétique et Pathologie, Ifremer, BP 133, Ronce les bains, 17390 La Tremblade, France Irma Nelly G. Rivera Department of Microbiology, Biomedical Science Institute, University of São Paulo, São Paulo, CEP 05508-900, Brazil Didier Mazel Unité postulante “Plasticité du Génome Bactérien,”— CNRS URA 2171, Dept. Structure et Dynamique des Génomes, Institut Pasteur, 75724 Paris, France Ana Roque Instituto de Recerca i Tecnologia Agroalimentaries, Centre d’Aquicultura, AP200 Sant Carles de la Rapita 43540, Spain Linda L. McCarter Microbiology Department, The University of Iowa, Iowa City, Iowa 52242 Diane McDougald School of Biotechnology and Biomolecular Sciences, Centre for Marine Biofouling and Bio-Innovation, University of New South Wales, Sydney 2052, Australia G. Balakrish Nair Laboratory Sciences Division, International Centre for Diarrhoeal Disease Research, Bangladesh, Mohakhali, Dhaka-1212, Bangladesh Mitsuaki Nishibuchi Center for Southeast Asian Studies, Kyoto University, Yoshida, Sakyo-ku, Kyoto 606-8501, Japan James D. Oliver Department of Biology, University of North Carolina at Charlotte, Charlotte, North Carolina 28223 Eugene Rosenberg Department of Molecular Microbiology and Biotechnology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Ramat Aviv 69978, Israel Dean A. Rowe-Magnus Department of Microbiology, Sunnybrook & Women’s College Health Sciences Centre, Toronto, Ontario M4N 3N5, Canada Tomoo Sawabe Laboratory of Microbiology, Graduate School of Fisheries Sciences, Hokkaido University, 3-1-1 Minato-cho, Hakodate 041-8611, Japan Eric V. Stabb University of Georgia, Department of Microbiology, 828 Biological Sciences, Athens Georgia 30602 Leigh Owens Microbiology and Immunology, School of Veterinary and Biomedical Sciences, James Cook University, Townsville 4811, Australia Hatch W. Stokes Department of Chemistry and Biomolecular Sciences, Macquarie University, Sydney, NSW 2109, Australia Kwan-Sam Park Department of Bacterial Infections, Research Institute for Microbial Diseases, Osaka University, 3-1 Yamadaoka, Suita, Osaka 565-0871, Japan Jean Swings Laboratory of Microbiology and BCCM/LMG Bacteria Collection, Ghent University, K. L. Ledeganckstraat 35, B-9000 Ghent, Belgium CONTRIBUTORS Fabiano L. Thompson Microbial Resources Division and Brazilian Collection of Environmental, and Industrial Micro-organisms (CBMAI), CPQBA, UNICAMP, Alexandre Caselatto 999, CEP 13140000, Paulínia, Brazil Janelle R. Thompson Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, Massachusetts 02139 Marcello E. Tolmasky Department of Biology, College of Natural Sciences and Mathematics, California State University— Fullerton, Fullerton, California 92834-6850 Hidetoshi Urakawa Center for Advanced Marine Research, Ocean Research Institute, The University of Tokyo, 1-15-1 Minamidai, Nakano, Tokyo 164-8639, Japan xi Yves Van de Peer BioInformatics & Evolutionary Genomics, Ghent University/VIB Technologiepark 927, B-9052 Ghent, Belgium Ana Carolina P. Vicente Department of Genetics, Instituto Oswaldo Cruz, Rio de Janeiro, CEP 21045-900, Brazil Michelle D. Vieira Department of Genetics, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, CEP 21944-970, Brazil Mohammed Zouine Unité Postulante “Plasticité du Génome Bactérien,”—CNRS URA 2171, Dept. Structure et Dynamique des Génomes, Institut Pasteur, 75724 Paris, France This page intentionally left blank PREFACE Two decades has passed since the last dedicated textbook on the vibrios, i.e. Vibrios in the Environment, which was edited by R. R. Colwell. Since then, there have been tremendous developments in the knowledge of the vibrios, including improvements in the taxonomy, ecology, and pathogenicity of the group. Indeed, vibrios are the best studied of all aquatic bacteria. Many new species have been described, and exciting concepts have been proposed. Improved detection, characterization, and identification tools have been developed to enable the rapid screening of strains. Molecular biology analyses and, more recently, whole genome sequencing of several vibrios, have shed much light on the biology of these microbes in their natural habitats and opened up new avenues for basic and applied research. It is therefore timely to compile a volume containing data about the current status of research and understanding of the vibrios. For this, we are grateful to the co-operation of the numerous authors, all of whom have produced manuscripts within a tight time frame. ASM Press was especially helpful during all stages of the book, from the nurturing of the original idea to the professional editing of the text, to the production of the finished volume. The result is a book that is primarily targeted at bacterial taxonomists, microbial ecologists, genome researchers, health management workers, and postgraduate and senior undergraduate students. We are grateful to the following publishers, who have given permission to use copyrighted material: ASM Press, Blackwell Publishing, Boxwood Press, Elsevier Science BV, and the Proceedings of the National Academy of Sciences, USA. Numerous scientists have provided original photographs, and for these we acknowledge J. Bina, M. N. Guentzel, J. Mekalanos, J. Oakey, J. Reidl and F. Yildiz. We hope the book will be a fitting tribute to those who have worked assiduously to improve the understanding of this fascinating group of vibrios. F. L. Thompson, B. Austin, and J. Swings August 2005 xiii This page intentionally left blank I. INTRODUCTION This page intentionally left blank The Biology