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Workshop Overview1 THE SOCIAL BIOLOGY OF MICROBIAL COMMUNITIES Introduction Beginning with the germ theory of disease in the 19th century and extending through most of the 20th century, microbes2 were believed to live their lives as solitary, unicellular, disease-causing organisms (Losick and Kaiser, 1997). This perception stemmed from the focus of most investigators on organisms that could be grown in the laboratory as cellular monocultures, often dispersed in liquid, and under ambient conditions of temperature, lighting, and humidity (Kolter and Greenberg, 2006). Most such inquiries were designed to identify microbial pathogens by satisfying Koch's postulates.3 This pathogen-centric approach to the study of microorganisms produced a metaphorical "war" against these microbial invaders waged with antibiotic therapies, while simultaneously obscuring the 1 The planning committee's role was limited to planning the workshop, and the workshop summary has been prepared by the workshop rapporteurs (with the assistance of Pamela Bertelson, Rebekah Hutton, and Katherine McClure) as a factual summary of what occurred at the workshop. Statements, recommendations, and opinions expressed are those of individual presenters and participants, and are not necessarily endorsed or verified by the Institute of Medicine, and they should not be construed as reflecting any group consensus. 2 Microscopic organisms, including bacteria, archaea, fungi, protists, and viruses. 3 Koch's postulates must be satisfied in order to state that a particular microbe causes a specific infectious disease. They include the following: (i) The parasite occurs in every case of the disease in question and under circumstances which can account for the pathological changes and clinical course of the disease. (ii) The parasite occurs in no other disease as a fortuitous and nonpathogenic parasite. (iii) After being fully isolated from the body and repeatedly grown in pure culture, the parasite can induce the disease anew (Fredricks and Relman, 1996; Koch, 1891; Rivers, 1937). 1
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2 THE SOCIAL BIOLOGY OF MICROBIAL COMMUNITIES dynamic relationships that exist among and between host organisms and their associated microorganisms--only a tiny fraction of which act as pathogens. A recent revolution in our collective understanding of microbes is that the vast majority of these organisms live in communities and lead intensely interac- tive lives, competing, cooperating, and forming associations with one another and with their living and nonliving host environments. As the earth's first living inhabitants, communities4 of microorganisms have had several billion years to coevolve and adapt to one another and their environments, resulting in a world of spectacular diversity and interdependence. Indeed, microbial communities are intricately intertwined with all ecosystems on Earth--from the extreme environ- ments of the human gut to deep-sea hydrothermal vents and the windswept plains of Antarctica. This ecological view of microbial life has enormous potential for transform- ing our understanding of the world around us. Recent research on the communi- ties of microorganisms that live in and on us (the human microbiome) suggests that many traits once assumed to be "human"--such as the digestion of certain foods or the ability to defend against disease--may result from human-microbe interactions (Dethlefsen et al., 2007; IOM, 2006). Such findings have dispelled the notion that "human beings are physiological islands, entirely capable of regu- lating [our] own internal workings" and replaced it with the notion of the human body as a complex ecosystem (Ackerman, 2012). This realization "promises to radically alter the principles and practices of medicine, public health, and basic science" (Relman, 2012). Recognition of the ubiquity and importance of microbial communities not only advances an ecological view of microbial life but also raises intriguing questions about the formation of groups that behave collectively in ways that have consequences for their individual members. There is mounting evidence to suggest that molecular "conversations" take place among members of a broad spectrum of microbial communities, and also between a variety of microbes and host organisms. Having only recently become aware that such conversations ex- ist at all, our ability to eavesdrop on them and to translate them into scientific knowledge can be described as rudimentary at best. Yet, there is the emerging sense that microbes interact in complex, diverse, and subtle ways that we have yet to fully appreciate, much less understand. Despite their obvious importance, very little is actually known about the processes and factors that influence the assembly, function, and stability of mi- crobial communities. Gaining this knowledge will require a seismic shift away from the study of individual microbes in isolation to inquiries into the nature of diverse and often complex microbial communities, the forces that shape them, 4 For the purposes of this overview, and as suggested by speaker Joan Strassmann of Washington University at St. Louis, "microbial community" simply means "all the small forms of life occurring in the same place and time, where same implies a shared place, with some possibility they will encounter each other, or take resources the other might have used."
