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NOTICE: The workshop that is the subject of this workshop summary was approved by the Governing Board of the National Research Council, whose members are drawn from the councils of the National Academy of Sciences, the National Academy of Engineering, and the Institute of Medicine.
Financial support for this activity was provided by the U.S. Department of Health and Human Services: National Institutes of Health, National Institute of Allergy and Infectious Diseases, Centers for Disease Control and Prevention, Food and Drug Administration, and the Fogarty International Center; U.S. Department of Defense: Armed Forces Health Surveillance Center, Defense Threat Reduction Agency, and Medical Research and Materiel Command; U.S. Department of Justice: Federal Bureau of Investigation; U.S. Department of Veterans Affairs; U.S. Department of Homeland Security; U.S. Agency for International Development; Uniformed Services University of the Health Sciences; Alfred P. Sloan Foundation; American Society for Microbiology; Burroughs Wellcome Fund; GlaxoSmithKline; Infectious Diseases Society of America; Johnson & Johnson; Merck Company Foundation; and sanofi pasteur. The views presented in this publication do not necessarily reflect the views of the organizations or agencies that provided support for this activity.
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Cover images: (Front, upper) Medical illustration of methicillin-resistant Staphylococcus aureus (MRSA); (Front, lower) Medical Illustration of Clostridium difficile; (Back) Medical illustration of Streptococcus pneumoniae. Photo Credits: All photos courtesy of the Centers for Disease Control and Prevention, www.cdc.gov.
Suggested citation: IOM (Institute of Medicine). 2014. Microbial ecology in states of health and disease: Workshop summary. Washington, DC: The National Academies Press.
THE NATIONAL ACADEMIES
Advisers to the Nation on Science, Engineering, and Medicine
The National Academy of Sciences is a private, nonprofit, self-perpetuating society of distinguished scholars engaged in scientific and engineering research, dedicated to the furtherance of science and technology and to their use for the general welfare. Upon the authority of the charter granted to it by the Congress in 1863, the Academy has a mandate that requires it to advise the federal government on scientific and technical matters. Dr. Ralph J. Cicerone is president of the National Academy of Sciences.
The National Academy of Engineering was established in 1964, under the charter of the National Academy of Sciences, as a parallel organization of outstanding engineers. It is autonomous in its administration and in the selection of its members, sharing with the National Academy of Sciences the responsibility for advising the federal government. The National Academy of Engineering also sponsors engineering programs aimed at meeting national needs, encourages education and research, and recognizes the superior achievements of engineers. Dr. C. D. Mote, Jr., is president of the National Academy of Engineering.
The Institute of Medicine was established in 1970 by the National Academy of Sciences to secure the services of eminent members of appropriate professions in the examination of policy matters pertaining to the health of the public. The Institute acts under the responsibility given to the National Academy of Sciences by its congressional charter to be an adviser to the federal government and, upon its own initiative, to identify issues of medical care, research, and education. Dr. Harvey V. Fineberg is president of the Institute of Medicine.
The National Research Council was organized by the National Academy of Sciences in 1916 to associate the broad community of science and technology with the Academy’s purposes of furthering knowledge and advising the federal government. Functioning in accordance with general policies determined by the Academy, the Council has become the principal operating agency of both the National Academy of Sciences and the National Academy of Engineering in providing services to the government, the public, and the scientific and engineering communities. The Council is administered jointly by both Academies and the Institute of Medicine. Dr. Ralph J. Cicerone and Dr. C. D. Mote, Jr., are chair and vice chair, respectively, of the National Research Council.
