THE Fecal Bacteria This page intentionally left blank THE Fecal Bacteria Edited by Michael J. Sadowsky Department of Soil, Water, and Climate and BioTechnology Institute, University of Minnesota, St. Paul, Minnesota Richard L. Whitman Lake Michigan Ecological Research Station, Great Lakes Science Center, U.S. Geological Survey, Porter, Indiana Washington, DC 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 © 2011 ASM Press American Society for Microbiology 1752 N St. NW Washington, DC 20036-2904 Library of Congress Cataloging-in-Publication Data The fecal bacteria / edited by Michael J. Sadowsky, Richard L. Whitman. p. ; cm. Includes bibliographical references and index. ISBN 978-1-55581-608-7 (hardcover : alk. paper) 1. Enterobacteriaceae. I. Sadowsky, M. J. (Michael J.) II. Whitman, Richard Lincoln. [DNLM: 1. Enterobacteriaceae. 2. Environmental Monitoring—methods. 3. Feces—microbiology. 4. Fresh Water—analysis. QW 138] QR82.E6F43 2011 579.3'4—dc22 2010029320 Current printing (last digit) 10 9 8 7 6 5 4 3 2 1 All Rights Reserved Printed in the United States of America Cover illustration: Interaction of Salmonella enterica serovar Typhimurium with mouse intestinal tissue. Bacteria are green, and mouse intestine epithelial tissue is blue and red. (Photo courtesy of Bärbel Stecher and Wolf-Dietrich Hardt, ETH Zürich, Switzerland.) CONTENTS Contributors vii Preface ix 1. The Fecal Environment, the Gut / 1 Denis O. Krause and Ehsan Khafipour 2. Taxonomy, Phylogeny, and Physiology of Fecal Indicator Bacteria / 23 Militza Carrero-Colón, Gene S. Wickham, and Ronald F. Turco 3. The Gut Microbiota: Ecology and Function / 39 Benjamin P. Willing and Janet K. Jansson 4. Animals and Humans as Sources of Fecal Indicator Bacteria / 67 Christopher K. Yost, Moussa S. Diarra, and Edward Topp 5. Environmental Sources of Fecal Bacteria / 93 Muruleedhara N. Byappanahalli and Satoshi Ishii 6. Physical and Biological Factors Influencing Environmental Sources of Fecal Indicator Bacteria in Surface Water / 111 Richard L. Whitman, Meredith B. Nevers, Katarzyna Przybyla-Kelly, and Muruleedhara N. Byappanahalli 7. Impacts of Fecal Bacteria on Human and Animal Health—Pathogens and Virulence Genes / 135 Timothy J. Johnson 8. Modeling Fate and Transport of Fecal Bacteria in Surface Water / 165 Meredith B. Nevers and Alexandria B. Boehm v vi CONTENTS 9. Microbial Source Tracking / 189 Valerie J. Harwood, Hodon Ryu, and Jorge Santo Domingo 10. Prevalence and Fate of Gut-Associated Human Pathogens in the Environment / 217 Katherine G. McElhany and Suresh D. Pillai 11. Classical and Molecular Methods To Measure Fecal Bacteria / 241 Thomas A. Edge and Alexandria B. Boehm 12. Fecal Bacteria and Foods / 275 Francisco Diez-Gonzalez 13. Conclusions and Future Use of Fecal Indicator Bacteria for Monitoring Water Quality and Protecting Human Health / 295 Michael J. Sadowsky and Richard L. Whitman Index / 303 CONTRIBUTORS Alexandria B. Boehm Environmental and Water Studies, Department of Civil & Environmental Engineering, Jerry Yang & Akiko Yamazaki Environment & Energy Building, Stanford, CA 94305 Muruleedhara N. Byappanahalli U.S. Geological Survey, Great Lakes Science Center, Lake Michigan Ecological Research Station, Porter, IN 46304 Militza Carrero-Colón Department of Agronomy, Purdue University, West Lafayette, IN 47907 Moussa S. Diarra Pacific Agri-Food Research Centre, Agriculture and Agri-Food Canada, Agassiz, BC, Canada V0M 1A0 Francisco Diez-Gonzalez Department of Food Science and Nutrition, University of Minnesota, St. Paul, MN 55108 Thomas A. Edge Water Science & Technology Directorate, National Water Research Institute, Environment Canada, Burlington, ON, Canada L7R 4A6 Valerie J. Harwood Department of Integrative Biology, University of South Florida, Tampa, FL 33620 Satoshi Ishii Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, University of Tokyo, Tokyo, 113-8657, Japan Janet K. Jansson Department of