Bacteriophages in the Control of Food- and Waterborne Pathogens E D I T E D B Y Parviz M. Sabour Guelph Food Research Centre, Research Branch Agriculture & Agri-Food Canada Guelph, Ontario, Canada Mansel MI. Griffiths Canadian Research Institute for Food Safity Department of Food Science University of Guelph Guelph, Ontario, Canada ASM PRESS W A S H I N G T O N , D C Cover image: Ed Atkeson, Berg Design Copyright(cid:2) 2010 ASM Press American Society for Microbiology 1752 N St., N.W. Washington, DC 20036-2904 Library of Congress Cataloging-in-Publication Data Bacteriophages in the control of food- and waterborne pathogens / edited by Parviz M. Sabour and Mansel W. Griffiths. p. ; cm. Includes bibliographical references and index. ISBN-13: 978-1-55581-502-8 (hardcover : alk. paper) ISBN-10: 1-55581-502-2 (hardcover : alk. paper) 1. Bacteriophages—Therapeutic use. 2. Bacteriophages—Diagnostic use. 3. Food contamination. 4. Water—Pollution. I. Sabour, Parviz M. II. Griffiths, Mansel. III. American Society for Microbiology. [DNLM: 1. Bacteriophages. 2. Food Contamination—prevention & control. 3. Food Microbiology. 4. Water Microbiology. QW 161 B1318 2010] QR342.B3385 2010 579.2(cid:2)6—dc22 2010014688 10 9 8 7 6 5 4 3 2 1 All Rights Reserved Printed in the United States of America Address editorial correspondence to ASM Press, 1752 N St., N.W., 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: http://estore.asm.org CONTENTS Contributors vii Foreword Elizabeth Kutter xi Preface xv Acknowledgments xvii 1. Implications of Antimicrobial Agents as Therapeutics and Growth Promoters in Food Animal Production Patrick Boerlin 1 2. Introduction to Bacteriophage Biology and Diversity Pieter-Jan Ceyssens and Rob Lavigne 11 3. Phage-Based Methods for the Detection of Bacterial Pathogens Mansel W. Griffiths 31 4. Application of Bacteriophages To Control Pathogens in Food Animal Production Lawrence D. Goodridge 61 5. Bacteriophages for Control of Phytopathogens in Food Production Systems Antonet M. Svircev, Alan J. Castle, and Susan M. Lehman 79 6. Potential Use of Bacteriophages as Indicators of Water Quality and Wastewater Treatment Processes Francisco Lucena and Juan Jofre 103 v (cid:3) vi CONTENTS 7. Application of Bacteriophages To Control Pathogenic and Spoilage Bacteria in Food Processing and Distribution J. Andrew Hudson, Lynn McIntyre, and Craig Billington 119 8. Bacteriophage Lytic Enzymes as Antimicrobials Caren J. Stark, Richard P. Bonocora, James T. Hoopes, and Daniel C. Nelson 137 9. Lysogenic Conversion in Bacteria of Importance to the Food Industry Marcin Ło´s, John Kuzio, Michael R. McConnell, Andrew M. Kropinski, Grzegorz We˛grzyn, and Gail E. Christie 157 10. Bacteriophages in Industrial Food Processing: Incidence and Control in Industrial Fermentation Simon Labrie and Sylvain Moineau 199 11. Practical and Theoretical Considerations for the Use of Bacteriophages in Food Systems Jason J. Gill 217 12. Encapsulation and Controlled Release of Bacteriophages for Food Animal Production Qi Wang and Parviz M. Sabour 237 13. Application of Bacteriophages for Control of Infectious Diseases in Aquaculture Toshihiro Nakai 257 14. Control of Bacterial Diarrhea with Phages: Coverage and Safety Issues in Bacteriophage Therapy Harald Bru¨ssow 273 15. Industrial and Regulatory Issues in Bacteriophage Applications in Food Production and Processing Alexander Sulakvelidze and Gary R. Pasternack 297 Index 327 CONTRIBUTORS Craig Billington Food Safety Programme Institute of Environmental Science and Research Ltd. Christchurch 8540, New Zealand Patrick Boerlin Department of Pathobiology Ontario Veterinary College University of Guelph Guelph, Ontario N1G 2W1, Canada Richard P. Bonocora Laboratory of Molecular and Cellular Biology National Institute of Diabetes and Digestive and Kidney Diseases National Institutes of Health Bethesda, MD 20892 Harald Bru¨ssow Nutrition and Health Department Nestle´ Research Center Vers-chez-les-Blanc CH-1000 Lausanne 26, Switzerland Alan J. Castle Department of Biological Sciences Brock University 500 Glenridge Avenue St. Catharines, Ontario L2S 3A1, Canada Pieter-Jan Ceyssens Department of Biosystems Division of Gene Technology Kasteelpark Arenberg 21 bus 2462 B-3001 Leuven, Belgium vii (cid:3) viii CONTRIBUTORS Gail E. Christie Department of Microbiology & Immunology Virginia Commonwealth University P.O. Box 980678, 1101 East Marshall Street, 6-034 Sanger Hall Richmond, VA 23298-0678 Jason J. Gill Department of Biochemistry