Click for next page ( 2


The National Academies | 500 Fifth St. N.W. | Washington, D.C. 20001
Copyright © National Academy of Sciences. All rights reserved.
Terms of Use and Privacy Statement



Below are the first 10 and last 10 pages of uncorrected machine-read text (when available) of this chapter, followed by the top 30 algorithmically extracted key phrases from the chapter as a whole.
Intended to provide our own search engines and external engines with highly rich, chapter-representative searchable text on the opening pages of each chapter. Because it is UNCORRECTED material, please consider the following text as a useful but insufficient proxy for the authoritative book pages.

Do not use for reproduction, copying, pasting, or reading; exclusively for search engines.

OCR for page 1
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

OCR for page 1
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."

OCR for page 1
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."

OCR for page 1
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)."

OCR for page 1
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).

OCR for page 1
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

OCR for page 1
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.

OCR for page 1
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

OCR for page 1
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.

OCR for page 1
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.

OCR for page 1
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 An, 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).

OCR for page 1
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).

OCR for page 1
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.

OCR for page 1
88 THE SOCIAL BIOLOGY OF MICROBIAL COMMUNITIES Aylward, F. O., K. E. Burnum, J. J. Scott, G. Suen, S. G. Tringe, S. M. Adams, K. W. Barry, C. D. Nicora, P. D. Piehowski, S. O. Purvine, G. J. Starrett, L. A. Goodwin, R. D. Smith, M. S. Lipton, and C. R. Currie. 2012. Metagenomic and metaproteomic insights into bacterial communities in leaf-cutter ant fungus gardens. ISME Journal. Epub ahead of print. Balter, M. 2012. Taking stock of the human microbiome and disease. Science 336:1246-1247. Banfield, J. 2012. Session IV: Microbial community assembly and dynamics: From acidophilic bio- films to the premature infant gut. Paper presented at the Forum on Microbial Threats Workshop, The Social Biology of Microbial Communities, Washington, DC, March 7. Bassler, B. L., and R. Losick. 2006. Bacterially speaking. Cell 125(2):237-246. Belt, T. 1874. The naturalist in Nicaragua. London: E. Bumpus. Ben-Jacob, E., Y. Aharonov, and Y. Shapira. 2004. Bacteria harnessing complexity. Biofilms 1:239-263. Bonachela, J., C. Nadell, J. Xavier, and S. A. Levin. 