PLANNING COMMITTEE FOR A WORKSHOP ON MICROBIAL ECOLOGY IN STATES OF HEALTH AND DISEASE1
ARTURO CASADEVALL, Albert Einstein College of Medicine, Bronx, New York
EDUARDO GOTUZZO, Instituto de Medicina Tropical–Alexander von Humboldt, Universidad Peruaña Cayetano Heredia, Lima, Peru
JO HANDELSMAN, Yale University, New Haven, Connecticut
JAMES M. HUGHES, Emory University, Atlanta, Georgia
DAVID A. RELMAN, Stanford University and Veterans Affairs Palo Alto Health Care System, Palo Alto, California
P. FREDERICK SPARLING, University of North Carolina, Chapel Hill, North Carolina
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1 Institute of Medicine planning committees are solely responsible for organizing the workshop, identifying topics, and choosing speakers. The responsibility for the published workshop summary rests solely with the workshop rapporteurs and the institution.
FORUM ON MICROBIAL THREATS1
DAVID A. RELMAN (Chair), Stanford University, and Veterans Affairs Palo Alto Health Care System, Palo Alto, California
JAMES M. HUGHES (Vice-Chair), Global Infectious Diseases Program, Emory University, Atlanta, Georgia
LONNIE J. KING (Vice-Chair), Ohio State University, Columbus, Ohio
KEVIN ANDERSON, Biological and Chemical Defense Division, Science and Technology Directorate, Department of Homeland Security, Washington, DC
ENRIQUETA C. BOND, Burroughs Wellcome Fund (Emeritus), QE Philanthropic Advisors, Marshall, Virginia
ROGER G. BREEZE, Lawrence Livermore National Laboratory, Livermore, California
JOHN E. BURRIS,2 Burroughs Wellcome Fund, Research Triangle Park, North Carolina
ARTURO CASADEVALL, Albert Einstein College of Medicine, Yeshiva University, Bronx, New York
ANDREW CLEMENTS, U.S. Agency for International Development, Washington, DC
PETER DASZAK, EcoHealth Alliance, New York, New York
JEFFREY S. DUCHIN, Public Health–Seattle and King County, Seattle, Washington
JONATHAN EISEN, Genome Center, University of California, Davis, California
RALPH L. ERICKSON,3 Walter Reed Army Institute of Research, Silver Spring, Maryland
MARK B. FEINBERG, Merck Vaccine Division, Merck & Co., Inc., West Point, Pennsylvania
JACQUELINE FLETCHER, Oklahoma State University, Stillwater, Oklahoma
CLAIRE FRASER, Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, Maryland
JESSE L. GOODMAN, Food and Drug Administration, Rockville, Maryland
EDUARDO GOTUZZO, Instituto de Medicina Tropical–Alexander von Humboldt, Universidad Peruaña Cayetano Heredia, Lima, Peru
CAROLE A. HEILMAN, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland
DAVID L. HEYMANN, Public Health England, London, United Kingdom
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1 Institute of Medicine forums and roundtables do not issue, review, or approve individual documents. The responsibility for the published workshop summary rests with the workshop rapporteurs and the institution.
2 Forum member until October 18, 2013.
3 Forum member until June 30, 2013.
ZHI HONG,4 GlaxoSmithKline, Research Triangle Park, North Carolina
PHILIP HOSBACH, sanofi pasteur, Swiftwater, Pennsylvania
STEPHEN ALBERT JOHNSTON, Arizona BioDesign Institute, Arizona State University, Tempe, Arizona
KENT KESTER,5 Uniformed Services University of the Health Sciences, Bethesda, Maryland
GERALD T. KEUSCH, Boston University School of Medicine and Boston University School of Public Health, Boston, Massachusetts
RIMA F. KHABBAZ, Centers for Disease Control and Prevention, Atlanta, Georgia
MARK KORTEPETER,6 Uniformed Services University of the Health Sciences, Bethesda, Maryland
STANLEY M. LEMON, University of North Carolina, Chapel Hill, North Carolina
MARGARET J. McFALL-NGAI, University of Wisconsin, Madison, Wisconsin
EDWARD McSWEEGAN, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland
PAULA J. OLSIEWSKI, Alfred P. Sloan Foundation, New York, New York
JULIE PAVLIN, Armed Forces Health Surveillance Center, Silver Spring, Maryland
GEORGE POSTE, Complex Adaptive Systems Initiative, Arizona State University, SkySong, Scottsdale, Arizona
DAVID RIZZO, University of California, Davis, California
GARY A. ROSELLE, Veterans Health Administration, Department of Veterans Affairs, Cincinnati, Ohio
KEVIN RUSSELL, Armed Forces Health Surveillance Center, Silver Spring, Maryland
JANET SHOEMAKER, American Society for Microbiology, Washington, DC
JAY P. SIEGEL,7 Johnson & Johnson, Radnor, Pennsylvania
P. FREDERICK SPARLING, University of North Carolina, Chapel Hill, North Carolina
MARY E. WILSON, Harvard School of Public Health, Harvard University, Boston, Massachusetts
EDWARD H. YOU,8 Federal Bureau of Investigation, Washington, DC
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4 Forum member until October 18, 2013.