Ecology, Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720 Timothy J. Johnson Department of Veterinary and Biomedical Sciences, University of Minnesota, St. Paul, MN 55108 vii viii CONTRIBUTORS Ehsan Khafipour Department of Animal Science, University of Manitoba, Winnipeg, MB, Canada R3T 2N2 Denis O. Krause Department of Animal Science and Department of Medical Microbiology, University of Manitoba, Winnipeg, MB, Canada R3T 2N2 Katherine G. McElhany Food Safety & Environmental Microbiology Program, Texas A&M University, College Station, TX 77843 Meredith B. Nevers U.S. Geological Survey, Great Lakes Science Center, Lake Michigan Ecological Research Station, Porter, IN 46304 Suresh D. Pillai Food Safety & Environmental Microbiology Program, Texas A&M University, College Station, TX 77843 Katarzyna Przybyla-Kelly U.S. Geological Survey, Great Lakes Science Center, Lake Michigan Ecological Research Station, Porter, IN 46304 Hodon Ryu ORD/NRMRL/WSWRD/MCCB U.S. Environmental Protection Agency, Cincinnati, OH 45268 Michael J. Sadowsky BioTechnology Institute and Department of Soil, Water, and Climate, University of Minnesota, St. Paul, MN 55108 Jorge Santo Domingo ORD/NRMRL/WSWRD/MCCB U.S. Environmental Protection Agency, Cincinnati, OH 45268 Edward Topp Agriculture and Agri-Food Canada, London, ON, Canada N5V 4T3 Ronald F. Turco Laboratory for Soil Microbiology, Department of Agronomy, Purdue University, West Lafayette, IN 47907 Richard L. Whitman U.S. Geological Survey, Great Lakes Science Center, Lake Michigan Ecological Research Station, Porter, IN 46304 Gene S. Wickham The Center for Environmental Biotechnology, University of Tennessee, Knoxville, TN 37996 Benjamin P. Willing Michael Smith Laboratories, University of British Columbia, Vancouver, BC, Canada V6T 1Z4 Christopher K. Yost Department of Biology, University of Regina, Regina, SK, Canada S4S 0A2 PREFACE Although often maligned, the fecal indicator bacteria, commonly found in the gastrointestinal tract of humans and warm-blooded animals, represent a broad group of enteric bacteria that have had much utility over the last 40 years as a means to assess water quality and food safety. These bacteria serve as the focal point of “the fecal indicator concept,” used worldwide to monitor water quality and protect people from swimming- and water-related illnesses. The fecal indicator concept stems, in part, from the pioneering work of Von Fritsch and Escherich who, in the 1800s, made the logical connections between the presence of Klebsiella pneumoniae and K. rhinoscleromatis and sewage contami- nation and the use of Bacillus coli (subsequently renamed Escherichia coli) as an indicator of fecal pollution. Their work eventually led to the development of the indicator bacterial paradigm as a means to assess microbial aspects of water quality, and the concept was promulgated by the U.S. Public Health Service in their 1914 standards for drinking water that were based on total coliforms. The regulations were based, in large part, on the belief that if these organisms were present in water there was a likelihood that human pathogens would also be present and that microorganisms causing diseases in humans were more likely to originate from human sources (e.g., human feces) than from other animals. Over the years, however, the fecal indicator concept has moved away from use of this complex and large group of organisms, collectively referred to as the coliform bacteria, many of which are members of the family Enterobacteriaceae, to reliance on measurements of E. coli and noncoliform bacteria such as enterococci. These bacteria are better related, based on epidemiological studies, to health risks associated with swimming and recreational activities in fresh and marine waters. It is important to note, however, that the fecal indicator bacteria represent just a small portion of the total fecal bacteria present in the gastrointestinal tracts ix