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WORKSHOP OVERVIEW 3 and their relationships with other communities and organisms, including their multicellular hosts. Statement of Task5 On March 6 and 7, 2012, the Institute of Medicine's (IOM's) Forum on Mi- crobial Threats hosted a public workshop to explore the emerging science of the "social biology" of microbial communities. Workshop presentations and discus- sions embraced a wide spectrum of topics, experimental systems, and theoretical perspectives representative of the current, multifaceted exploration of the micro- bial frontier. Participants discussed ecological, evolutionary, and genetic factors contributing to the assembly, function, and stability of microbial communities; how microbial communities adapt and respond to environmental stimuli; theo- retical and experimental approaches to advance this nascent field; and potential applications of knowledge gained from the study of microbial communities for the improvement of human, animal, plant, and ecosystem health and toward a deeper understanding of microbial diversity and evolution. Organization of the Workshop Summary This workshop summary was prepared by the rapporteurs for the Forum's members and includes a collection of individually authored papers and com- mentary. Sections of the workshop summary not specifically attributed to an individual reflect the views of the rapporteurs and not those of the members of the Forum on Microbial Threats, its sponsors, or the IOM. The contents of the unattributed sections of this summary report provide a context for the reader to appreciate the presentations and discussions that occurred over the 2 days of this workshop. The summary is organized into sections as a topic-by-topic description of the presentations and discussions that took place at the workshop. Its purpose is 5 The original Statement of Task stated the following: An ad hoc committee will plan and conduct a public workshop that will feature invited presentations and discussions to explore the scientific and policy implications of the microbiome in health and disease. Topics to be discussed may include, but are not limited to, the social behavior of microorganisms to form and maintain stable communities; how the use of antibiotics and other drugs can influence the community composition of the microbiome; microbial evolution and co-adaptation; an exploration of the various microbiomes in mammalian/terrestrial/aquatic environments; and the impacts of globalization on the introduction, establishment and evolution of "novel" diseases in established microbial communities. In the course of planning this workshop, the planning committee decided to focus the workshop's agenda on "the ecological, evolutionary, and genetic factors contributing to the assembly, function, and stability of microbial communities; how microbial communities adapt and respond to environmental stimuli; theoretical and experimental approaches to advance this nascent field; and potential applications of knowledge gained from the study of microbial communities for the improvement of human, animal, plant, and ecosystem health and toward a deeper understanding of microbial diversity and evolution."
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4 THE SOCIAL BIOLOGY OF MICROBIAL COMMUNITIES to present information from relevant experience, to delineate a range of pivotal issues and their respective challenges, and to offer differing perspectives on the topic as discussed and described by the workshop participants. Manuscripts and reprinted articles submitted by workshop participants may be found, in alphabeti- cal order, in Appendix A. Although this workshop summary provides a description of the individual presentations, it also reflects an important aspect of the Forum's philosophy. The workshop functions as a dialogue among representatives from different sectors and allows them to present their views about which areas, in their opinion, merit further study. This report only summarizes the statements of participants at the workshop over the course of 2 consecutive days. This workshop summary is not intended to be an exhaustive exploration of the subject matter nor does it rep- resent the findings, conclusions, or recommendations of a consensus committee process. Glimpses of Microbial Community Dynamics "We have to get away from this monolithic, one-dimensional perspec- tive of a one bugone-disease picture of health. The community is the unit of study." --David Relman (Buchen, 2010) "One reason we may have a hard time remembering that all microbes exist in communities is due to an early focus of scientists on microbes that cause disease." --Joan Strassmann (2012a) Observations of bacteria grown in the artificially simple environments of the Petri dish and the test tube have provided detailed knowledge of the physiology and cellular processes of organisms amenable to such culturing techniques (Little et al., 2008). With the recent development of "culture-independent" methods of microbial characterization,6 researchers have determined that such culturable species represent only a minuscule fraction of the microbial diversity around us. These techniques have further revealed the dynamic communities that the vast majority of microorganisms shape and inhabit--from simple communities composed of one to two species to complex, spatially diversified, host-associated communities comprising hundreds of species (Handelsman, 2004; Little et al., 2008; Nee, 2004). This workshop's focus on the community as the unit of study continues the Forum's exploration of "a more realistic and detailed picture of the dynamic 6 Various "culture-independent" techniques are discussed in the section "The Structure and Func- tion of Microbial Communities (see page 25)."
