Front Matter

Cambridge University Press 978-0-521-86297-4 - Horizontal Gene Transfer in the Evolution of Pathogenesis Edited by Michael Hensel and Herbert Schmidt Frontmatter More information

Horizontal Gene Transfer in the Evolution of Pathogenesis

Horizontal gene transfer is a major driving force in the evolution of many bacterial pathogens. The development of high-throughput sequencing tools and more sophisticated genomic and proteomic techniques in recent years has resulted in a better understanding of this phenomenon. Written by leading experts in the ﬁeld, this edited volume is aimed at graduate students and researchers and provides an overview of current knowledge relating to the evolution of microbial pathogenicity. This volume provides an overview of the mechanisms and biological consequences of the genome rearrangements resulting from horizontal gene transfer, in both prokaryotes and eukaryotes, as well as overviews of the key mobile genetic elements involved. Subse- quent chapters focus on paradigms for the evolution of important bacterial pathogens, including Salmonella enterica, Streptococcus pneumoniae,and Staphylococcus aureus. The inﬂuence of socioeconomic parameters in the dissemination of transferable elements, such as antibiotic-resistant genes in bacteria, is also discussed.

Michael Hensel is currently Professor of Microbiology and Immunology at the University of Erlangen in Germany.

Herbert Schmidt is currently Professor of Food Microbiology at the Univer- sity of Hohenheim in Germany.

© Cambridge University Press www.cambridge.org More information Frontmatter Edited byMichaelHenselandHerbertSchmidt 978-0-521-86297-4 -HorizontalGeneTransferintheEvolutionofPathogenesis Cambridge UniversityPress © Cambridge University Press AMCM

ADVANCES IN MOLECULAR AND n CELLULAR MICROBIOLOGY irognssa h oeua level. molecular of the understanding at been future microorganisms our have for bacteria implications model immense and with sequenced, pathogenic fully of number the growing biology, a molecular current of in of revolution genomes part this no of integrated are part an As and biology research. tools microbiological cellular vital evolutionary but and complex areas a Molecular subject be discrete products. longer to gene out competing turning is of bacteria what battle in pathogenic cells how host with revealing interact is of microbiology cellular fusion Cellular eukaryotic the and microbiology. is biology, microbiology molecular in microbial advance microbiology, classical recent revolutionized. been exciting has most example, the for level, Perhaps molecular the animal at their hosts with plant interact and viruses and bacteria pathogenic evolutionary how and of diversity and microbial biology of understanding Our all. of influ- of been in most areas perhaps enced whole techniques has Microbiology transformed of sciences. has biological array the biology across an molecular research and of cellular development of rapid fields the the decade, past the Over tBrhlmwsadRylLno optl London Hospital, London Royal and Bartholomew’s St Curtis Michael Professor London School, Medical Hospital George’s St Coates Anthony Sir Professor London College, University Wilson Michael Professor London College, University Henderson Brian Professor Editors Series research. microbiological the current with in up keep literature to diversifying researchers rapidly research. and current students examine graduate as enable microbiology well will as molecular series area, This or the cellular of overview of an vol- aspect provide Each will particular and fields. a expanding on rapidly focus will and ume exciting these in active researchers dacsi oeua n ellrMicrobiology Cellular and Molecular in Advances sasre dtdby edited series a is www.cambridge.org Cambridge University Press 978-0-521-86297-4 - Horizontal Gene Transfer in the Evolution of Pathogenesis Edited by Michael Hensel and Herbert Schmidt Frontmatter More information

Published Titles

1. Bacterial Adhesion to Host Tissues: Mechanisms and Consequences. Edited by Michael Wilson 9780521801072 2. Bacterial Evasion of Host Immune Responses. Edited by Brian Henderson and Petra Oyston 9780521801737 3. Dormancy and Low Growth States in Microbial Diseases. Edited by Anthony Coates 9780521809405 4. Susceptibility to Infectious Diseases: The Importance of Host Genetics. Edited by Richard Bellamy 9780521815253 5. Bacterial Invasion of Host Cells. Edited by Richard Lamont 9780521809542 6. Mammalian Host Defense Peptides. Edited by Deirdre A. Devine and Robert E. W. Hancock 9780521822206 7. Bacterial Protein Toxins: Role in the Interference with Cell Growth Regulation. Edited by Alistair Lax 9780521820912X 8. The Dynamic Bacterial Genome. Edited by Peter Mullany 9780521821575 9. Salmonella Infections: Clinical, Immunological and Molecular Aspects. Edited by Pietro Mastroeni and Duncan Maskell 9780521835046 10. The Inﬂuence of Cooperative Bacteria on Animal Host Biology. Edited by Margaret J. McFall-Ngai, Brian Henderson, and Edward G. Ruby 9780521834650 11. Bacterial Cell-to-Cell Communication: Role in Virulence and Pathogenesis. Edited by Donald R. Demuth and Richard Lamont 9780521846387 12. Phagocytosis of Bacteria and Bacterial Pathogenicity. Edited by Joel D. Ernst and Olle Stendahl 9780521845694 13. Bacterial-Epithelial Cell Cross-Talk: Molecular Mechanisms in Pathogenesis. Edited by Beth A. McCormick 9780521852449 14. Dendritic Cell Interactions with Bacteria. Edited by Maria Rescigno 9780521855860 15. Bacteriophage Ecology: Population Growth, Evolution, and Impact of Bacterial Viruses. Edited by Stephen T. Abedon 9780521858458