2011. Universality in bacterial colonies. Journal of Statistical Physics 144:303-315. Bonner, J. T. 2010. Brainless behavior: A myxomycete chooses a balanced diet. Proceedings of the National Academy of Sciences of the United States of America 107(12):5267-5268. Brock, D. A., T. E. Douglas, D. C. Queller, and J. E. Strassmann. 2011. Primitive agriculture in a social amoeba. Nature 469(7330):393-396. Brockhurst, M. A., M. E. Hochberg, T. Bell, and A. Buckling. 2006. Character displacement promotes cooperation in bacterial biofilms. Current Biology 16(20):2030-2034. Brown, S. P. 2006. Cooperation: Integrating evolutionary and ecological perspectives. Current Biol- ogy 16(22):R960-R961. Brown, S. P., S. A. West, S. P. Diggle, and A. S. Griffin. 2009. Social evolution in micro-organisms and a Trojan horse approach to medical intervention strategies. Philosophical Transactions of the Royal Society of London B: Biological Sciences 364(1533):3157-3168. Brown, S. P., D. M. Cornforth, and N. Mideo. 2012. Evolution of virulence in opportunistic patho- gens: Generalism, plasticity, and control. Trends in Microbiology 20(7):336-342. Bucci, V., S. Bradde, G. Biroli, and J. B. Xavier. 2012. Social interaction, noise and antibiotic- mediated switches in the intestinal microbiota. PLoS Computational Biology 8(4):e1002497. Buchen, L. 2010. Microbiology: The new germ theory. Nature 468(7323):492-495. Buffie, C. G., I. Jarchum, M. Equinda, L. Lipuma, A. Gobourne, A. Viale, C. Ubeda-Morant, J. Xavier, and E. G. Pamer. 2011. Profound alterations of intestinal microbiota following a single dose of clindamycin results in sustained susceptibility to C. difficileinduced colitis. Infection and Immunity 80(1):63-73. Caetano, L., M. Antunes, J. E. Davies, and B. B. Finlay. 2011. Mining bacterial small molecules. The Scientist, January 1, 26-30. Caporaso, J. G., C. L. Lauber, E. K. Costello, D. Berg-Lyons, A. Gonzalez, J. Stombaugh, D. Knights, P. Gajer, J. Ravel, N. Fierer, J. I. Gordon, and R. Knight. 2011. Moving pictures of the human microbiome. Genome Biology 12(5):R50. Cash, H. L., C. V. Whitham, C. L. Behrendt, and L. V. Hooper. 2006. Symbiotic bacteria direct expres- sion of an intestinal bactericidal lectin. Science 313(5790):1126-1130. Cavanaugh, C. M., Z. P. McKiness, I. L. G. Newton, and F. J. Stewart. 2006. Marine chemosynthetic symbioses. Pp. 475-507 in The Prokaryotes, Vol. 1, edited by M. Dworkin et al. New York: Springer-Verlag. Available at http://link.springer-ny.com/link/service/books/10125. Clatworthy, A. E., E. Pierson, and D. T. Hung. 2007. Targeting virulence: A new paradigm for anti- microbial therapy. Nature Chemical Biology 3:541-548. Cordero, O. X. H. Wildschutte, B. Kirkup, S. Proehl, L. Ngo, F. Hussain, F. LeRoux, T. Mincer, and M. F. Polz. 2012. Ecological populations of bacteria act as socially cohesive units of antibiotic production and resistance. Science 337(6099):1228-1231. Costello, E. K., K. Stagman, L. Dethlefsen, B. J. M. Bohannan, and D. A. Relman. 2012. The ap- plication of ecological theory toward and understanding of the human microbiome. Science 336:1255-1262.

