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NOTICE: The project that is the subject of this report 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 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, Department of the Army: Global Emerging Infections Surveillance and Response System, Medical Research and Materiel Command, and the Defense Threat Reduction Agency; 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; American Society for Microbiology; sanofi pasteur; Burroughs Wellcome Fund; GlaxoSmithKline; Infectious Diseases Society of America; and the Merck Company Foundation. The views presented in this publication do not necessarily reflect the views of the organizations or agencies that provided support for this project.
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Cover images: (Front) Colony developed by the Gram-positive social bacteria Paenibacillus dendritiformis (chiral morphotype). The colony diameter is about 6 cm, and the number of cells is about the same as the number of people on Earth. For more information see http://star.tau.ac.il/~eshel. Photo credit: Eshel Ben-Jacob/Tel Aviv University. (Back) Bioluminescence offers undersea advantages to (clockwise from top left) a pelagic worm, squid, krill, scaleless black dragonfish, and deepwater jellyfish. Photo Credit: Edith Widder/Ocean Research and Conservation Association.
Suggested citation: IOM (Institute of Medicine). 2012. The Social Biology of Microbial Communities: 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.
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PLANNING COMMITTEE FOR A WORKSHOP ON
THE MICROBIOME IN HEALTH AND DISEASE1
BONNIE BASSLER, Princeton University, Princeton, New Jersey
ARTURO CASADEVALL, Albert Einstein College of Medicine, Bronx, New York
JONATHAN EISEN, University of California, Davis, California
JO HANDELSMAN, Yale University, New Haven, Connecticut
CAROLE HEILMAN, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland
DAVID RELMAN, Stanford University and Veterans Affairs Palo Alto Health Care System, Palo Alto, California
P. FREDRICK SPARLING, University of North Carolina, Chapel Hill, North Carolina
___________
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), The Ohio State University, Columbus, Ohio
KEVIN ANDERSON, Biological and Chemical Defense Division, Science and Technology Directorate, Department of Homeland Security, Washington, DC
DAVID BLAZES,2 Division of Global Emerging Infectious Surveillance, Armed Forces Health Surveillance Center, Silver Spring, Maryland
ENRIQUETA C. BOND, Burroughs Wellcome Fund (Emeritus), QE Philanthropic Advisors, Marshall, Virginia
ROGER G. BREEZE, Lawrence Livermore National Laboratory, Livermore, California
PAULA R. BRYANT, Defense Threat Reduction Agency, Medical S&T Division, Fort Belvoir, Virginia
JOHN E. BURRIS, Burroughs Wellcome Fund, Research Triangle Park, North Carolina
ARTURO CASADEVALL, Albert Einstein College of Medicine, Bronx, New York
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, 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,3 Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, Maryland
JESSE L. GOODMAN, Food and Drug Administration, Rockville, Maryland
___________
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 March 31, 2012.
3 Forum member since June 1, 2012.
EDUARDO GOTUZZO, Instituto de Medicina Tropical–Alexander von Humbolt, 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, Health Protection Agency, London, United Kingdom
ZHI HONG, 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,4 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
STANLEY M. LEMON, School of Medicine, University of North Carolina, Chapel Hill, North Carolina
EDWARD McSWEEGAN, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland
MARK A. MILLER,5 Fogarty International Center, Bethesda, Maryland
JULIE PAVLIN,6 Armed Forces Health Surveillance Center, Silver Spring, Maryland
GEORGE POSTE, Complex Adaptive Systems Initiative, Arizona State University, Tempe, Arizona
DAVID RIZZO, Department of Plant Pathology, University of California, Davis, California
GARY A. ROSELLE, Veterans Health Administration, Department of Veterans Affairs, Cincinnati, Ohio
ALAN S. RUDOLPH, Defense Threat Reduction Agency, Fort Belvoir, Virginia
KEVIN RUSSELL, Armed Forces Health Surveillance Center, Silver Spring, Maryland
JANET SHOEMAKER, American Society for Microbiology, Washington, DC
P. FREDERICK SPARLING, University of North Carolina, Chapel Hill, North Carolina
MURRAY TROSTLE, U.S. Agency for International Development, Washington, DC
MARY E. WILSON, Harvard School of Public Health, Harvard University, Boston, Massachusetts