© Cambridge University Press www.cambridge.org Cambridge University Press 978-0-521-86297-4 - Horizontal Gene Transfer in the Evolution of Pathogenesis Edited by Michael Hensel and Herbert Schmidt Frontmatter More information

Advances in Molecular and Cellular Microbiology 16

Horizontal Gene Transfer in the Evolution of Pathogenesis

EDITED BY MICHAEL HENSEL University of Erlangen, Germany

HERBERT SCHMIDT University of Hohenheim, Germany

cambridge university press Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, Sao˜ Paulo, Delhi

Cambridge University Press 32 Avenue of the Americas, New York, NY 10013–2473, USA

www.cambridge.org Information on this title: www.cambridge.org/9780521862974

c Cambridge University Press 2008

This publication is in copyright. Subject to statutory exception and to the provisions of relevant collective licensing agreements, no reproduction of any part may take place without the written permission of Cambridge University Press.

First published 2008

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Library of Congress Cataloging in Publication Data

Horizontal gene transfer in the evolution of pathogenesis / [edited by] Michael Hensel, Herbert Schmidt. p. ; cm. – (Advances in molecular and cellular microbiology; 16) Includes bibliographical references and index. ISBN 978-0-521-86297-4 (hardback) 1. Genetic transformation. 2. Bacterial diseases – Pathogenesis. 3. Molecular evolution. I. Hensel, Michael, 1962– II. Schmidt, Herbert, 1961– III. Title. IV. Series. [DNLM: 1. Gene Transfer, Horizontal. 2. Bacterial Infections – etiology. 3. Evolution, Molecular. QW 51 H8115 2008] QH448.4.H67 2008 579.3165–dc22 2007041583

ISBN 978-0-521-86297-4 hardback

Cambridge University Press has no responsibility for the persistence or accuracy of URLs for external or third-party Internet Web sites referred to in this publication and does not guarantee that any content on such Web sites is, or will remain, accurate or appropriate.

We dedicate this book to our mentors Jurgen¨ Heesemann and Helge Karch

Contents

Preface page xi Contributors xv

PART I Theoretical Considerations on the Evolution of Bacterial Pathogens

1 Genomes in Motion: Gene Transfer as a Catalyst for Genome Change 3 Jeffrey G. Lawrence and Heather Hendrickson

2 Bacterial Recombination in vivo 23 Xavier Didelot and Daniel Falush

PART II Mobile Genetic Elements in Bacterial Evolution

3 Phage-bacterium Co-evolution and Its Implication for Bacterial Pathogenesis 49 Harald Brussow¨

4 The Role of Bacteriophages in the Generation and Spread of Bacterial Pathogens 79 Roger W. Hendrix and Sherwood R. Casjens

5 Genomic Islands in the Bacterial Chromosome – Paradigms of Evolution in Quantum Leaps 113 Tobias Olschl¨ ager¨ and Jorg¨ Hacker

PART III Paradigms of Bacterial Evolution

6 Genomic Islands in Plant-pathogenic Bacteria 137 Dawn L. Arnold and Robert W. Jackson

7 Prophage Contribution to Salmonella Virulence and Diversity 159 Sebastien´ Lemire, Nara Figueroa-Bossi, and Lionello Bossi

8 Pathogenic Yersinia: Stepwise Gain of Virulence due to Sequential Acquisition of Mobile Genetic Elements 193 Elisabeth Carniel

9 Genomic or Pathogenicity Islands in Streptococcus pneumoniae 217 Barbara Albiger, Christel Blomberg, Jessica Dagerhamn, Staffan Normark, and Birgitta Henriques-Normark