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WORKSHOP OVERVIEW 5 interactions among and between host organisms and their diverse populations of microbes" (IOM, 2006, 2009). Newly recognized as social organisms, microbes also provide a fresh lens through which to view interactions both among and between species. Studies of such interactions among multicellular organisms in- form the disciplines of social biology7 and ecology.8 While theoretical constructs derived from observations of the macroscopic world offer ways to interpret mi- crobial interactions, it is also possible that these phenomena will require novel explanatory frameworks. Microbial Communities in Biotic and Abiotic Environments The following descriptions of microbial communities, adapted to several distinct habitats, provide glimpses of microbes interacting with each other and with their environments, and reveal collective functions that exceed the capabili- ties of individual members. Biofilms The vast majority of microbes form and inhabit biofilms: complex, differentiated aggregations, typically of multiple species, that thrive on nearly every surface (Hall-Stoodley et al., 2004; Kolter and Greenberg, 2006; Parsek and Greenberg, 2005). Surrounded by a self-produced polymeric matrix,9 biofilms are characterized by structural heterogeneity, genetic diversity, and complex commu- nity interactions, as shown in Figure WO-1. For example, the microbial constitu- ents of the biofilm known as dental plaque include hundreds of species and strains of bacteria, as well as various methanogens (archaea) whose collective metabolic activities are associated with tooth decay (Lepp et al., 2004; Relman, 2005). By analogy to human communities, biofilms are organized into divisions of labor, with individual cells taking on specific tasks (Kolter and Greenberg, 2006). The structure of biofilms protects resident organisms from environmental extremes such as ultraviolet light, toxins (including antibiotics), pH, and de- hydration--advantages that may have allowed the first microbes to populate Earth's surface--as well as from host immune defenses (e.g., phagocytosis) and predation (Hall-Stoodley et al., 2004). The matrix polymer surrounding biofilms can store water and nutrients, and some biofilms have networks of channels that enable these resources to be distributed (IOM, 2011; Kolter and Greenberg, 2006; Stewart and Franklin, 2008). In medical settings, biofilms contribute to hospital-acquired infections, most notably by colonizing in-dwelling medical devices such as catheters and 7 The study of interactions within communities of single species. 8 The study of organisms' interactions with each other and with their environment. 9 Cells in a biofilm secrete polymers of varying chemical composition that form an extracellular polymeric substance (EPS) or a slime matrix that gives the biofilm stability and helps it to adhere to a surface. Although generally assumed to be primarily composed of polysaccharides, the EPS can also contain proteins and nucleic acids (Hall-Stoodley et al., 2004).