5 Retired as of December 31, 2013.
6 Forum member since January 15, 2014.
7 Forum member since January 15, 2014.
8 Forum member since July 1, 2013.
IOM Staff
EILEEN CHOFFNES, Scholar and Director
LEIGHANNE OLSEN,9 Program Officer
KATHERINE McCLURE, Associate Program Officer
REBEKAH HUTTON, Research Associate
CHARLEE ALEXANDER,10 Senior Program Assistant
JOANNA ROBERTS,11 Senior Program Assistant (Temp)
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9 Staff member until August 15, 2013.
10 Staff member from April 1 to November 15, 2013.
11 Staff member since November 1, 2013.
BOARD ON GLOBAL HEALTH1
THOMAS C. QUINN (Chair), Associate Director for International Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Professor of Medicine, International Health, Epidemiology, and Molecular Biology and Immunology, Johns Hopkins University School of Medicine, Baltimore, Maryland
JO IVEY BOUFFORD (IOM Foreign Secretary), President, New York Academy of Medicine, New York
CLAIRE V. BROOME, Adjunct Professor, Division of Global Health, Rollins School of Public Health, Emory University, Atlanta, Georgia
JACQUELYN C. CAMPBELL, Anna D. Wolf Chair, and Professor, Johns Hopkins University School of Nursing, Baltimore, Maryland
THOMAS J. COATES, Michael and Sue Steinberg Professor of Global AIDS, Research Co-Director, UC Global Health Institute, David Geffen School of Medicine, University of California, Los Angeles, California
GARY DARMSTADT, Director, Family Health Division, Global Health Program, Bill & Melinda Gates Foundation, Seattle, Washington
VALENTIN FUSTER, Director, Wiener Cardiovascular Institute, Kravis Cardiovascular Health Center, Professor of Cardiology, Mount Sinai School of Medicine, Mount Sinai Medical Center, New York, New York
JACOB A. GAYLE, Vice President, Community Affairs, Executive Director, Medtronic Foundation, Minneapolis, Minnesota
GLENDA E. GRAY, Executive Director, Perinatal HIV Research Unit, Chris Hani Baragwanath Hospital, University of the Witwatersrand, Diepkloof, South Africa
STEPHEN W. HARGARTEN, Associate Dean, Global Health Program, Medical College of Wisconsin, Milwaukee, Wisconsin
PETER J. HOTEZ, Professor of Pediatrics and Molecular Virology and Microbiology, Texas Children’s Hospital Endowed Chair of Tropical Pediatrics, President, Sabin Vaccine Institute and Texas Children’s Center for Vaccine Development, Dean, National School of Tropical Medicine, Baylor College of Medicine, Houston, Texas
CLARION JOHNSON, Consultant, Exxon Mobil, Fairfax, Virginia
FITZHUGH MULLAN, Professor, Department of Health Policy, The George Washington University, Washington, DC
OLUFUNMILAYO F. OLOPADE, Walter L. Palmer Distinguished Service Professor of Medicine, The University of Chicago, Chicago, Illinois
________________
1 Institute of Medicine boards do not review or approve individual workshop summaries. The responsibility for the content of the workshop summary rests with the workshop rapporteurs and the institution.