10 The Mobile Genetic Elements of Staphylococcus aureus 237 Richard P. Novick x 11 Inﬂuence of Human Lifestyle on Dissemination of Transferable Elements 273 Wolfgang Witte contents PART IV Interkingdom Transfer and Endosymbiosis

12 Eukaryotic Gene Transfer: Adaptation and Replacements 293 Jan O. Andersson

13 Lessons in Evolution from Genome Reduction in Endosymbionts 317 Andres´ Moya and Amparo Latorre

Index 335

Preface

During the past 25 years, a nearly exponential increase has occurred in nucleotide sequences available from databases. The first microbial genomes were published in 1995 (Fleischmann et al., 1995; Fraser et al., 1995; Himmel- reich et al., 1996); the NCBI database currently contains 534 complete bacterial chromosome sequences. The genomes have been determined not only from different species, but also from different strains of the same species. This has paved the way for comparative genomics and has allowed detailed analysis of genetic differences between strains (Wren, 2000; Dobrindt and Hacker, 2001; Edwards, Olsen, and Maloy, 2002; Raskin, Seshadri, Pukatzki, and Mekalanos, 2006). Since infectious diseases are a major health threat worldwide and range among the most frequent causes of death worldwide (WHO Health Statistics 2006), it is not surprising that the first two organisms to be sequenced were pathogenic bacteria. During the past decade many attempts have been made to understand the molecular basis of microbial pathogenicity, and our knowledge has advanced quickly, in particular through the use of methods of cellular biology, genomics, and proteomics. Various events in the pathogenesis of microbial infections, such as adherence to and entry into human and animal host, invasion of host cells, toxin production, establishment and dissemination of bacterial populations in the host, and the role of the host immune system, have been studied in detail for many host-pathogen interactions. In most cases, the specific features that define microbial pathogenicity are encoded by mobile genetic elements such as bacteriophages, plasmids, and pathogenicity islands, and fast transferability is often facilitated by transpos- able elements (for reviews, see Finlay and Falkow, 1997; Low and Porter, 1978).

In particular, the sequencing of whole genomes and the development of more sophisticated bioinformatics tools have shown that the genomes of microorganisms in even a single species may vary enormously (for example, in Staphylococcus aureus;seeChapter 10). Improved methods for generation and analysis of sequence data, as well as application of techniques for molecular typing, such as multilocus sequence typing (MLST) and single-nucleotide polymorphism (SNP) analyses, have been used throughout the kingdoms of life and have shown that the sequence diversity between organisms, even between members of the same species, is greater than previously suspected. Microorganisms can be found in every ecological niche on earth, and this ecological speciation could occur only through the acquisition of new genetic xii traits. Although horizontal gene transfer is much more elaborate in eukaryotic cells and can lead to changes in the progeny by meiosis and mitosis, recombination events also take place in bacteria following DNA uptake in many ways preface (Andersson, 2005; Ochman, Lawrence, and Groisman, 2000). Adaptation of bacteria to extreme environments is a consequence of changes in the genetic content and is stabilized by selective pressure. Genome changes may develop by gene loss, gene duplication, gene mutation, or acquisition of new genetic material by lateral gene transfer (LGT; Lawrence and Hendrickson, 2003; Ochman and Moran, 2001; Campbell, 2000). It has been hypothesized that between 1.6% and 32% of the genes of a given genome have been acquired by LGT (Ochman, Lawrence, and Groisman, 2000; Koonin, Makarova, and Aravind, 2001; Marri, Hao, and Golding, 2007). The main mechanisms of DNA uptake in bacteria are conjugation, trans- duction, and transformation. These mechanisms must be followed by recombination events that allow the genetic traits to be inserted more or less stably into the chromosome. As Low and Porter summarized in 1978: “The term recombination can be used in a sense that it means a reassortment of series of nucleotides along nucleic acid molecules.” In this book, articles on the basics of lateral gene transfer are provided by authors who are leading scientists in the ﬁeld. In the ﬁrst part, the chapters written by Jeffrey G. Lawrence and Heather Hendrickson (Chapter 1) and by Xavier Didelot and Daniel Falush (Chapter 2) provide an overview of the impact and the mechanisms of LGT as well as detailed insight into the mathematical approaches in evolutionary biology. The second part of the book contains contributions to the role of dis- tinct mobile genetic elements in bacterial evolution. This section contains comprehensive chapters on the role of bacteriophages as “accelerators” of bacterial evolution by Harald Brussow¨ (Chapter 3) and on the global