___________
4 Forum member since June 1, 2012.
5 Forum member until August 31, 2012.
6 Forum member since April 1, 2012.
BOARD ON GLOBAL HEALTH1
RICHARD GUERRANT (Chair), Thomas H. Hunter Professor of International Medicine and Director, Center for Global Health, University of Virginia School of Medicine, Charlottesville, Virginia
JO IVEY BOUFFORD (IOM Foreign Secretary), President, New York Academy of Medicine, New York, 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, 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, Professor and Chair, Emergency Medicine, Director, Medical College of Wisconsin, Milwaukee, Wisconsin
JAMES HOSPEDALES, Coordinator, Chronic Disease Project, Health Surveillance and Disease Management Area, Pan American Health Organization and World Health Organization, Washington, DC
PETER J. HOTEZ, Professor and Chair, Department of Microbiology, Immunology, and Tropical Medicine, The George Washington University, Washington, DC
CLARION JOHNSON, Global Medical Director, Medicine and Occupational Medicine Department, 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.
GUY PALMER, Regents Professor of Pathology and Infectious Diseases, Director of the School for Global Animal Health, Washington State University, Pullman, Washington
THOMAS C. QUINN, 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
JENNIFER PRAH RUGER, Associate Professor, Division of Health Policy and Administration, Yale University School of Public Health, New Haven, Connecticut
Staff
PATRICK KELLEY, Director
ANGELA CHRISTIAN, Program Associate
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:
Eshel Ben-Jacob, School of Physics and Astronomy, Tel Aviv University, Tel Aviv, Israel
Steve Diggle, School of Molecular Medical Sciences, University of Nottingham, Nottingham, United Kingdom
David Rizzo, Department of Plant Pathology, University of California, Davis, California
Mary E. Wilson, Harvard School of Public Health, Harvard University, Boston, Massachusetts
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 Dr. Melvin Worth. Appointed by the Institue 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: Bonnie Bassler (Princeton University), Arturo Casadevall (Albert Einstein College of Medicine), Jonathan Eisen (University of California, Davis), Jo Handelsman (Yale University), Carole Heilman (National Institute of Allergy and Infectious Diseases, NIH), David Relman (Stanford University and Veterans Affairs Palo Alto Health Care System), and P. Fredrick 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, program officer; Katherine McClure, senior program associate; Rebekah Hutton, research associate; and Pamela Bertelson, 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, Alison Mack, Vilija Teel, and Sarah Ziegenhorn.
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, Department of the Army: Global Emerging Infections Surveillance and Response System, Medical Research and Materiel Command, and the Defense Threat Reduction Agency; 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; American Society for Microbiology; sanofi pasteur; Burroughs Wellcome Fund; GlaxoSmithKline; Infectious Diseases Society of America; and the Merck Company Foundation. 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.
___________
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.