Reviewers
This workshop summary has been reviewed in draft form by individuals chosen for their diverse perspectives and technical expertise, in accordance with procedures approved by the National Research Council’s Report Review Committee. The purpose of this independent review is to provide candid and critical comments that will assist the institution in making its published workshop summary as sound as possible and to ensure that the workshop summary meets institutional standards for objectivity, evidence, and responsiveness to the study charge. The review comments and draft manuscript remain confidential to protect the integrity of the process. We wish to thank the following individuals for their review of this workshop summary:
Jeffrey L. Dangl, University of North Carolina, Chapel Hill, North Carolina
Maria Dominguez-Bello, New York University Langone Medical Center, New York, New York
Jesse L. Goodman, Food and Drug Administration, Rockville, Maryland
Margaret J. McFall-Ngai, University of Wisconsin, Madison, Wisconsin
Although the reviewers listed above have provided many constructive comments and suggestions, they did not see the final draft of the workshop summary before its release. The review of this workshop summary was overseen by Melvin Worth. Appointed by the Institute of Medicine, he was responsible for making certain that an independent examination of this workshop summary was carried out in accordance with institutional procedures and that all review comments were carefully considered. Responsibility for the final content of this workshop summary rests entirely with the rapporteurs and the institution.
Acknowledgments
The Forum on Emerging Infections was created by the Institute of Medicine (IOM) in 1996 in response to a request from the Centers for Disease Control and Prevention (CDC) and the National Institutes of Health (NIH). The purpose of the Forum is to provide structured opportunities for leaders from government, academia, and industry to regularly meet and examine issues of shared concern regarding research, prevention, detection, and management of emerging, reemerging, and novel infectious diseases in humans, plants, and animals. In pursuing this task, the Forum provides a venue to foster the exchange of information and ideas, identify areas in need of greater attention, clarify policy issues by enhancing knowledge and identifying points of agreement, and inform decision makers about science and policy issues. The Forum seeks to illuminate issues rather than resolve them. For this reason, it does not provide advice or recommendations on any specific policy initiative pending before any agency or organization. Its value derives instead from the diversity of its membership and from the contributions that individual members make throughout the activities of the Forum. In September 2003, the Forum changed its name to the Forum on Microbial Threats.
The Forum on Microbial Threats and the IOM wish to express their warmest appreciation to the individuals and organizations who gave their valuable time to provide information and advice to the Forum through their participation in the planning and execution of this workshop. A full list of presenters, and their biographical information, may be found in Appendixes B and E, respectively.
The forum gratefully acknowledges the contributions of the members of the planning committee1: Arturo Casadevall (Albert Einstein College of Medicine),
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1 Institute of Medicine planning committees are solely responsible for organizing the workshop, identifying topics, and choosing speakers. The responsibility for the published workshop summary rests solely with the workshop rapporteurs and the institution.
Eduardo Gotuzzo (Universidad Peruaña Cayetano Heredia), Jo Handelsman (Yale University), James M. Hughes (Emory University), David A. Relman (Stanford University), and P. Frederick Sparling (University of North Carolina, Chapel Hill).
The Forum is also indebted to the IOM staff who tirelessly contributed throughout the planning and execution of the workshop and the production of this workshop summary report. On behalf of the Forum, we gratefully acknowledge these efforts led by Dr. Eileen Choffnes, Scholar and Director of the Forum; Dr. LeighAnne Olsen,2 Program Officer; Katherine McClure, Associate Program Officer; Rebekah Hutton, Research Associate; and Charlee Alexander,3 Senior Program Assistant for dedicating much effort and time to developing this workshop’s agenda and for their thoughtful and insightful approach and skill in planning for the workshop and in translating the workshop’s proceedings and discussion into this workshop summary report. We would also like to thank the following IOM staff and consultants for their valuable contributions to this activity: Daniel Bethea, Laura Harbold DeStefano, Chelsea Frakes, Alison Mack, Erika Vijh, and Julie Wiltshire.