impact of bacteriophages (Chapter 4) from Roger W. Hendrix and Sherwood R. Casjens. Whereas the chapter by Hendrix and Casjens explains mechanisms of gene acquisition and moron acquisition of Gram-negative bacteria and their phages, Harald Brussow¨ points out the predator-prey relationship and gives a more evolutionary view of bacteriophages. A further important group of mobile genetic elements are genomic islands (GEI), in particular the subgroup of pathogenicity islands (PAI). In Chapter 5, Tobias Olschl¨ ager¨ and Jorg¨ Hacker describe the structure and function of these elements and provide various examples for the impact of GEI and PAI in bacterial evolution. The third part of the book includes a selection of paradigms for the evolution of important bacterial pathogens. Dawn L. Arnold and Robert W. Jack- xiii son provide a state-of-the art chapter on genomic islands in plant-pathogenic preface bacteria (Chapter 6); Sebastien´ Lemire, Nara Figueroa-Bossi, and Lionello Bossi focus on the contribution of prophages to virulence and diversity of Salmonella enterica serovars (Chapter 7). Elisabeth Carniel describes in Chap- ter 8 how pathogenicity and transmission in the genus Yersinia progressively evolved together with the gradual acquisition of foreign mobile genetic elements. Genomic and pathogenicity islands of Streptococcus pneumoniae are addressed in Chapter 9 by Barbara Albiger, Christel Blomberg, Jessica Dager- hamn, Staffan Normark, and Birgitta Henriques-Normark. In Chapter 10, Richard P. Novick provides detailed information on the current knowledge on mobile genetic elements of Staphylococcus aureus.In the last part of this section, Wolfgang Witte sheds light on the influence of socioeconomic parameters on the dissemination of transferable elements (Chapter 11). The specific emphasis of this chapter is on the spread of antibiotic-resistant genes in bacteria. In the last section, Jan O. Andersson gives insight into gene transfer events in eukaryotes (Chapter 12). Finally, in Chapter 13 Andres´ Moya and Amparo Latorre describe the events that are involved in genome reduction of bacterial endosymbionts in the paradigmatic system of aphids and their endosymbionts Buchneria spp. The information given in this book shows clearly that LTG is a driving force in the evolution of various groups of bacterial pathogens; however, LTG is not restricted to this kingdom. The tools of high-throughput sequencing and the development of more sophisticated bioinformatics and genome and proteome techniques facilitate the analysis of LGT and recombination and help us to understand the processes of diversification, reduction, and adaptation to different environments.

REFERENCES

Andersson, J. O. (2005). Lateral gene transfer in eukaryotes. Cell Mol Life Sci, 62, 1182–97. Campbell, A. M. (2000). Lateral gene transfer in prokaryotes. Theor Popul Biol, 57, 71–7. Dobrindt, U., and Hacker, J. (2001). Whole genome plasticity in pathogenic bacteria. Curr Opin Microbiol, 4, 550–7. Edwards, R. A., Olsen, G. J., and Maloy, S. R. (2002). Comparative genomics of closely related salmonellae. Trends Microbiol, 10, 94–9. Finlay, B. B., and Falkow, S. (1997). Common themes in microbial pathogenicity revisited. Microbiol Mol Biol Rev, 61, 136–69. xiv Fleischmann, R. D., Adams, M. D., White, O., et al. (1995). Whole-genome ran- dom sequencing and assembly of Haemophilus influenzae Rd. Science, 269, 496–512. Fraser, C. M., Gocayne, J. D., White, O., et al. (1995). The minimal gene comple- preface ment of Mycoplasma genitalium. Science, 270, 397–403. Himmelreich, R., Hilbert, H., Plagens, H., et al. (1996). Complete sequence analysis of the genome of the bacterium Mycoplasma pneumoniae. Nucleic Acids Res, 24, 4420–49. Koonin, E. V., Makarova, K. S., and Aravind, L. (2001). Horizontal gene transfer in prokaryotes: Quantification and classification. Annu Rev Microbiol, 55, 709–42. Lawrence, J. G., and Hendrickson, H. (2003). Lateral gene transfer: When will adolescence end? Mol Microbiol, 50, 739–49. Low, K. B., and Porter, D. D. (1978). Modes of gene transfer and recombination in bacteria. Annu Rev Genet, 12, 249–87. Marri, P. R., Hao, W., and Golding, G. B. (2007). The role of laterally transferred genes in adaptive evolution. BMC Evol Biol, 7 (Suppl 1), S8. Ochman, H., Lawrence, J. G., and Groisman, E. A. (2000). Lateral gene transfer and the nature of bacterial innovation. Nature, 405, 299–304. Ochman, H., and Moran, N. A. (2001). Genes lost and genes found: Evolution of bacterial pathogenesis and symbiosis. Science, 292, 1096–9. Raskin, D. M., Seshadri, R., Pukatzki, S. U., and Mekalanos, J. J. (2006). Bacterial genomics and pathogen evolution. Cell, 124, 703–14. Wren, B. W. (2000). Microbial genome analysis: Insights into virulence, host adaptation and evolution. Nat Rev Genet, 1, 30–9.