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6 FIGURE WO-1 Microbial biofims: Sticking together for success. Single-celled microbes readily form communities in resilient structures that provide advantages of multi cellular organization. This schematic was drawn by Peg Dirckx from the Center for Biofilm Engineering to incorporate various biofilm behaviors and concepts based largely on observations from confocal and time- lapse microscopy. An interactive version can be found at http:// www.erc.montana.edu/ MultiCellStrat/default. html. SOURCE: MSU Center for Biofilm Engineering, P. Dirckx. Figure WO-1.eps landscape, bitmap
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WORKSHOP OVERVIEW 7 prostheses (Hall-Stoodley et al., 2004; Kolter and Greenberg, 2006). According to Freemont (IOM, 2011), bacteria within established biofilm communities have been shown to tolerate antimicrobial agents at concentrations as high as 1,000 times the dosage needed to kill genetically equivalent bacteria in liquid culture. Bacterial biofilms may also make certain infections, such as those found in chronic wounds and the respiratory tract of individuals with cystic fibrosis, very difficult to treat (Hall-Stoodley et al., 2004). Multicellular structures for migration and dispersal The lifecycle of several types of microbes--including algae of the order Volvocales, social amoebae 10 of the order Dictyosteliida, and more than 50 species of Myxobacteria 11-- contain stages in which these usually unicellular organisms aggregate to form multicel- lular structures (Brock et al., 2011; Kaiser, 2006; Strassmann and Queller, 2011). When the unicellular stage of the social amoeba Dictyostelium discoideum runs out of bacteria to prey upon, tens of thousands of amoebae aggregate into a mul- ticellular migratory slug (Brock et al., 2011; Kuzdzal-Fick et al., 2011). It moves toward light and, once in a suitable location, the slug transforms into a fruiting body, a process during which one in five cells die in order to form the structure's sterile stalk. The stalk aids in the dispersal of the remaining cells, which differ- entiate into spores. The social biology of D. discoideum is further discussed in Control of cheating in the social amoeba and Farming of bacteria. Myxobacteria xanthus undergoes a similar transformation when nutrients are scarce, aggregating into groups of more than 100,000 cells that then form elaborate fruiting bodies for spore dispersal as illustrated in Figure WO-2. Chemi- cal and cell-contact signals have been found to coordinate developmental gene expression with cellular movement, leading to the construction of fruiting bodies in this bacterium (Kaiser, 2006). The bacterium and the squid The Hawaiian squid Euprymna scolopes forms a persistent association with the Gram-negative luminous bacterium Vibrio fischeri (Nyholm and McFall-Ngai, 2004). Incorporated into the squid's light organ, the bacterium emits luminescence that resembles moonlight and starlight filtering through ocean waters, camouflaging the nocturnal squid from predators (Figure WO-3) (Nyholm and McFall-Ngai, 2004). The forces supporting the formation and stability of this association were discussed by several workshop speakers. V. fischeri is the exclusive partner of the host squid in a special adaptation of the squid's light organ. Colonization of the squid's light organ by the bacterium 10 Although they are amoeboid protists, not fungi, members of this order are commonly known as "cellular slime molds." 11 Any of numerous Gram-negative, rod-shaped saprophytic bacteria (deriving nourishment from dead or decaying organic matter) of the phylum Myxobacteria, typically found embedded in slime in which they form complex colonies and noted for their ability to move by gliding along surfaces without any known organ of locomotion.