of Vibrios Edited by F. L. Thompson et al. © 2006 ASM Press, Washington, D.C. Chapter 1 A Global and Historical Perspective of the Genus Vibrio R. R. COLWELL Vibrios have played a significant role in human history. Outbreaks of cholera, caused by Vibrio cholerae, can be traced back in time to early recorded descriptions of enteric infections. Indeed, the path of human history has been influenced significantly by this organism (Wendt, 1885; Pollitzer, 1959). First described by Pacini (1854) while he was a medical student in Italy and at a time when the germ theory of disease was in dispute, V. cholerae was subsequently identified and described in greater detail by Robert Koch (1883, 1884), to whom credit for the discovery of the causative agent of cholera traditionally has been given. However, Pacini was rescued from obscurity and provided recognition for his pioneering work; his stained microscope slides remain on display at the University of Verona, Italy. Volumes have been published on cholera, its origins, pathology, and epidemiology, rendering V. cholerae one of the most studied of the bacterial species (Wachsmuth et al., 1994). The germ theory of disease was developed in the 19th century, based on the British queen’s physician John Snow’s tracing an 1849 cholera outbreak to a single contaminated well in the Broad Street area of central London; it remains a canonical example of epidemiology. Snow’s demonstration that the contaminated communal hand-operated pump was supplied by a particular water company remains equally powerful today. Snow’s book was an important milestone in public health, correctly identifying the fecaloral route to human infection and offering powerful arguments for the germ theory (Snow, 1855). Many advances in the prevention and treatment of infectious diseases during the latter half of the 19th century and the first half of the 20th century follow directly from the acceptance of Snow’s point of view. Yet, in 2002,
120,000 cases of cholera were reported, and
3,700 resulted in death (World Health Organization, 1992). The vibrios have also received the attention of marine microbiologists who observed that the readily cultured bacterial populations in near-shore waters and those associated with fish and shellfish were predominantly Vibrio spp. For example, the “gut group” vibrios were described by Liston (1954, 1957), working at the Marine Laboratory in Aberdeen, Scotland. Fish diseases caused by vibrios have been reviewed extensively by many investigators (Austin, in press) and, among the many fish pathogens, Vibrio anguillarum has been recognized historically as a major pathogen of marine animals. In the 1950s, Vibrio parahaemolyticus was first isolated and described by Japanese medical scientists, and the major epidemics caused by this Vibrio species have been extensively documented (Takeda, 1988). V. parahaemolyticus was subsequently shown to have an annual cycle of abundance in near-shore marine waters and estuaries, particularly in association with zooplankton (Kaneko and Colwell, 1973, 1975, 1978). The biology, ecology, and pathogenicity of V. parahaemolyticus have been extensively reviewed and are addressed in this book. A third significant human pathogenic species of the genus, Vibrio vulnificus, has stimulated extensive research, and the literature is rich with descriptions of its ecology, pathogenicity, and biology (Oliver, 1995). Shared characteristics of these vibrios include requirement for salt for growth (either that sufficient in prepared bacteriological media or requiring amendment to concentrations of 1 to 3% [wt/vol] NaCl), chitin digestion, and general morphological features, i.e., curved rods. Vibrios are fermentative in metabolism and, most recently, have been found to carry two chromosomes (Heidelberg et al., 2000). Many Vibrio spp. are bioluminescent, including V. cholerae and V. fischeri, the genes for bioluminescence having been characterized and detected in Vibrio spp. by employing gene probes and Rita R. Colwell • Center for Bioinformatics and Computational Biology (CBCB), Biomolecular Sciences Bldg. #296, Room 3103, University of Maryland, College Park, MD 20742. 3 4 COLWELL genomic sequencing (see Palmer and Colwell, 1991; Heidelberg et al., 2000). Over the past 20 years, many nonpathogenic species of Vibrio have been described, including V. diazotrophicus (Guerinot et al., 1982), a nitrogen-fixing species, and species associated with marine mammals, e.g., V. carchariae (Grimes et al., 1989). Clearly, a wider role of vibrios in the environment, notably in nutrient cycling, has begun to be appreciated. The complete genome sequences of V. cholerae, V. parahaemolyticus, and V. vulnificus have been determined, providing a rich set of data illuminating the metabolic versatility of these species. Recently, a Vibrio sp. isolated from a hydrothermal vent has been sequenced (unpublished data). Interestingly, extensive sequence similarity among genes of the three previously sequenced Vibrio spp. and the vent vibrio has been observed (Fig. 1), suggesting a historical origin in the deep sea. Thus, comparative genomics of the vibrios, based on complete genomic sequences, is now possible and highly useful in establishing both a phylogenomic taxonomy and a biogeography for the genus (manuscript in preparation). Vibrios are clearly very important inhabitants of the riverine, estuarine, and marine aquatic environments. For this reason, by taking the perspective of a global microbial ecology of the vibrios, a