OCR for page 1
WORKSHOP OVERVIEW 89 Couzin, I. D., J. Krause, N. R. Franks, and S. A. Levin. 2005. Effective leadership and decision- making in animal groups on the move. Nature 433(7025):513-516. Couzin-Frankel, J. 2010. Bacteria and asthma: Untangling the links. Science 330(6008):1168-1169. Crespi, B. J. 2001. The evolution of social behavior in microorganisms. Trends in Ecology & Evolu- tion 16(4):178-183. Curtis, M. M., and V. Sperandio. 2011. A complex relationship: The interaction among symbiotic microbes, invading pathogens, and their mammalian host. Mucosal Immunology 4(2):133-138. Czyz, A., K. Plata, and G. Wegrzyn. 2003. Stimulation of DNA repair as an evolutionary drive for bacterial luminescence. Luminescence 18(3):140-144. Davis, R., and C. Joyce. 2011. The deep-sea finding that changed biology. NPR. http://www.npr .org/2011/12/05/142678239/the-deep-sea-find-that-changed-biology (accessed February 8, 2012). Denef, V. J., L. H. Kalnejais, R. S. Mueller, P. Wilmes, B. J. Baker, B. C. Thomas, N. C. VerBerkmoes, R. L. Hettich, and J. F. Banfield. 2010a. Proteogenomic basis for ecological divergence of closely related bacteria in natural acidophilic microbial communities. Proceedings of the National Academy of Sciences of the United States of America 107(6):2383-2390. Denef, V. J., R. S. Mueller, and J. F. Banfield. 2010b. AMD biofilms: Using model communities to study microbial evolution and ecological complexity in nature. ISME Journal 4(5):599-610. Desbrosses, G. J., and J. Stougaard. 2011. Root nodulation: A paradigm for how plant-microbe sym- biosis influences host developmental pathways. Cell Host & Microbe 10(4):348-358. Dethlefsen, L., and D. A. Relman. 2011. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proceedings of the National Academy of Sciences of the United States of America 108(Suppl 1):4554-4561. Dethlefsen, L., M. McFall-Ngai, and D. A. Relman. 2007. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449(7164):811-818. Dethlefsen, L., S. Huse, M. L. Sogin, and D. A. Relman. 2008. The pervasive effects of an antibi- otic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biology 6(11):e280. Diggle, S. P. 2010. Microbial communication and virulence: Lessons from evolutionary theory. Microbiology 156(Pt 12):3503-3512. Diggle, S. P., A. Gardner, S. A. West, and A. S. Griffin. 2007a. Evolutionary theory of bacterial quo- rum sensing: When is a signal not a signal? Philosophical Transactions of the Royal Society B: Biological Sciences 362(1483):1241-1249. Diggle, S. P., A. S. Griffin, G. S. Campbell, and S. A. West. 2007b. Cooperation and conflict in quorum-sensing bacterial populations. Nature 450(7168):411-414. Diner, E. J., C. M. Beck, J. S. Webb, D. A. Low, and C. S. Hayes. 2012. Identification of a target cell permissive factor required for contact-dependent growth inhibition (CDI). Genes & Develop- ment 26(5):515-525. Dubilier, N., C. Bergin, and C. Lott. 2008. Symbiotic diversity in marine animals: The art of harness- ing chemosynthesis. Nature Reviews Microbiology 6(10):725-740. Dunn, A., and J. Handelsman. 2002. Toward an understanding of microbial communities through analysis of communication networks. Antonie van Leeuwenhoek 81:565-574. Dusheck, J. 2002. It's the ecology, stupid! Nature 418(6898):578-579. Dussutour, A., T. Latty, M. Beekman, and S. J. Simpson. 2010. Amoeboid organism solves complex nutritional challenges. Proceedings of the National Academy of Sciences of the United States of America 107(10):4607-4611. Emmert, E. A., A. K. Klimowicz, M. G. Thomas, and J. Handelsman. 2004. Genetics of zwittermicin A production by Bacillus cereus. Applied Environmental Microbiology 70(1):104-113. Eppley, J. M., G. W. Tyson, W. M. Getz, and J. F. Banfield. 2007. Genetic exchange across a species boundary in the archaeal genus Ferroplasma. Genetics 177(1):407-416. Ferguson, B. J., A. Indrasumunar, S. Hayashi, M. H. Lin, Y. H. Lin, D. E. Reid, and P. M. Gresshoff. 2010. Molecular analysis of legume nodule development and autoregulation. Journal of Integra- tive Plant Biology 52(1):61-76.

