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The Social Biology of Microbial Communities Workshop Summary LeighAnne Olsen, Eileen R. Choffnes, and Alison Mack, Rapporteurs Forum on Microbial Threats Board on Global Health

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THE NATIONAL ACADEMIES PRESS 500 Fifth Street, NW Washington, DC 20001 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; G laxoSmithKline; 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. International Standard Book Number-13: 978-0-309-26432-7 International Standard Book Number-10: 0-309-26432-4 Additional copies of this report are available from the National Academies Press, 500 Fifth Street, NW, Keck 360, Washington, DC 20001; (800) 624-6242 or (202) 334-3313; http://www.nap.edu. For more information about the Institute of Medicine, visit the IOM home page at: www. iom.edu. Copyright 2012 by the National Academy of Sciences. All rights reserved. Printed in the United States of America The serpent has been a symbol of long life, healing, and knowledge among almost all cultures and religions since the beginning of recorded history. The serpent adopted as a logotype by the Institute of Medicine is a relief carving from ancient Greece, now held by the Staatliche Museen in Berlin. 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.

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"Knowing is not enough; we must apply. Willing is not enough; we must do." --Goethe Advising the Nation. Improving Health.

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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. Charles M. Vest 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 examina- tion 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 Na- tional 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. Charles M. Vest are chair and vice chair, respectively, of the National Research Council. www.national-academies.org

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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. v

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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 HealthSeattle 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 docu- ments. 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. vi

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EDUARDO GOTUZZO, Instituto de Medicina TropicalAlexander von Humbolt, Universidad Peruaa 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. vii

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Staff EILEEN CHOFFNES, Scholar and Director LEIGHANNE OLSEN, Program Officer KATHERINE McCLURE, Senior Program Associate REBEKAH HUTTON, Research Associate PAMELA BERTELSON, Senior Program Assistant viii

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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. ix

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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 x

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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 Com- mittee. The purpose of this independent review is to provide candid and criti- cal 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 com- ments and suggestions, they did not see the final draft of the workshop summary xi

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xviiiCONTENTS A11 Dispersal of Cargo Microorganisms by Swarming Bacteria, 304 Colin J. Ingham A12 Evidence for Cascades of Perturbation and Adaptation in the Metabolic Genes of Higher Termite Gut Symbionts, 323 Xinning Zhang and Jared R. Leadbetter A13 Mathematical and Computational Challenges in the Study of Complex Adaptive Microbial Systems, 361 Simon A. Levin, Juan A. Bonachela, and Carey D. Nadell A14 Identification of a Target Cell Permissive Factor Required for Contact-Dependent Growth Inhibition (CDI), 385 Elie J. Diner, Christina M. Beck, Julia S. Webb, David A. Low, and Christopher S. Hayes A15 Cheats as First Propagules: A New Hypothesis for the Evolution of Individuality During the Transition from Single Cells to Multicellularity, 409 Paul B. Rainey and Benjamin Kerr A16 An Ecological and Evolutionary Perspective on Human-Microbe Mutualism and Disease, 426 Les Dethlefsen, Margaret McFall-Ngai, and David A. Relman A17 Incomplete Recovery and Individualized Responses of the Human Distal Gut Microbiota to Repeated Antibiotic Perturbation, 447 Les Dethlefsen and David A. Relman A18 Studying the Enteric Microbiome in Inflammatory Bowel Diseases: Getting Through the Growing Pains and Moving Forward, 470 Vincent B. Young, Stacy A. Kahn, Thomas M. Schmidt, and Eugene B. Chang A19 Inter-Kingdom Signalling: Communication Between Bacteria and Their Hosts, 484 David T. Hughes and Vanessa Sperandio A20 Evolution of Cooperation and Control of Cheating in a Social Microbe, 509 Joan E. Strassmann and David C. Queller A21 Glowing Corpses and Radiant Excrement: The Role of Bioluminescence in Microbial Communities, 533 Edith A. Widder A22 Social Interaction, Noise and Antibiotic-Mediated Switches in the Intestinal Microbiota, 549 Vanni Bucci, Serena Bradde, Giulio Biroli, and Joao B. Xavier B Agenda 581 CAcronyms 585 D Glossary 587 E Speaker Biographies 595