Finally, the Forum wishes to recognize the sponsors that supported this activity. Financial support for this project was provided by the U.S. Department of Health and Human Services: National Institutes of Health, National Institute of Allergy and Infectious Diseases, Centers for Disease Control and Prevention, Food and Drug Administration, and the Fogarty International Center; U.S. Department of Defense: Armed Forces Health Surveillance Center, Defense Threat Reduction Agency, and Medical Research and Materiel Command; U.S. Department of Justice: Federal Bureau of Investigation; U.S. Department of Veterans Affairs; U.S. Department of Homeland Security; U.S. Agency for International Development; Uniformed Services University of the Health Sciences; Alfred P. Sloan Foundation; American Society for Microbiology; Burroughs Wellcome Fund;4 GlaxoSmithKline;5 Infectious Diseases Society of America; Johnson & Johnson; Merck Company Foundation; and sanofi pasteur. The views presented in this workshop summary are those of the workshop participants and have been summarized by the rapporteurs. They do not necessarily reflect the views of the Forum on Microbial Threats, its sponsors, or the IOM.
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2 Staff member until August 15, 2013.
3 Staff member from April 1 to November 15, 2013.
4 Sponsor until October 18, 2013.
5 Sponsor until October 18, 2013.
Contents
A1 Effector and Memory T Cell Responses to Commensal Bacteria
Yasmine Belkaid, Nicolas Bouladoux, and Timothy W. Hand
A2 What Are the Consequences of the Disappearing Human Microbiota?
Martin J. Blaser and Stanley Falkow
A3 Pathways in Microbe-Induced Obesity
Laura M. Cox and Martin J. Blaser
A4 Microbial Exposure During Early Life Has Persistent Effects on Natural Killer T Cell Function
Torsten Olszak, Dingding An, Sebastian Zeissig, Miguel Penilla Vera, Julia Richter, Andre Franke, Jonathan N. Glickman, Reiner Siebert, Rebecca M. Barron, Dennis L. Kasper, and Richard S. Blumberg
A5 The Application of Ecological Theory Toward an Understanding of the Human Microbiome
Elizabeth K. Costello, Keaton Stagaman, Les Dethlefsen, Brendan J. M. Bohannan, and David A. Relman
A6 Seasonal Restructuring of the Ground Squirrel Gut Microbiota Over the Annual Hibernation Cycle
Hannah V. Carey, William A. Walters, and Rob Knight
A7 Lessons from Studying Insect Symbioses
A8 A New Vision of Immunity: Homeostasis of the Superorganism
A9 Host Defense and Immunomodulation of Mucosal Candidiasis
Paul J. Fidel, Jr., and Mairi C. Noverr
A10 Microbiota-Targeted Therapies: An Ecological Perspective
Katherine P. Lemon, Gary C. Armitage, David A. Relman, and Michael Fischbach
A11 Community Ecology and the Vaginal Microbiome
Larry J. Forney and Jacques Ravel
A12 Investigating Bacterial-Animal Symbioses with Light Sheet Microscopy
Michael J. Taormina, Matthew Jemielita, W. Zac Stephens, Adam R. Burns, Joshua V. Troll, Raghuveer Parthasarathy, and Karen Guillemin
Josbert J. Keller and Els van Nood
Daniel Garrido, David C. Dallas, and David A. Mills
A15 Bacteriophage Adhering to Mucus Provide a Non–Host-Derived Immunity
Jeremy J. Barr, Rita Auro, Mike Furlan, Katrine L. Whiteson, Marcella L. Erb, Joe Pogliano, Aleksandr Stotland, Roland Wolkowicz, Andrew S. Cutting, Kelly S. Doran, Peter Salamon, Merry Youle, and Forest Rohwer
A16 Topographic Diversity of Fungal and Bacterial Communities in Human Skin
Keisha Findley, Julia Oh, Joy Yang, Sean Conlan, Clayton Deming, Jennifer A. Meyer, Deborah Schoenfeld, Effie Nomicos, Morgan Park, NIH Intramural Sequencing Center Comparative Sequencing Program, Heidi H. Kong, and Julia A. Segre