Contents
The Social Biology of Microbial Communities
Organization of the Workshop Summary
Glimpses of Microbial Community Dynamics
Microbial Communities in Biotic and Abiotic Environments
Multicellular structures for migration and dispersal
Plant roots and their partners
Microbial inhabitants of the human gut
Microbial Communities: The Ultimate Social Network
Interactions with Other Species: Bioluminescence in Marine Microbial Communities
Structure and Function of Microbial Communities
Factors Influencing Community Formation and Function
The Role of Oxygen in the Structure and Function of Microbial Communities
Source-Sink Dynamics: Host-Associated and Free-Living Chemosynthetic Symbionts
Phylogenetic and Phylogenomic Approaches to Studies of Microbial Communities
Microbial Community Assembly and Dynamics: From Acidophilic Biofilms to the Premature Infant Gut
Dynamic Interactions of Microbial Communities
Communication and Information Processing
Intraspecies Interaction: Contact-Dependent Communication
Interkingdom Interactions: Symbiotic Microbes, Their Mammalian Host, and Invading Pathogens
Swarming Bacteria as Agents of Microbial Dispersal
The Fungal Gardens of the Leaf-Cutter Ants
Evolution of Cooperation and Control of Cheating in the Social Amoeba
Emergence and Robustness of Multicellular Behavior in Bacteria
Evolutionary Transitions to Multicellularity
Communities of microbes and genes
Cooperative Survival Strategies
Community Cooperation and the Expression of Virulence
Cooperation, Cheating, and Coordinated Behaviors
Multicellular behavior in bacteria
Evolutionary Transitions Through Higher-Level Selection
Looking Ahead: Moving to the Community as the Unit of Study
Developing Theoretical and Experimental Frameworks
Microbial Communities as Complex Adaptive Systems
Probing Resilience Through Perturbation
New Tools and Approaches for an Emerging Field of Inquiry
Statistical Tools for Integrating Community Networks and Spatial and Clinical Data
Insights into Life on Earth and Other Worlds
Untapped Innovation and Functional Novelty
A1 Strain-Resolved Community Genomic Analysis of Gut Microbial Colonization in a Premature Infant
Michael J. Morowitz, Vincent J. Denef, Elizabeth K. Costello, Brian C. Thomas, Valeriy Poroyko, David A. Relman, and Jillian F. Banfield
A2 Evolution of Virulence in Opportunistic Pathogens: Generalism, Plasticity, and Control
Sam P. Brown, Daniel M. Cornforth, and Nicole Mideo
A3 Free-Living Tube Worm Endosymbionts Found at Deep-Sea Vents
Tara L. Harmer, Randi D. Rotjan, Andrea D. Nussbaumer, Monika Bright, Andrew W. Ng, Eric G. DeChaine, and Colleen M. Cavanaugh
A4 Parasites May Help Stabilize Cooperative Relationships
Ainslie E. F. Little and Cameron R. Currie
Frank O. Aylward, Kristin E. Burnum, Jarrod J. Scott, Garret Suen, Susannah G. Tringe, Sandra M. Adams, Kerrie W. Barry, Carrie D. Nicora, Paul D. Piehowski, Samuel O. Purvine, Gabriel J. Starrett, Lynne A. Goodwin, Richard D. Smith, Mary S. Lipton, and Cameron R. Currie
A6 Phylogenetic and Phylogenomic Approaches to Studies of Microbial Communities
Jonathan A. Eisen
A7 Sociomicrobiology and Quorum Sensing—Mediated Communication
Josephine R. Chandler and E. Peter Greenberg
Josephine R. Chandler, Silja Heilmann, John E. Mittler, and E. Peter Greenberg
A9 Rules of Engagement: Interspecies Interactions That Regulate Microbial Communities
Ainslie E. F. Little, Courtney J. Robinson, S. Brook Peterson, Kenneth F. Raffa, and Jo Handelsman
A10 Statistical Data Analysis Challenges from the Microbiome
Susan Holmes and Paul J. McMurdie
A11 Dispersal of Cargo Microorganisms by Swarming Bacteria
Colin J. Ingham
Xinning Zhang and Jared R. Leadbetter
A13 Mathematical and Computational Challenges in the Study of Complex Adaptive Microbial Systems
Simon A. Levin, Juan A. Bonachela, and Carey D. Nadell
Elie J. Diner, Christina M. Beck, Julia S. Webb, David A. Low, and Christopher S. Hayes
Paul B. Rainey and Benjamin Kerr
A16 An Ecological and Evolutionary Perspective on Human-Microbe Mutualism and Disease
Les Dethlefsen, Margaret McFall-Ngai, and David A. Relman