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Tables, Figures, and Boxes TABLES WO-1 Social Traits Exhibited by Bacteria Compared with Examples from Vertebrates and Invertebrates, 14 A2-1 An Ecological Classification of Pathogens with Representative Examples, 116 A3-1 Detection of Free-Living Symbiont Phylotype of Vent Vestimentiferan Tube Worms Via PCR and Sequence Analyses of Biofilms, 131 A5-1 Sequencing Statistics of the Community Metagenomes, 158 A5-2 Family-Level Classification of Partial-Length 16S Sequences Recovered from Atta Colombica and Atta Cephalotes Fungus Gardens, 159 A5-3 Phylogenetic Classification of All Assembled Contigs and Singletons in the Leaf-Cutter Ant Fungus Garden Metagenomes, 161 A5-4 Partial List of CAZymes Identified in the Leaf-Cutter Ant Fungus- Garden Metagenomes, as Compared with Those Found in the Termite Hindgut and Wallaby Foregut, 165 A5-5 A Subset of Bacterial Proteins Identified in Leaf-Cutter Ant Fungus Gardens Using Liquid Chromatography-Tandem Mass Spectrometry, 169 xix

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xx TABLES, FIGURES, AND BOXES A8-1 Sensitivity of C. violaceum (Cv) Strains to B. thailandensis (Bt) culture fluid, 229 A8-2 Sensitivity of B. thailandensis (Bt) Strains to C. violaceum (Cv) Culture Fluid, 230 A8-3 Final Yields of B. thailandensis (Bt) and C. Violaceum (Cv) in a Pure Culture and Co-Culture, 231 A10-1 Differentially Represented OTUs, 288 A12-1 Characteristics of Higher Termites Examined in this Study, 328 A12-2 fdhF Inventories Constructed in this Study, 330 A12-3 Distribution of Higher Termite Inventory Sequences amongst Four Major FDHH Clades, 333 A12-4 PCR Conditions for Clone Library Construction, 346 A12-5 Detailed Composition of Higher Termite fdhF Inventories, 348 A12-6 Sequences Used in Phylogenetic Analyses, 351 A13-1 Exponents Measured in the Different Theoretical and Experimental Work Cited in the Text, 369 A14-1 Proteins Identified in the Cdi-CT Activating Fraction, 390 A16-1 Model Systems for AnimalMicrobe Symbioses, 432 A17-1 Pyrosequencing reads, refOTUs, and coverage, 451 A19-1 Hormonal Signals, Receptors and Biological Functions, 489 FIGURES WO-1 Microbial biofims: Sticking together for success, 6 WO-2 Myxobacteria build multicellular fruiting bodies, 8 WO-3 The bacterium and the squid, 9 WO-4 The winnowing, 10 WO-5 An example of nitrogen-fixing symbiosis between legumes and rhizobia bacteria, 11 WO-6 The microbiome of various anatomical locations of the human body, 12 WO-7 Mechanism of quorum sensing in the luminescent bacterium Vibrio fischeri, 19 WO-8 The chemical structures of the four best-known luciferins are as diverse as their phylogenetic distribution, 22