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8 THE SOCIAL BIOLOGY OF MICROBIAL COMMUNITIES FIGURE WO-2 Myxobacteria build multicellular fruiting bodies. Each of the 50 species of myxobacteria inherits a plan to build a morphologically different fruiting body. Fruiting Figure WO-2.eps bodies are 100 to 400 microns high and contain about 100,000 terminally differentiated spores. bitmap SOURCE: Kaiser (2006). begins within an hour after hatching and appears to occur in stages, as shown in Figure WO-4, with each step enabling greater specificity between host and symbi- ont. Once established, V. fischeri drives the development of the tissues with which they associate, inducing the maturation of the squid's light organ from a morphol- ogy that promotes colonization to one that promotes the maintenance of an exclu- sive association with V. fischeri through the life of the host (McFall-Ngai et al., 2012). Up to 95 percent of the resident symbiont population is expelled each day at dawn, followed by daily regrowth of bacteria within the crypts (McFall-Ngai
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WORKSHOP OVERVIEW 9 A B C D FIGURE WO-3 The bacterium and the squid. A persistent, symbiotic association be- tween the squid Euprymna scolopes (A) and its luminous bacterial symbiont Vibrio fischeri (B) forms within the squid'sFigure WO-3 light organ (C and D). After colonization of the host's light organ tissue, V. fischeri induces a series of irreversible developmental changes that trans- form these tissues into a mature, functional light organ (Nyholm and McFall-Ngai, 2004). SOURCE: (A) Images taken by C. Frazee, provided by M. McFall-Ngai and E. G. Ruby; (B) Image provided courtesy of Marianne Engel; (C and D). Reprinted by permission from Macmillan Publishers Ltd: Nature, Dusheck (2002), copyright 2002. et al., 2012). This simple model of persistent colonization of animal epithelia by Gram-negative bacteria provides a "valuable complement to studies of both beneficial and pathogenic consortial interactions, such as in the mammalian in- testine, and chronic disease that involve persistent colonization by Gram-negative bacteria, such as cystic fibrosis" (Nyholm and McFall-Ngai, 2004). Plant roots and their partners Plants establish associations with several micro- organisms in a relationship somewhat analogous to that of mammals with their gastrointestinal microbiota. The roots of most higher plant species form mycor- rhizae, an association with specific fungal species that significantly improves the plant's ability to acquire phosphorous, nitrogen, and water from the soil. 12 A few plant families, including legumes, associate with nitrogen-fixing bacteria. They colonize the plant's roots and form specialized nodules, where the bacteria 12 See http://agronomy.wisc.edu/symbiosis.
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10 THE SOCIAL BIOLOGY OF MICROBIAL COMMUNITIES FIGURE WO-4 The winnowing. This model depicts the progression of light-organ colo- nization as a series of steps, each more specific for symbiosis-competent Vibrio fischeri. (a) In response to Gram-positive Figure WO-4.eps and Gram-negative bacteria (alive or dead) the bacterial peptidoglycan signal causes the cells of bitmap the ciliated surface epithelium to secrete mucus. (b) Only viable Gram-negative bacteria form dense aggregations. (c) Motile or nonmotile V. fischeri out-compete other Gram-negative bacteria for space and become dominant in the aggregations. (d) Viable and motile V. fischeri are the only bacteria that are able to migrate through the pores and into the ducts to colonize host tissue. (e) Following successful coloni- zation, symbiotic bacterial cells become nonmotile and induce host epithelial cell swelling. Only bioluminescent V. fischeri will sustain long-term colonization of the crypt epithelium. SOURCE: Reprinted by permission from Macmillan Publishers Ltd: Nature Reviews Microbiology, Nyholm and McFall-Ngai (2004), copyright 2004. receive energy from the plant and convert atmospheric nitrogen to ammonia, which the plant can then assimilate into amino acids, nucleotides, and other cel- lular constituents (Desbrosses and Stougaard, 2011). This partnership furnishes much of Earth's biologically available nitrogen,13 a key contributor to agricultural productivity that has long been achieved by growing legumes in rotation with nonlegume crops. 13Nitrogen is a critical nutrient for plants, but often it is not readily available in soil, hence the extensive use in agriculture of chemical fertilizers containing nitrogen.