Contributors

Barbara Albiger Lionello Bossi Lund University Centre de Gen´ etique´ Moleculaire´ Department of Medical CNRS Microbiology 91198 Gif-sur-Yvette Malmo,¨ Sweden France

Jan O. Andersson Harald Brussow¨ Institute of Cell and Molecular Nestle´ Research Centre Biology, 26 Vers-chez-les-Blanc Uppsala University, Biomedical CH-1000 Lausanne Center, Switzerland Box 596, S-751 24 Uppsala, Sweden Elisabeth Carniel Yersinia Research Unit Dawn L. Arnold Institut Pasteur Centre for Research in Plant Science 28 Rue du Dr. Roux University of the West of England 75724 Paris Cedex 15 Bristol France UK Sherwood R. Casjens Christel Blomberg Pathology Department Swedish Institute for Infectious 5200 Emma Eccles Jones Medical Disease Control and Department Research Building of Microbiology University of Utah School of Tumor and Cell Biology Medicine Karolinska Institutet Salt Lake City, UT 84112 Solna, Sweden USA

Jessica Dagerhamn Heather Hendrickson Swedish Institute for Infectious Department of Biological Disease Control and Department Sciences of Microbiology University of Pittsburgh Tumor and Cell Biology Pittsburgh, PA 15260 Karolinska Institutet USA Solna Sweden Roger W. Hendrix Pittsburgh Bacteriophage Institute Xavier Didelot and Department of Biological Peter Medawar Building for Sciences xvi Pathogen Research A340 Langley Hall South Parks Road University of Pittsburgh Oxford OX1 3SY Pittsburgh, PA 15260 UK USA

Daniel Falush Birgitta Henriques-Normark contributors Peter Medawar Building for Swedish Institute for Infectious Pathogen Research Disease Control and Department South Parks Road of Microbiology Oxford OX1 3SY Tumor and Cell Biology UK Karolinska Institutet Solna Nara Figueroa-Bossi Sweden Centre de Gen´ etique´ Moleculaire´ CNRS Michael Hensel 91198 Gif-sur-Yvette Mikrobiologisches Institut France Universitatsklinikum¨ Erlangen Wasserturmstr. 3-5 Jorg¨ Hacker 91054 Erlangen Institut fur¨ Molekulare Germany Infektionsbiologie Universitat¨ Wurzburg¨ Robert W. Jackson Rontgenring¨ 11 School of Biological Sciences 97070 Wurzburg¨ University of Reading Germany Reading UK

Amparo Latorre Richard P. Novick Institut Cavanilles de Biodiversitat i Skirball Institute and Department Biolog´ıa Evolutiva of Microbiology Universitat de Valencia` New York University School Spain of Medicine 540 First Avenue Jeffrey G. Lawrence New York, NY 10016 Department of Biological USA Sciences University of Pittsburgh Tobias Olschl¨ ager¨ Pittsburgh, PA 15260 Institut fur¨ Molekulare USA Infektionsbiologie xvii Universitat¨ Wurzburg¨ contributors Sebastien´ Lemire Rontgenring¨ 11 Centre de Gen´ etique´ Moleculaire´ 97070 Wurzburg¨ CNRS Germany 91198 Gif-sur-Yvette France Herbert Schmidt Institut fur¨ Andres´ Moya Lebensmittelwissenschaft und Institut Cavanilles de Biodiversitat i Biotechnologie Biolog´ıa Evolutiva Fachgebiet Universitat de Valencia` Lebensmittelmikrobiologie (150a) Spain Universitat¨ Hohenheim Garbenstrasse 28 Staffan Normark 70599 Stuttgart Swedish Institute for Infectious Germany Disease Control and Department of Microbiology Wolfgang Witte Tumor and Cell Biology Robert Koch Institute Karolinska Institutet Wernigerode Branch Solna Burgstraße 37 Sweden 38855 Wernigerode Germany