Les Dethlefsen and David A. Relman
Vincent B. Young, Stacy A. Kahn, Thomas M. Schmidt, and Eugene B. Chang
A19 Inter-Kingdom Signalling: Communication Between Bacteria and Their Hosts
David T. Hughes and Vanessa Sperandio
A20 Evolution of Cooperation and Control of Cheating in a Social Microbe
Joan E. Strassmann and David C. Queller
A21 Glowing Corpses and Radiant Excrement: The Role of Bioluminescence in Microbial Communities
Edith A. Widder
A22 Social Interaction, Noise and Antibiotic-Mediated Switches in the Intestinal Microbiota
Vanni Bucci, Serena Bradde, Giulio Biroli, and Joao B. Xavier
A8-1 Sensitivity of C. violaceum (Cv) Strains to B. thailandensis (Bt) culture fluid
A8-2 Sensitivity of B. thailandensis (Bt) Strains to C. violaceum (Cv) Culture Fluid
A8-3 Final Yields of B. thailandensis (Bt) and C. Violaceum (Cv) in a Pure Culture and Co-Culture
A10-1 Differentially Represented OTUs
A12-1 Characteristics of Higher Termites Examined in this Study
A12-2 fdhF Inventories Constructed in this Study
A12-3 Distribution of Higher Termite Inventory Sequences amongst Four Major FDHH Clades
A12-4 PCR Conditions for Clone Library Construction
A12-5 Detailed Composition of Higher Termite fdhF Inventories
A12-6 Sequences Used in Phylogenetic Analyses
A13-1 Exponents Measured in the Different Theoretical and Experimental Work Cited in the Text
A14-1 Proteins Identified in the Cdi-CT Activating Fraction
A16-1 Model Systems for Animal–Microbe Symbioses
A17-1 Pyrosequencing reads, refOTUs, and coverage
A19-1 Hormonal Signals, Receptors and Biological Functions
FIGURES
WO-1 Microbial biofims: Sticking together for success
WO-2 Myxobacteria build multicellular fruiting bodies
WO-3 The bacterium and the squid
WO-5 An example of nitrogen-fixing symbiosis between legumes and rhizobia bacteria
WO-6 The microbiome of various anatomical locations of the human body
WO-7 Mechanism of quorum sensing in the luminescent bacterium Vibrio fischeri
WO-9 The burglar alarm jellyfish lights up blue to call in predators of its attackers
WO-10 Progression from studies on the individual scale to studies on the community scale
WO-11 Oxygen gradients and microbial function
WO-12 Hydrothermal vent organisms and their bacterial symbionts
WO-13 Molecular communication networks between organisms in the Bacillus cereus biocontrol system
WO-14 Parts of a root tip and areas of the rhizosphere
WO-17 Microbial community proteomics: Functional assays in situ
WO-18 The dynamic genetic repertoire of microbial communities
WO-19 Contact-dependent growth inhibition (CDI)
WO-22 Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ants
WO-24 Cheating in low-relatedness studies
WO-25 rhlA regulation ensures metabolic prudence
WO-26 A putative life cycle for mat-forming bacteria
WO-28 Patterns emerge from individual interactions in bacterial communities
WO-29 The persistence of influenza A illustrates how robustness can result from flexibility
WO-30 Alternative stable states, disturbance, and loss of resilience
A1-1 Multiple stable compositional states in the developing gut microbiota of the premature infant
A1-3 Analyses of two ecologically divergent Citrobacter UC1CIT subpopulations
A1-4 Citrobacter UC1CIT genomic overview
A2-1 Ecological and evolutionary dynamics of virulence factors across two growth environments
A3-1 FISH detection of free-living vestimentiferan bacterial symbionts
A4-1 Cheating/infection experiments
A4-2 Prisoner’s Dilemma simulations
A4-3 Cooperation and conflict within the fungus-growing ant microbe symbiosis
A5-3 Comparison of the COG category distributions of the three combined fungus-garden metagenomes
A6-4 Phylogenetic diversity of Sargasso Sea sequences using multiple phylogenetic markers
A6-5 A flow chart of the STAP pipeline
A6-6 A flow chart illustrating the major components of AMPHORA
A6-8 Major phylotypes identified in Sargasso Sea metagenomic data
A6-9 Comparison of the phylotyping performance by AMPHORA and MEGAN
A6-17 Searching for novel phylogenetic lineages
A6-18 Phylogenetic tree of the RecA superfamily
A6-19 Phylogenetic tree of the RpoB superfamily