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WORKSHOP OVERVIEW 11 Partnerships between plant roots and microbes are established through chem- ical and genetic "cross-talk." During nodule formation, legume roots release flavonoid compounds that trigger nitrogen-fixing Rhizobium bacteria to express modified chitin oligomers known as nodulation (Nod) factors, which in turn facilitate infection of the root by the bacteria, as well as nodule development (Desbrosses and Stougaard, 2011; Ferguson et al., 2010; Long, 2001; Riely et al., 2006) (see Figure WO-5). Other plants produce chemical signals called strigolactones that increase their contact with arbuscular mycorrhizal fungi; this triggers the fungi to release diffusible factors that, when recognized by the plant, activate genes collectively known as Myc factors (Parniske, 2008). Both Nod and Myc factors promote plant growth, which may benefit microbes by increasing the availability of infection sites (IOM, 2009). Microbial inhabitants of the human gut Just as microbes colonize the bobtail squid's light organ shortly after hatching, microbes colonize the human body internally and externally during its first weeks to years of life and establish themselves in relatively stable communities in various microhabitats (Costello et al., 2012; Dethlefsen et al., 2007). Research to date suggests that the site-specific microbial communities--known as microbiota or microbiomes14--that inhabit the skin, intestinal lumen, mouth, vagina, etc., contain characteristic microbial FIGURE WO-5 An example of nitrogen-fixing symbiosis between legumes and rhizobia bacteria. SOURCE: Provided courtesy of Jean-Michel Ané, University of Wisconsin, Madison. 14The term microbiome is attributed to the late Joshua Lederberg, who suggested that a comprehensive genetic view of the human as an organism should include the genes of the human microbiome (Hooper and Gordon, 2001). Because most of the organisms that make up the microbiome are known only by their genomic sequences, the microbiota and the microbiome are from a practical standpoint largely one and the same (IOM, 2009).
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86 THE SOCIAL BIOLOGY OF MICROBIAL COMMUNITIES this information, he and colleagues searched for and found beetle-associated, antibiotic-producing Actinobacteria that mediate this fungal community, inhibit- ing O. minus without similarly affecting Entomocorticium (Scott et al., 2008). Another species of Actinobacteria they have isolated from honeybees produces a small- molecule antagonist to Paenibacillus larvae, the bees' major bacterial pathogen. In total, Currie and coworkers have identified seven novel small mol- ecules from Actinobacteria associated with insects; some of which are currently being tested as potential drug leads. Microbial Roles in Health Insights into microbial interactions--and ways to disrupt them--could lead to new therapeutic approaches. Current approaches to infection, such as antibiot- ics and other antimicrobials, are nonspecific and create strong selective pressures for the development of resistance (Xavier, 2011). Targeting social strategies that underlie virulence, or the mechanisms by which microorganisms become pathogenic within certain environments may prove a more efficient and effective means to treat disease (Brown et al., 2009; Rasko and Sperandio, 2010). Indeed, a more ecologically-informed view of antibiotic production and resistance in bacteria may lead to new approaches to treat bacterial infections. While antibiotic resistance is generally thought to be driven by brief, cyclic invasions of popula- tions by antibiotic-producing and antibiotic-resistant bacteria, recent research suggests that non-clonal communities of bacteria in structured, wild habitats use cooperation as a strategy in antibiotic-mediated competition with neighboring populations (Cordero et al., 2012). Reflecting the concept of "ecological context dependence," noted by Currie and many others throughout the workshop, this research suggests that within a population, only a few members produce the antibiotic to which all others are resistant, creating interaction networks within and between populations that prevent invasion while also maintaining diversity (Cordero et al., 2012; Morlon, 2012). As noted by Dethlefsen et al. (2007), it is "crucial to consider the role of microbial communities, and not just individual species, as pathogens and mu- tualists." Recent investigations have revealed links between altered microbiota ecology (dysbiosis) and infectious and noninfectious diseases alike. These obser- vations have prompted calls to transition clinical practice from "the body-as-a- battleground to the human-as-habitat perspective" and to consider system-level, adaptive management approaches to managing health. Adaptive management approaches are used to "manage biodiversity in a variety of habitats, including communities in highly disturbed environments affected by overfishing and by climate change" (Costello et al., 2012). This approach may better reflect health as "a product of ecosystem services provided by microbial communities" and would require the development of new diagnostic tools to inform health management decisions (Costello et al., 2012).