and Biophysics and Center for Phage Technology Texas A&M University 2128 TAMU College Station, TX 77843 Lawrence D. Goodridge Department of Animal Sciences Center for Meat Safety and Quality Colorado State University Fort Collins, CO 80523 Mansel W. Griffiths Department of Food Science and Canadian Research Institute for Food Safety University of Guelph 43 McGilvray Street Guelph, Ontario N1G 2W1, Canada James T. Hoopes Center for Advanced Research in Biotechnology University of Maryland Biotechnology Institute Rockville, MD 20850 J. Andrew Hudson Food Safety Programme Institute of Environmental Science and Research Ltd. Christchurch 8540, New Zealand Juan Jofre Department of Microbiology Faculty of Biology University of Barcelona Avinguda Diagonal 645 08028 Barcelona, Spain Andrew M. Kropinski Laboratory for Foodborne Zoonoses Public Health Agency of Canada 110 Stone Road West Guelph, Ontario N1G 3W4, Canada John Kuzio Department of Microbiology and Immunology Queen’s University Kingston, Ontario K7L 3N6, Canada (cid:3) CONTRIBUTORS ix Simon Labrie De´partementde biochimie et de microbiologie Faculte´ des sciences et de ge´nie Groupe de recherche en e´cologiebuccale Faculte´ de me´decinedentaire Fe´lix d’He´relle Reference Center for Bacterial Viruses Universite´ Laval Que´becCity, Que´becG1V 0A6, Canada Rob Lavigne Department of Biosystems Division of Gene Technology Kasteelpark Arenberg 21 bus 2462 B-3001 Leuven, Belgium Susan M. Lehman Centers for Disease Control and Prevention 1600 Clifton Road NE, Mail Stop C-16 Atlanta, GA 30333 Marcin Łos´ Department of Molecular Biology University of Gdansk Kladki 24 80-822 Gdansk, Poland Francisco Lucena Department of Microbiology Faculty of Biology University of Barcelona Avinguda Diagonal 645 08028 Barcelona, Spain Lynn McIntyre Food Safety Programme Institute of Environmental Science and Research Ltd. Christchurch 8540, New Zealand Michael R. McConnell Department of Biology Point Loma Nazarene University 3900 Lomaland Drive San Diego, CA 92106 Sylvain Moineau De´partementde biochimie et de microbiologie Faculte´ des sciences et de ge´nie Groupe de recherche en e´cologiebuccale Faculte´ de me´decinedentaire Fe´lix d’He´relle Reference Center for Bacterial Viruses Universite´ Laval Que´becCity, Que´becG1V 0A6, Canada Toshihiro Nakai Laboratory of Fish Pathology Graduate School of Biosphere Sciences Hiroshima University Higashi-Hiroshima 739-8528, Japan (cid:3) x CONTRIBUTORS Daniel C. Nelson Center for Advanced Research in Biotechnology University of Maryland Biotechnology Institute Rockville, MD 20850 Gary R. Pasternack Intralytix, Inc. The Columbus Centre 701 East Pratt Street Baltimore, MD 21202 Parviz M. Sabour Guelph Food Research Centre Research Branch Agriculture and Agri-Food Canada 93 Stone Road West Guelph, Ontario N1G 5C9, Canada Caren J. Stark Center for Advanced Research in Biotechnology University of Maryland Biotechnology Institute Rockville, MD 20850 Alexander Sulakvelidze Intralytix, Inc. The Columbus Centre 701 East Pratt Street Baltimore, MD 21202 Antonet M. Svircev Research Branch Agriculture and Agri-Food Canada 4902 Victoria Avenue North, P.O. Box 6000 Vineland Station, Ontario L0R 2E0, Canada Qi Wang Guelph Food Research Centre Research Branch Agriculture and Agri-Food Canada 93 Stone Road West Guelph, Ontario N1G 5C9, Canada Grzegorz We˛grzyn Department of Molecular Biology University of Gdansk Kladki 24 80-822 Gdansk, Poland FOREWORD This very timely book effectively addresses a number of important issues: he growing concerns about food safety in light of widespread outbreaks of pathogens such as Salmonella and Escherichia coli, leading to massive food recalls; the rise in resistance to current antimicrobials, exacerbated by their extensive use in agriculture; the challenges of quickly and specifically identi- fying pathogenic bacterial strains; and the frustrations of phage invasion of food-fermentation vats. As antibiotic resistance becomes more widespread, it makes sense to aggressively explorethetherapeuticpotentialofphages,taking advantage of modern biological tools to select the most effective, characterize them thoroughly under relevant physiological conditions, and carryoutwell- controlled studies. Gaining research funding and approval for human therapy implementation has proven very challenging in the Western world for a va- riety of regulatory and financial reasons. As a result, many of those drawn to such work have decided to focus