OCR for page 1
90 THE SOCIAL BIOLOGY OF MICROBIAL COMMUNITIES Flores, J. F., C. R. Fisher, S. L. Carney, B. N. Green, J. K. Freytag, S. W. Schaeffer, and W. E. Royer, Jr. 2005. Sulfide binding is mediated by zinc ions discovered in the crystal structure of a hydro- thermal vent tubeworm hemoglobin. Proceedings of the National Academy of Sciences of the United States of America 102:2713-2718. Folke, C., S. Carpenter, B. Walker, M. Scheffer, T. Elmqvist, L. Gunderson, and C. S. Holling. 2004. Regime shifts, resilience, and biodiversity in ecosystem management. Annual Review of Ecol- ogy, Evolution, and Systematics 335:557-581. Fredricks, D. N., and D. A. Relman. 1996. Sequence-based identification of microbial pathogens: A reconsideration of Koch's postulates. Clinical Microbiology Reviews 9:18-33. Fukuyama J., P. J. McMurdie, L. Dethlefsen, D. A. Relman, and S. Holmes. 2012. Comparisons of distance methods for combining covariates and abundances in microbiome studies. Pacific Symposium on Biocomputing 2012:213-224. Fuqua, C., and E. P. Greenberg. 2002. Listening in on bacteria: Acyl-homoserine lactone signalling. Nature Reviews Molecular Cell Biology 3(9):685-695. Fuqua, C., S. C. Winans, and E.P. Greenberg. 1994. Quorum sensing in bacteria: The LuxR-LuxI fam- ily of cell density-responsive transcriptional regulators. Journal of Bacteriology 176(2):269-275. Gilbert, G. S., J. L. Parke, M. K. Clayton, and J. Handelsman. 1993. Effects of an introduced bacte- rium on bacterial communities on roots. Ecology 74:840-854. Gilbert, G. S., J. Handelsman, and J. L. Parke. 1994. Root camouflage and disease control. Phyto- pathology 84:222-225. Gilbert, G. S., M. K. Clayton, J. Handelsman, and J. L. Parke. 1996. Use of cluster and discriminant analysese to compare, rhizosphere bacterial communities following biological perturbation. Microbial Ecology 32:123-147. Gill, S. R., M. Pop, R. T. Deboy, P. B. Eckburg, P. J. Turnbaugh, B. S. Samuel, J. I. Gordon, D. A. Relman, C. M. Fraser-Liggett, and K. E. Nelson. 2006. Metagenomic analysis of the human distal gut microbiome. Science 312(5778):1355-1359. Gonzalez, A., J. C. Clemente, A. Shade, J. L. Metcalf, S. Song, B. Prithiviraj, B.E. Palmer, and R. Knight. 2011. Our microbial selves: What ecology can teach us. EMBO Reports 12:775-784. Hall-Stoodley, L., J. W. Costerton, and P. Stoodley. 2004. Bacterial biofilms: From the natural environ- ment to infectious diseases. Nature Reviews Microbiology 2(2):95-108. Hamilton, W. D. 1964. The genetical evolution of social behaviour. I-II. Journal of Theoretical Biol- ogy 7:1-52. Han, H., J. Hemp, L. A. Pace, H. Ouyang, K. Ganesan, J. H. Roh, F. Daldal, S. R. Blanke, and R. B. Gennis. 2011a. Adaptation of aerobic respiration to low O2 environments. Proceedings of the National Academy of Sciences of the United States of America 108(34):14109-14114. Han, S. W., M. Sriariyanun, S. W. Lee, M. Sharma, O. Bahar, Z. Bower, and P. C. Ronald. 2011b. Small protein-mediated quorum sensing in a gram-negative bacterium. PLoS One 6(12):e29192. Handelsman, J. 2004. Metagenomics: Application of genomics to uncultured microorganisms. Micro- biology and Molecular Biology Reviews 68(4):669-685. ------. 2007. Metagenomics and microbial communities. In Encyclopedia of life sciences. Chichester, UK: John Wiley & Sons. ------. 2009. Expanding the microbial universe: Metagenomics and microbial community dynamics. In Microbial evolution and co-adaptation. Washington, DC: The National Academies Press: A tribute to the life and scientific legacies of Joshua Lederburg: Workshop summary. Institute of Medicine. Harmer, T. L., R. D. Rotjan, A. D. Nussbaumer, M. Bright, A. W. Ng, E. G. DeChaine, and C. M. Cavanaugh. 2008. Free-living tube worm endosymbionts found at deep-sea vents. Applied and Environmental Microbiology 74(12):3895-3898. Hayes, C. S., S. K. Aoki, and D. A. Low. 2010. Bacterial contact-dependent delivery systems. Annual Review of Genetics 44:71-90. He, H., L. A. Silo-Suh, J. Clardy, and J. Handelsman. 1994. Zwittermicin A, an antifungal and plant protection agent from Bacillus cereus. Tetrahedron Letters 35:2499-2502.