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WORKSHOP OVERVIEW 87 Relman observed that "there are all sorts of promises that are dangling out there in front of us in the way of diagnostics and predictive aspects of medicine. There is a lot of as yet unrealized potential and as yet unrealized promise." Early investigations have revealed that there is a great deal left to discover about the patterns of microbial diversity in humans and the stability of these populations, particularly in the face of perturbations (i.e., resilience). This ecological perspec- tive will likely provide new leads for the management of disease. Indeed, as noted by Lita Proctor, a program director of the Human Microbiome Project, "unlike the human genome, the microbiome is changeable; and it is this changeability that holds promise for prevention and treatment of disease" (Balter, 2012). The increased recognition of the beneficial as well as benign host-microbe relationships will further drive the paradigm shift--in the way we collectively identify and think about the microbial world around us--first suggested by Joshua Lederberg more than two decades ago. The familiar "war metaphor" in which the only good bug is a dead bug will be replaced with a more ecologically informed view of the dynamic relationships within and between hosts, their microbiomes, and their environments (Lederberg, 2000). This perspective recognizes that mi- crobes and their hosts ultimately depend upon one another for survival and en- courages the exploration and exploitation of these ecological relationships in order to improve human, animal, plant, and environmental health and well-being (Lederberg, 2000). WORKSHOP OVERVIEW REFERENCES Ackerman, J. 2012. The ultimate social network. Scientific American, June 27-43. American Heritage Science Dictionary, 1st Edition. 2011. Boston: Houghton Mifflin Harcourt. Anderson, P. W. 1972. More is different. Science 177(4047):393-396. Aoki, S. K., E. J. Diner, C. T. de Roodenbeke, B. R. Burgess, S. J. Poole, B. A. Braaten, A. M. Jones, J. S. Webb, C. S. Hayes, P. A. Cotter, and D. A. Low. 2010. A widespread family of polymorphic contact-dependent toxin delivery systems in bacteria. Nature 468(7322):439-442. Aoki, S. K., S. J. Poole, C. S. Hayes, and D. A. Low. 2011. Toxin on a stick: Modular CDI toxin delivery systems play roles in bacterial competition. Virulence 2(4):356-359. Arumugam, M., J. Raes, E. Pelletier, D. Le Paslier, T. Yamada, D. R. Mende, G. R. Fernandes, J. Tap, T. Bruls, J. M. Batto, M. Bertalan, N. Borruel, F. Casellas, L. Fernandez, L. Gautier, T. Hansen, M. Hattori, T. Hayashi, M. Kleerebezem, K. Kurokawa, M. Leclerc, F. Levenez, C. Manichanh, H. B. Nielsen, T. Nielsen, N. Pons, J. Poulain, J. Qin, T. Sicheritz-Ponten, S. Tims, D. Torrents, E. Ugarte, E. G. Zoetendal, J. Wang, F. Guarner, O. Pedersen, W. M. de Vos, S. Brunak, J. Dore, M. Antolin, F. Artiguenave, H. M. Blottiere, M. Almeida, C. Brechot, C. Cara, C. Chervaux, A. Cultrone, C. Delorme, G. Denariaz, R. Dervyn, K. U. Foerstner, C. Friss, M. van de Guchte, E. Guedon, F. Haimet, W. Huber, J. van Hylckama-Vlieg, A. Jamet, C. Juste, G. Kaci, J. Knol, O. Lakhdari, S. Layec, K. Le Roux, E. Maguin, A. Merieux, R. Melo Minardi, C. M'Rini, J. Muller, R. Oozeer, J. Parkhill, P. Renault, M. Rescigno, N. Sanchez, S. Sunagawa, A. Torrejon, K. Turner, G. Vandemeulebrouck, E. Varela, Y. Winogradsky, G. Zeller, J. Weissenbach, S. D. Eh- rlich, and P. Bork. 2011. Enterotypes of the human gut microbiome. Nature 473(7346):174-180.
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