deeper understanding of microbial ecological systems can be gained. V. cholerae provides a useful example and is therefore discussed here in the context of a general pattern of environmental pathogens and their close linkage with climate, weather systems, seasonality, and physical and chemical parameters. Through such an analysis, the vibrios can be more fully appreciated in their many activities and functions (Colwell, in press; unpublished data). Today, the study of infectious disease, whether of humans, animals, or plants, draws insight from a series of contexts, each nesting like one concentric circle within the last, from nanoscience to genomics and from mathematics, ecology, geography, and social science to climatology. The connections between cholera—an ancient and extensively studied waterborne disease—and the environment provide a valuable paradigm for this perspective. Fully dimensional understanding of an infectious disease, whether cholera, hantavirus, or malaria, reaches from countries to continents and beyond and connects medicine to many viewpoints across science and engineering, and even to daily life. A global context indisputably frames all human health issues in the 21st century. This context is formed of several realities: the worldwide movement of people and goods, the new recognition that earth processes operate on a global scale, and a dynamic international scientific enterprise. Science and engineering have always flourished across national borders, but the current global scale of research is unprecedented. As research grows increasingly interdisciplinary, more scientific questions surmount national borders. A study of the vibrios suitably must address the concentric circles surrounding the diseases caused by vibrios, as well as their Figure 1. Comparison of the V. parahaemolyticus genome (upper) and V. cholerae (lower) genome sequences with the genome sequence of a recently isolated Vibrio sp. from a hydrothermal vent in the East Pacific Rise. CHAPTER 1 many functions and capabilities—notably, the international setting and the philosophical construct of biocomplexity (Colwell, 2002; R. R. Colwell, Editorial, EcoHealth 1:6–7, 2004). Therefore, it can be instructive to compare selected cases of infectious diseases, whether of humans, animals, or plants, in their ecological and climatological environments, providing context for the case of cholera and the geographical distribution of vibrios. V. cholerae serves as a paradigm for this perspective and a model, perhaps, of a larger perspective for understanding the more general role of vibrios in nature. The concentric circles of many disciplines provide insights from mathematics, ecology, oceanography, and the space and social sciences. World Health Organization (WHO) data provide a useful starting point (Fig. 2). Infectious diseases cause about one-quarter of deaths worldwide (not including cancer and cardiovascular and respiratory diseases, many of which have recently been shown to be caused by infections). Broken down into the six leading infectious killers, diarrheal diseases, not long ago number one, are currently third overall—but still rank second for children under age 5 (Fig. 3). The major cause of death for children 4 years old and under is infectious disease, which causes almost two-thirds, or 63%, of these deaths (Fig. 4), and outbreaks of cholera substantially exceed those of any other disease. Thus, V. cholerae ranks near the top of the list of human pathogens, and these data constitute some of the largest concentric circles that frame today’s global context for environment and health. International travel has skyrocketed in the past half century, with more than 500 million inter- • A GLOBAL PERSPECTIVE 5 national arrivals per year by 2000, and continuing to climb. Thus, the ubiquity of selected pathogens in the environment and the ease of transmissibility by the migration of people and goods justify consideration of the vibrios, commonly present in riverine, estuarine, and coastal systems, at a global level. The international arena is one context, and another is conceptual—the framework termed biocomplexity, which denotes the study of complex interactions in biological systems, including humans, and their physical environments (Colwell, 2002; R. R. Colwell, Editorial, EcoHealth 1:6–7, 2004). Ecosystems do not respond linearly to environmental change, nor do the microorganisms that live in them. It is important to underscore the point that understanding demands observing at multiple scales, from the nano to the global. Complexity principles emerge at each level: the cell, organism, community, and ecosystems. With the perspective of biocomplexity, disciplinary worlds, formerly discrete, intersect to form fuller, more nuanced viewpoints and integrate across disciplines and scales, a perspective that roots epidemiology firmly in ecology. As signals from climate models are recognized and incorporated into health measures, new opportunities arise for proactive—rather than reactive—approaches to public health, providing the basis for a new kind of medicine, a predictive, hence a preemptive, medicine. Indeed, ecology has immediate lessons for epidemiology. One useful model is the mosquito that lays its eggs in North American carnivorous plants, the pitcher plants, which are similar to plants that harbor mosquitoes in Southeast Asia. Although the Figure 2. Leading causes of death (57.02 million) worldwide in 2002. Reproduced from the World Health Organization, with permission.