OCR for page 1
WORKSHOP OVERVIEW 91 Holmes, E., J. V. Li, T. Athanasiou, H. Ashrafian, and J. K. Nicholson. 2011. Understanding the role of gut microbiome-host metabolic signal disruption in health and disease. Trends in Microbiol- ogy 19(7):349-359. Hooper, L. V., and J. I. Gordon. 2001. Commensal host-bacterial relationships in the gut. Science 292(5519):1115-1118. Hooper, L. V., D. R. Littman, and A. J. Macpherson. 2010. Interactions between the microbiota and the immune system. Science 336(6086):1268-1273. Hughes, D. T., and V. Sperandio. 2008. Inter-kingdom signalling: Communication between bacteria and their hosts. Nature Reviews Microbiology 6(2):111-120. Human Microbiome Jumpstart Reference Strains Consortium. 2010. A catalog of reference genomes from the human microbiome. Science 328(5981):994-999. Human Microbiome Project Consortium. 2012. Structure, function and diversity of the healthy human microbiome. Nature 486:207-214. Ingham, C. J., and E. Ben Jacob. 2008. Swarming and complex pattern formation in Paenibacillus vortex studied by imaging and tracking cells. BMC Microbiology 8:36. Ingham, C. J., O. Kalisman, A. Finkelshtein, and E. Ben-Jacob. 2011. Mutually facilitated dispersal between the nonmotile fungus Aspergillus fumigatus and the swarming bacterium Paenibacil- lus vortex. Proceedings of the National Academy of Sciences of the Untied States of America 108(49):19731-19736. IOM (Institute of Medicine). 2006. Ending the war metaphor: The changing agenda for unraveling the host-microbe relationship. Washington DC: The National Academies Press. ------. 2009. Microbial adaptation and co-evolution: A tribute to the life and scientific legacies of Joshua Lederberg. Washington, DC: Workshop summary. The National Academies Press. ------. 2011. The science and applications of synthetic and systems biology: Workshop summary. Washington, DC: The National Academies Press. Jernberg, C., S. Lofmark, C. Edlund, and J. K. Jansson. 2007. Long-term ecological impacts of anti- biotic administration on the human intestinal microbiota. ISME Journal 1:56-66. Kaiser, D. 2006. A microbial genetic journey. Annual Review of Microbiology 60:1-25. Kearns, D. B. 2010. A field guide to bacterial swarming motility. Nature Reviews Microbiology 8(9):634-644. King, R. 2011. A bacterial platoon with fungal engineers. New York Times. http://www.nytimes. com/2011/11/29/science/a-bacterial-platoon-with-fungi-engineers.html (accessed July 25, 2012). Koch, R. 1891. Uber bakteriologische Forschung Verhandlung des X Internationalen Medichinischen Congresses, Berlin, 1890, 1, 35. Berlin: August Hirschwald [in German]. Xth International Congress of Medicine, Berlin. Kolter, R., and E. P. Greenberg. 2006. Microbial sciences: The superficial life of microbes. Nature 441(7091):300-302. Kuzdzal-Fick, J. J., S. A. Fox, J. E. Strassmann, and D. C. Queller. 2011. High relatedness is neces- sary and sufficient to maintain multicellularity in Dictyostelium. Science 334(6062):1548-1551. Lederberg, J. 2000. Infectious history. Science 288(5464):287-293. Lee, Y. K., and S. K. Mazmanian. 2010. Has the microbiota played a critical role in the evolution of the adaptive immune system? Science 330(6012):1768-1773. Lepp, P. W., M. M. Brinig, C. C. Ouverney, K. Palm, G. C. Armitage, and D. A. Relman. 2004. Methanogenic archaea and human periodontal disease. Proceedings of the National Academy of Sciences of the United States of America 101(16):6176-6181. Levin, S. 1998. Ecosystems and the biosphere as complex adaptive systems. Ecosystems 1:431-436. Levin, S. A. 2006. Fundamental questions in biology. PLoS Biology 4(9):e300. Ley, R. E., D. A. Peterson, and J. I. Gordon. 2006a. Ecological and evolutionary forces shaping mi- crobial diversity in the human intestine. Cell 124(4):837-848. Ley, R. E., P. J. Turnbaugh, S. Klein, and J. I. Gordon. 2006b. Microbial ecology: Human gut microbes associated with obesity. Nature 444(7122):1022-1023.