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TABLES, FIGURES, AND BOXES xxi WO-9 The burglar alarm jellyfish lights up blue to call in predators of its attackers, 24 WO-10 Progression from studies on the individual scale to studies on the community scale, 25 WO-11 Oxygen gradients and microbial function, 29 WO-12 Hydrothermal vent organisms and their bacterial symbionts, 31 WO-13 Molecular communication networks between organisms in the Bacillus cereus biocontrol system, 34 WO-14 Parts of a root tip and areas of the rhizosphere, 35 WO-15 rRNA universal tree of life based on a comparison of nucleic acid sequences found in all cellular life (small subunit ribosomal RNA), 37 WO-16 Schematic illustrating important features that make the AMD system a good model for studying microbial communities, 40 WO-17 Microbial community proteomics: Functional assays in situ, 41 WO-18 The dynamic genetic repertoire of microbial communities, 43 WO-19 Contact-dependent growth inhibition (CDI), 46 WO-20 Photograph showing the result of transporting Aspergillus fumigatus conidia by swarming Paenibacillus vortex, 50 WO-21 Colored scanning electron micrograph showing transport of a single conidium of Aspergillus fumigatus transported by swarming Paenibacillus vortex, 51 WO-22 Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ants, 53 WO-23 Inferred evolutionary history for fdhF in the symbiotic gut microbial communities of lignocellulose-feeding insects, 56 WO-24 Cheating in low-relatedness studies, 58 WO-25 rhlA regulation ensures metabolic prudence, 60 WO-26 A putative life cycle for mat-forming bacteria, 61 WO-27 The number of genes distributed among the human-associated microbiota far outnumbers the number of genes humans inherit from their parents, 64 WO-28 Patterns emerge from individual interactions in bacterial communities, 73 WO-29 The persistence of influenza A illustrates how robustness can result from flexibility, 75 WO-30 Alternative stable states, disturbance, and loss of resilience, 78 WO-31 In 1977, the deep-ocean submersible Alvin led scientists to discover tubeworms living at the edges of hydrothermal vents in the deep sea, 82 A1-1 Multiple stable compositional states in the developing gut microbiota of the premature infant, 100 A1-2 Population dynamics based on metagenomic profiling, 102

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xxii TABLES, FIGURES, AND BOXES A1-3 Analyses of two ecologically divergent Citrobacter UC1CIT subpopulations, 105 A1-4 Citrobacter UC1CIT genomic overview, 107 A2-1 Ecological and evolutionary dynamics of virulence factors across two growth environments, 120 A2-2 Adaptation to a benign environment A can pre-adapt an opportunistic pathogen for virulent growth in V if there is a significant positive association between the properties of environments A and V, 121 A2-3 Adaptation to a benign environment A can reduce the capacity for virulent growth in V (and vice versa) if there is a significant negative association (trade-off) between growth rates g and r, 122 A3-1 FISH detection of free-living vestimentiferan bacterial symbionts, 133 A4-1 Cheating/infection experiments, 145 A4-2 Prisoner's Dilemma simulations, 146 A4-3 Cooperation and conflict within the fungus-growing ant microbe symbiosis, 148 A5-1 Leaf cutter ants forage on plant material that they use as manure for specialized fungus gardens, 155 A5-2 Reconstruction of KEGG pathways recovered from phylogenetic bins generated from the leaf-cutter ant fungus-garden metagenomes, 163 A5-3 Comparison of the COG category distributions of the three combined fungus-garden metagenomes, 164 A5-4 Fragment recruitment analysis of genes phylogenetically binned to Enterobacter FGI 35 against the draft Enterobacter FGI 35 genome, 167 A5-5 Example of overlap between field-collected and laboratory-reared fungus-garden samples for the glycoside hydrolase family 3 peptide N.AIADLLFGDVNPSGK.L, 168 A6-1 Unrooted phylogenetic tree showing the position of the S. velum symbionts in relation to that of other Proteobacteria species on the basis of 16s rRNA gene sequences, 183 A6-2 rRNA tree, 184 A6-3 RecA tree, 185 A6-4 Phylogenetic diversity of Sargasso Sea sequences using multiple phylogenetic markers, 186 A6-5 A flow chart of the STAP pipeline, 188 A6-6 A flow chart illustrating the major components of AMPHORA, 189 A6-7 An unrooted maximum likelihood bacterial genome tree, 190