Neil R. Gottel, Hector F. Castro, Marilyn Kerley, Zamin Yang, Dale A. Pelletier, Mircea Podar, Tatiana Karpinets, Ed Uberbacher, Gerald A. Tuskan, Rytas Vilgalys, Mitchel J. Doktycz, and Christopher W. Schadt
A18 Interactions Between Commensal Fungi and the C-Type Lectin Receptor Dectin-1 Influence Colitis
Iliyan D. Iliev, Vincent A. Funari, Kent D. Taylor, Quoclinh Nguyen, Christopher N. Reyes, Samuel P. Strom, Jordan Brown, Courtney A. Becker, Phillip R. Fleshner, Marla Dubinsky, Jerome I. Rotter, Hanlin L. Wang, Dermot P. B. McGovern, Gordon D. Brown, and David M. Underhill
A19 Metagenomics and Personalized Medicine
Herbert W. Virgin and John A. Todd
A20 From Genetics of Inflammatory Bowel Disease Towards Mechanistic Insights
Daniel B. Graham and Ramnik J. Xavier
Tables, Figures, and Boxes
TABLES
WO-1 Microbial Ecology Definitions
WO-2 Changes in Human Ecology That Might Affect Microbiota Composition
A2-1 Changes in Human Ecology That Might Affect Microbiota Composition
A3-1 Metabolic Consequences of Specified Host and Dietary Interactions with the Microbiome
A6-1 Ground Squirrel Body Mass, Cecal Tissue Mass, Body Temperature, and Torpor Characteristics
A6-3 Correlations Between SCFA Levels and Microbial Taxa in Squirrel Cecal Contents
A11-1 Median Vaginal pH by Community State Types Within Ethnic Background
A12-1 List of Key Parts for the Author’s Light Sheet Microscope
FIGURES
WO-1 Model for early colonization
WO-3 Host–microbe systems biology
WO-4 Monoassociation with zebrafish gut bacterial isolates elicits a wide range of neutrophil influx
WO-5 The gut microbial community composition changes over developmental time
WO-6 Positive and negative selection of colonizing microbial species in the gut
WO-7 The dynamic interfaces that exist between plants, microbes, and the environment
WO-8 Constructed communities based on functional diversity
WO-9 The ancestry of humans reflected in the genomic signature
WO-11 Annual cycles of body temperature, gut morphology, and feeding behavior
WO-12 Compositional differences in the microbiota by anatomical site
WO-14 The continuum of microbial states and immune responses: a dynamic equilibrium
WO-15 The intestinal mucosa in states of health and disease
WO-17 Bacterial diversity increases with age in populations from distinct cultural traditions
WO-18 Factors modifying mother-to-child microbial transmission
WO-19 Influence of birth cohort on risk of breast cancer among BRCA-1 and BRCA-2 mutation carriers
WO-21 Epithelial cell sensitivity—organism threshold hypothesis
WO-22 Potential consequences of commensal-specific memory T cells
WO-23 Chronic viral infections in humans
WO-24 The Bacteriophage Adherence to Mucus Immunity model
WO-26 Bacterial phyla identified in the human gut microbiota
WO-27 IBD as a multifactorial disorder
WO-29 Proposed metabolic roles of the gut microbiome in IBD
WO-30 Therapeutic modulation of the gut microbiota: from the cradle to the grave
WO-31 Natural products with medicinal relevance
WO-32 Genomics can reveal cryptic natural products
WO-33 The secreted anti-infective protein/peptide arsenal of innate immunity
WO-34 Wound healing in a severely wounded bottlenose dolphin
WO-35 Atopic dermatitis (AD) progression hypothesis
A1-1 Commensal-specific T cells at homeostasis and during infection
A1-2 Potential consequences of commensal-specific memory T cells
A2-1 The effect of maternal status on the resident microbiota of the next generation