atpresentonnonmedicalapplicationsinless regulated key areas such as agriculture and food safety, thus dealing with significant parts of the problem while collecting relevant phage experience and developing expertise at commercialization. The most significant recent advances toward phage therapy are in fact re- lated to food safety, as discussed in several chapters of this new ASM book. A major milestone was the 2006 FDA approval of an Intralytix, Inc. cocktail of phages targeting Listeria monocytogenes for use on ready-to-eat meats and cheeses, including the right to substitute related well-characterizedphagesfor those in the cocktail as initially approved—a crucial factor for many phage applications. In this context chapter 15, by Alexander Sulakvelidze and Gary R. Pasternack of Intralytix, on industrial and regulatory issues related to bac- teriophageapplicationsinfoodproductionandprocessingisparticularlyuseful, complementing chapter 7, by the New Zealand team of J. Andrew Hudson et al., on phagecontrol ofpathogenicandspoilagebacteriainfoodprocessing and distribution. xi (cid:3) xii FOREWORD Muchinterestingandproductiveworkisalreadyunderway.AUtahphage company, OmniLytics, Inc., has won permission to market phage treatments for such applications as managing plant pathogens and preslaughter reduction ofE.coliO157levelsincattle,withclearofficialrecognitionthatthisapproach isfarlesspotentiallyhazardousthanstandardchemicalmethods.BoththeU.S. military and the U.S. Department of Agriculture are supporting sophisticated pathogen detection and food safety work. The research cluster of the Guelph Food Research Centre, the University of Guelph and its Canadian Research InstituteforFoodSafety,andthePublicHealthAgencyofCanada,alllocated in Guelph, Ontario, are deeply committed to exploring and applying phage approaches for livestock, crops, and food safety, along with providing badly needed underpinnings in basic research. Significant initiatives are also under way in Australia, New Zealand, Great Britain, Japan, and other countries. Bacteriophages in the Control of Food- and Waterborne Pathogens doesanexcellent job of bringing the resultant academic, governmental, and corporate work togetherforthefirsttime.Itcanbeexpectedtohelpspearheadfutureresearch and increasingly rapid progress in this new field, with many possibilities for new applications and patents. (It should be noted here thattheveryextensive phage research in Eastern Europewas sodeeplycommittedtohumantherapy that little agricultural or water quality work was carried out there until very recently; the same was true of the work going on in the West over the first half of the last century.) Historically,thefirst-everASMmonograph(Mathewsetal.,1983)focused on a phage—bacteriophage T4, the primary tool in the development of the field of molecular biology. There were detailed discussions of T4’s structure and initiation of infection; of the enzymes of DNA metabolism that it en- coded; of the processes of DNA replication, recombination, and repair; of RNA polymerase modifications and the regulation of the various classes of genes; and of the processes of head, tail, and tail fiber morphogenesis. It also included a restriction map of the whole T4 genome and details of the 133 T4 genes known to date. The next ASM phage book (Karam, 1994) again focused on T4. It elaborated much further on molecular aspects of the infec- tion process and included the first analysis of the complete T4 genomic se- quence, a two-dimensional protein gel portrayal of the pattern of synthesis of T4 early proteins, and a chapter on the effects of host physiology on the infection process. It also included a very extensive section on methods of working with phage—the first such compendium since the classic book Bac- teriophages by Adams (1959). That book, still used worldwide, was based on the Cold Spring Harbor phage courses of the 1940s and 1950s, and was en- riched by the phage meetings there (as were the Cold Spring Harbor Labo- ratory volumes on phages lambda [e.g., Hendrix et al., 1983]and muand the RNA phages). BothASMT4booksgrewoutoftheEvergreenInternationalT4Meetings, with competing research labs often collaborating on the chapters, reflecting the strong collegiality of the phage community that has been so important to the field since the 1940s. The 1994 book had an amazing 105 contributors from around the world but not a single mention of phage applications. At that time the West was just beginning to be aware of the ongoing Soviet