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TABLES, FIGURES, AND BOXES xxiii A6-8 Major phylotypes identified in Sargasso Sea metagenomic data, 192 A6-9 Comparison of the phylotyping performance by AMPHORA and MEGAN, 193 A6-10 Hypothetical multiple sequence alignment including full length "reference" sequences as well as fragmentary sequences from metagenomic data, 194 A6-11 Hypothetical multiple sequence alignment showing one approach to carrying out phylogenetic analysis of metagenomic data--to extract a "core" region of the alignment and only analyze sequences that contain most of this core, 194 A6-12 Hypothetical multiple sequence alignment showing an alternative strategy for phylogenetic analysis of metagenomic data--to analyze everything even if some sequences do not overlap with each other, 195 A6-13 Computational processes are represented as squares and databases are represented as cylinders in this generalized workflow of PhylOTU, 196 A6-14 Conceptual overview of approach to infer phylogenetic relationships among sequences from metagenomic data sets, 197 A6-15 Phylogenetic tree linking metagenomic sequences from 31 gene families along an oceanic depth gradient at the HOT ALOHA site, 198 A6-16 Taxonomic diversity and standardized phylogenetic diversity versus depth in environmental samples along an oceanic depth gradient at the HOT ALOHA site, 199 A6-17 Searching for novel phylogenetic lineages, 201 A6-18 Phylogenetic tree of the RecA superfamily, 202 A6-19 Phylogenetic tree of the RpoB superfamily, 203 A6-20 Outline of a phylogenomic methodology, 205 A6-21 Phylogenomic functional prediction is based on the concept of phylotyping, 206 A6-22 Phylogenetically biased genome sequencing, 208 A6-23 For each of four groupings (species, different strains of Streptococcus agalactiae; family, Enterobacteriaceae; phylum, Actinobacteria; domain, GEBA bacteria), all proteins from that group were compared to each other to identify protein families, 209 A6-24 Using a phylogenetic tree of unique SSU rRNA gene sequences7, phylogenetic diversity was measured for four subsets of this tree: organisms with sequenced genomes pre-GEBA (blue), the GEBA organisms (red), all cultured organisms (dark grey), and all available SSU rRNA genes (light grey), 210 A7-1 Some examples of acyl-HSL quorum-sensing signals, 215 A7-2 Acyl-HSL signaling in V. fischeri and P. aeruginosa, 216 A7-3 The quorum-sensing circuits of B. thailandensis, B. pseudomallei, and B. mallei, 218

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xxiv TABLES, FIGURES, AND BOXES A8-1 B. thailandensisC. violaceum competition, 227 A8-2 Competition in co-cultures of wild-type C. violaceum (Cv) and wild- type or mutant B. thailandensis (Bt) strains, 228 A8-3 Co-cultures of the C. violaceum (Cv) wild-type Cv017 or the AHL mutant Cv026 and the B. thailandensis (Bt) competition-impaired AHL, bactobolin double mutant JBT125, 229 A8-4 C. violaceum (Cv) quorum sensing is activated by B. thailandensis (Bt) AHLs, 233 A8-5 Eavesdropping promotes competitiveness of Cv in co-cultures with a B. Bt bactobolin mutant, 234 A8-6 In silico modeling, 236 A9-1 Continuum of interspecific interactions that occur in microbial communities, 248 A9-2 Progression from studies on the individual scale to studies on the community scale, 257 A9-3 Four groups of questions in microbial ecology and some techniques to address them, 258 A10-1 1985: A dripping tap. 1998: A fire hydrant. 2012: A perfect storm, 276 A10-2 A) Heatmap of abundance reads. B) Volcano plot for expressions with transparency, 280 A10-3 Global patterns global data mapped onto the OTU reference tree, 281 A10-4 Plotting the values of gPCA variables with a tree using R, 282 A10-5 Multicomponent class typical to R, 284 A10-6 Initial analysis with only two batches; on the right we see the addition of a third set of data, 285 A10-7 A PCA flowchart, with choice levels highlighted, 287 A10-8 Network of enterotype groups among samples as defined by patients having 70 percent shared OTUs, 289 A10-9 Network of enterotype taxa co-occurring in at least 85 percent of the samples, 291 A10-10 Procrustes and co-inertia analysis of Cipro patients seen in their compromise common projection (the large scatterplot) and the taxa and mass spec feature projections on the left of the plot, 294 A11-1 Swarming by Proteus mirabilis, 306 A11-2 Microscopy of P. vortex cells and microcolonies, 308 A11-3 Pattern formation by swarming P. vortex, 309 A11-4 Transport of A. fumigatus conidia by P. vortex, 310 A11-5 Transport of conidia by P. vortex, 312 A11-6 Examples of motile microorganisms moving other objects within microengineered environments, 313

