The BIOLOGYof VIBRIOS
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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.
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Cover figure: Colonial morphology of vibrios in different media (courtesy of Gomez-Gil and Roque
[see Chapter 2]).
To Huai-Shu Xu
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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
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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
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I. INTRODUCTION
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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.