A2-2 Helicobacter pylori prevalence in the United States by age and year of birth
A2-3 Interactions between host and microbiota
A3-1 Pathways in microbe-induced obesity
A3-2 Pathways involving microbiome and immunity that contribute to obesity
A3-3 Response of r- and K-selected species to environmental stress
A3-4 Microbial equilibrium and host effects in relation to energy substrates
A4-4 Microbiota affects tissue specific iNKT cell accumulation by genetic modifications of Cxcl16
A5-2 Disturbance can be illustrated using a stability landscape schematic
A6-1 Principal coordinate analysis plots of unweighted UniFrac metrics for squirrel microbiotas
A6-2 Alpha diversity rarefaction plots of squirrel cecal microbiotas
A6-3 Phylogenetic trees of squirrel cecal microbiotas colored by seasonal taxa
A6-4 Relative abundance of major taxa in squirrel cecal microbiotas
A7-1 The insect IMD pathway and persistence of resident microorganisms
A8-2 The dualistic and the continuum models of the microbial and immunological worlds
A8-3 The continuum of microbial states and immune responses: a dynamic equilibrium
A9-1 OPC: Protection, susceptibility, and results of treatment with ART/PI or IFN-g
A9-3 Proposed model of immunopathogenesis of Candida-associated denture stomatitis
A10-1 Microbial communities as networks
A10-2 New opportunities in treatment and diagnostics
A10-3 Microbiota-targeted therapy can shift a community to a healthier stable state
A11-2 Representation of vaginal bacterial community groups within each ethnic group of women
A11-3 Contribution of ethnicity to each of the five vaginal community groups expressed as percentage
A11-5 Assignment of vaginal community state types
A11-6 Dynamics of vaginal community state types in 32 women over 16 weeks
A11-9 Temporal dynamics of vaginal bacterial communities in two women over 16 weeks
A12-1 A zebrafish larva at 7 dpf (days post-fertilization)
A12-2 Schematic illustrations of fluorescence imaging techniques
A12-3 Schematic illustration of our light sheet microscope setup
A12-5 Fluorescently labeled enteroendocrine cells in a larval zebrafish gut
A12-7 Image auto- and cross-correlations
A15-1 Phage adhere to cell-associated mucus layers and mucin glycoprotein
A15-2 Effect of phage adsorption on subsequent bacterial infection of epithelial cells
A15-3 Effect of Hoc protein on phage–mucin interactions
A16-1 Relative abundance of fungal genera and Malassezia species at different human skin sites
A16-2 Median richness of fungal and bacterial genera
A16-3 Forces that shape fungal and bacterial communities
A16-4 Clinical involvement alters shared fungal community structure
A17-1 Rarefaction curves for bacterial OTUs, clustering at 97% rRNA sequence similarity
A17-2 Rarefaction curves for fungal OTUs, clustering at 95% rRNA sequence similarity
A18-1 Commensal fungi are present in the intestine and are recognized by Dectin-1
A18-2 Dectin-1 regulates the severity of colitis
A19-1 Perfect storms for developing Crohn’s disease and type 1 diabetes
A19-2 Refining the relationship between genotype and phenotype in complex inflammatory diseases
A19-3 The iterative redefinition of mechanism-based disease subtypes
A19-4 Microbe plus gene interactions determine inflammatory bowel disease phenotypes
A19-5 A metagenetic view of developing normal and pathological immune responses
A20-1 From genetics to disease mechanisms
A20-2 Inflammatory bowel disease (IBD) pathways and key cell types
A20-3 Molecular pathogenesis of inflammatory bowel disease (IBD): assembling the evidence