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TABLES, FIGURES, AND BOXES xxv A11-7 Simple diagram of soil composed of manifold microniches separated by barriers that include air gaps and aqueous environments, 315 A11-8 Dispersal of motile bacteria facilitated by fungal mycelia, 316 A11-9 Example of dispersal of motile bacteria facilitated by fungal pseudomycelia mycelia, 317 A11-10 Dispersal of Streptomyces coelicolor spores facilitated by swarming P. vortex, 318 A12-1 Mitochondrial cytochrome oxidase II (COII) phylogeny of termites and related roaches, 327 A12-2 Schematic cladogram of major termite families and higher termite subfamilies showing major events in gut habitat evolution, 329 A12-3 Protein phylogeny of hydrogenase-linked formate dehydrogenases (FDHH), 332 A12-4 Protein phylogeny of Sec and Cys clade sequences within the "Gut spirochete group" of FDHH, 334 A12-5 Targeted PCR assays on termite and roach gut DNA using Cys clade specific fdhF primers (Cys499F1b, 1045R), which yield a ca. 600 bp product (ladder left lane: NEB 2-log), 335 A12-6 Protein phylogeny of Higher Termite Spirochete group sequences, 336 A12-7 Protein phylogeny and amino acid character analysis of AGR group sequences, 339 A12-8 Products from nested PCR reactions using universal fdhF primers followed by Amitermes-Gnathamitermes-Rhychotermes clade specific primers on gut templates, 340 A12-9 UniFrac principal component analysis of FDHH phylogeny associated with the gut microbial communities of termites and related insects, 342 A12-10 Inferred evolutionary history for fdhF in the symbiotic gut microbial communities of lignocellulose-feeding insects, 343 A13-1 Morphological phase diagram depicting the five different qualitative behaviors shown by bacterial colonies growing under different agar concentration (CA) and nutrient concentration (C), 363 A13-2 Snapshots of the bacterial colonies obtained, with the detailed simulation framework described in the text, 367 A13-3 Bacterial fronts obtained, with the simulation framework using mid-to- low nutrient concentrations, with an elapse of time of 8 hours, 371 A13-4 A time-series of polymer-producing cells (red) growing in a biofilm with non-producing cells (blue), 379 A14-1 CdiA-CT tRNase activity requires a cofactor, 389 A14-2 CysK is necessary and sufficient for tRNase activity, 391