A6-20 Outline of a phylogenomic methodology
A6-21 Phylogenomic functional prediction is based on the concept of phylotyping
A6-22 Phylogenetically biased genome sequencing
A7-1 Some examples of acyl-HSL quorum-sensing signals
A7-2 Acyl-HSL signaling in V. fischeri and P. aeruginosa
A7-3 The quorum-sensing circuits of B. thailandensis, B. pseudomallei, and B. mallei
A8-1 B. thailandensis–C. violaceum competition
A8-4 C. violaceum (Cv) quorum sensing is activated by B. thailandensis (Bt) AHLs
A8-5 Eavesdropping promotes competitiveness of Cv in co-cultures with a B. Bt bactobolin mutant
A9-1 Continuum of interspecific interactions that occur in microbial communities
A9-2 Progression from studies on the individual scale to studies on the community scale
A9-3 Four groups of questions in microbial ecology and some techniques to address them
A10-1 1985: A dripping tap. 1998: A fire hydrant. 2012: A perfect storm
A10-2 A) Heatmap of abundance reads. B) Volcano plot for expressions with transparency
A10-3 Global patterns global data mapped onto the OTU reference tree
A10-4 Plotting the values of gPCA variables with a tree using R
A10-5 Multicomponent class typical to R
A10-7 A PCA flowchart, with choice levels highlighted
A10-9 Network of enterotype taxa co-occurring in at least 85 percent of the samples
A11-1 Swarming by Proteus mirabilis
A11-2 Microscopy of P. vortex cells and microcolonies
A11-3 Pattern formation by swarming P. vortex
A11-4 Transport of A. fumigatus conidia by P. vortex
A11-5 Transport of conidia by P. vortex
A11-6 Examples of motile microorganisms moving other objects within microengineered environments
A11-8 Dispersal of motile bacteria facilitated by fungal mycelia
A11-9 Example of dispersal of motile bacteria facilitated by fungal pseudomycelia mycelia
A11-10 Dispersal of Streptomyces coelicolor spores facilitated by swarming P. vortex
A12-1 Mitochondrial cytochrome oxidase II (COII) phylogeny of termites and related roaches
A12-3 Protein phylogeny of hydrogenase-linked formate dehydrogenases (FDHH)
A12-4 Protein phylogeny of Sec and Cys clade sequences within the “Gut spirochete group” of FDHH
A12-6 Protein phylogeny of Higher Termite Spirochete group sequences
A12-7 Protein phylogeny and amino acid character analysis of AGR group sequences
A14-3 CdiA-CT is an intrinsic tRNase
A14-4 CdiA-CT and CysK form a stable complex in vitro
A14-5 Activation of CdiA-CT in E. coli cells results in growth arrest and tRNA degradation
A14-6 CysK is required for CdiA-CT-mediated growth inhibition and tRNase activity in vivo
A14-7 CysK is required for growth inhibition during CDIUPEC536
A15-1 The role of group reproduction in group adaptation
A15-2 The rise, fall, and destruction of a simple undifferentiated group
A15-3 A putative life cycle for mat-forming bacteria
A16-1 Site-specific distributions of bacterial phyla in healthy humans
A16-2 Patterns of human-associated microbial diversity
A17-1 Heat map displaying the relative abundance of refOTUs in three prominent clades of bacteria
A17-2 Three measures of biological diversity for samples
A19-1 Chemical structures of bacterial and host signals
A19-2 Mammalian signalling through membrane receptors
A19-3 Adrenergic sensing in enterohaemorrhagic Escherichia coli
A19-4 AHL inter-kingdom signalling
A20-1 D. discoideum fruiting bodies on an agar plate
A20-2 Colony cycles of D. discoideum
A20-3 In the social stage, clones may take advantage of their partner in three different ways
A21-4 Female anglerfish with attached male
A21-6 The life-cycle of the nematode host of the bioluminescent bacterium Photorhabdus luminescens
A22-2 Multistability and hysteresis in a simple model of the intestinal microbiota
A22-S1 Vectorial field of forces and the phase-plane analysis for bistable conditions
A22-S2 Model nullclines analysis in the absence of noise
A22-S6 Stationary path connecting the stable points 1 and 2
A22-S8 Log2 abundance versus samples for all the phylotypes detected in each subject (A-C)
A22-S9 Ordination plot of the time samples based on their first two principal components