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xxvi TABLES, FIGURES, AND BOXES A14-3 CdiA-CT is an intrinsic tRNase, 392 A14-4 CdiA-CT and CysK form a stable complex in vitro, 394 A14-5 Activation of CdiA-CT in E. coli cells results in growth arrest and tRNA degradation, 396 A14-6 CysK is required for CdiA-CT-mediated growth inhibition and tRNase activity in vivo, 397 A14-7 CysK is required for growth inhibition during CDIUPEC536, 399 A15-1 The role of group reproduction in group adaptation, 413 A15-2 The rise, fall, and destruction of a simple undifferentiated group, 414 A15-3 A putative life cycle for mat-forming bacteria, 417 A16-1 Site-specific distributions of bacterial phyla in healthy humans, 433 A16-2 Patterns of human-associated microbial diversity, 434 A16-3 Relationships between bacterial 16S rRNA gene sequences from the intestinal microbiota of animals, 435 A16-4 Adaptive landscapes, 438 A17-1 Heat map displaying the relative abundance of refOTUs in three prominent clades of bacteria, 452 A17-2 Three measures of biological diversity for samples, 455 A17-3 PCoA of unweighted UniFrac distances, a phylogenetically aware measure of intersample () diversity, 456 A17-4 Distance-based redundancy analysis of BrayCurtis intersample distances calculated with log2-transformed abundance data, 459 A19-1 Chemical structures of bacterial and host signals, 486 A19-2 Mammalian signalling through membrane receptors, 487 A19-3 Adrenergic sensing in enterohaemorrhagic Escherichia coli, 492 A19-4 AHL inter-kingdom signalling, 496 A20-1 D. discoideum fruiting bodies on an agar plate, 513 A20-2 Colony cycles of D. discoideum, 514 A20-3 In the social stage, clones may take advantage of their partner in three different ways, 517 A20-4 Conflict is manifested in chimeras in the form of shorter stalk lengths, shorter migration distances, and unequal spore/stalk ratios, 518 A20-5 Cheating can be controlled in the social stage if fruiting bodies are clonal, as might happen if they arise from different patches, 521 A21-1 The chemical structures of known luciferins, 535 A21-2 The bacterial bioluminescence reaction, 536

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TABLES, FIGURES, AND BOXES xxvii A21-3 Pinecone fish, 536 A21-4 Female anglerfish with attached male, 537 A21-5 Fire shooter squid, 538 A21-6 The life-cycle of the nematode host of the bioluminescent bacterium Photorhabdus luminescens, 541 A22-1 The two-group model of the intestinal microbiota with antibiotic- sensitive and antibiotic-tolerant bacteria, 548 A22-2 Multistability and hysteresis in a simple model of the intestinal microbiota, 551 A22-3 Most probable microbiota states change from bistable scenario to mono-stable coexistence with increasing noise, 553 A22-4 Microbiota resident time in antibiotic-tolerant domination as a function of the: antibiotic action () and social interaction () parameters, 555 A22-5 Analysis of microbiota response to the antibiotic ciprofloxacin from three subjects using singular value decomposition identifies antibiotic- sensitive and antibiotic-tolerant bacteria, 557 A22-SI Vectorial field of forces and the phase-plane analysis for bistable conditions, 571 A22-S2 Model nullclines analysis in the absence of noise, 572 A22-S3 Normalized-to-one areas of the basins of attraction, corresponding to sensitives (green curve) and tolerants (red curve), versus the antibiotic- killing y (A) or the social interaction e (B), 573 A22-S4 Time evolution of the sensitive (green) and tolerant (red) densities obtained by solving the Langevin equations for f = 1.1, y = 0.7, e variable with time (see Panel A) and three different noise regimes, 573 A22-S5 A: most probable bacterial density r change with respect the noise parameter D when the boundary condition are fixed at negative values far enough from the location of the stable states; B: plot of four different stationary distributions, 574 A22-S6 Stationary path connecting the stable points 1 and 2, 575 A22-S7 Plot of the correlation with principal component 2 (PC2) versus correlation with principal component 1 (PC1) for all the phylotypes detected in each subjects (A-C), 576 A22-S8 Log2 abundance versus samples for all the phylotypes detected in each subject (A-C), 577 A22-S9 Ordination plot of the time samples based on their first two principal components, 578

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xxviii TABLES, FIGURES, AND BOXES BOXES WO-1 Microbiome Research Projects, 27 WO-2 Biologically Inspired Computing Algorithms, 84 A2-1 Ecological and evolutionary dynamics in structured environments, 119 A6-1 Questions During Talk, 200 A15-1 Model for the Development of a Single Mat, 418 A15-2 Adaptive Developmental Programs in Mat Populations, 420 A19-1 Questions for Future Research, 502