OCR for page 1
92 THE SOCIAL BIOLOGY OF MICROBIAL COMMUNITIES Little, A. E., and C. R. Currie. 2008. Black yeast symbionts compromise the efficiency of antibiotic defenses in fungus-growing ants. Ecology 89(5):1216-1222. Little, A. E., C. J. Robinson, S. B. Peterson, K. F. Raffa, and J. Handelsman. 2008. Rules of engage- ment: Interspecies interactions that regulate microbial communities. Annual Review of Micro- biology 62:375-401. Littman, D. R., and E. G. Pamer. 2011. Role of the commensal microbiota in normal and pathogenic host immune responses. Cell Host & Microbe 10(4):311-323. Long, S. R. 2001. Genes and signals in the Rhizobium-legume symbiosis. Plant Physiology 125(1): 69-72. Losick, R., and D. Kaiser. 1997. Why and how bacteria communicate. Scientific American 276(2): 68-73. Lysenko, E. S., R. S. Lijek, S. P. Brown, and J. N. Weiser. 2010. Within-host competition drives selection for the capsule virulence determinant of streptococcus pneumoniae. Current Biology 20(13):1222-1226. Maier, R. M., I. L. Pepper, and C. P. Gerba. 2000. Environmental microbiology. San Diego: Academic Press. Maloy, S., J. Handelsman, and S. Singh. 2011. Dynamics of host-associated microbial communities. Microbe 6(1):21-25. Marteyn, B., N. P. West, D. F. Browning, J. A. Cole, J. G. Shaw, F. Palm, J. Mounier, M. C. Prevost, P. Sansonetti, and C. M. Tang. 2010. Modulation of Shigella virulence in response to available oxygen in vivo. Nature 465(7296):355-358. Marwan, W. 2010. Amoeba-inspired network design. Science 327(5964):419-420. Matson, E. G., X. Zhang, and J. R. Leadbetter. 2010. Selenium controls transcription of paralogous formate dehydrogenase genes in the termite gut acetogen, Treponema primitia. Environmental Microbiology 12:2245-2258. May, R. M., S. A. Levin, and G. Sugihara. 2008. Complex systems: Ecology for bankers. Nature 451(7181):893-895. McFall-Ngai, M., E. A. C. Heath-Heckman, A. A. Gillette, S. M. Peyer, and E. A. Harvie. 2012. The secret languages of coevolved symbioses: Insights from the Euprymna scolopesVibrio fischeri symbiosis. Seminars in Immunology 24:3-8. McGinty, S. E., D. J. Rankin, and S. P. Brown. 2010. Horizontal gene transfer and the evolution of bacterial cooperation. Evolution 65(1):21-32. Morlon, H. 2012. Microbial cooperative warfare. Science 337(6099):1184-1185. Morowitz, M. J., V. J. Denef, E. K. Costello, B. C. Thomas, V. Poroyko, D. A. Relman, and J. F. Banfield. 2010. Strain-resolved community genomic analysis of gut microbial colonization in a premature infant. Proceedings of the National Academy of Sciences of the United States of America 108(3):1128-1133. Mueller, R. S., V. J. Denef, L. H. Kalnejais, K. B. Suttle, B. C. Thomas, P. Wilmes, R. L. Smith, D. K. Nordstrom, R. B. McCleskey, M. B. Shah, N. C. Verberkmoes, R. L. Hettich, and J. F. Banfield. 2010. Ecological distribution and population physiology defined by proteomics in a natural microbial community. Molecular Systems Biology 6:374. Nadell, C. D., J. B. Xavier, and K. R. Foster. 2009. The sociobiology of biofilms. FEMS Microbiol- ogy Review 33(1):206-224. NASA (National Aeronautic and Atmospheric Administration). 2011. Mars science laboratory. http:// www.jpl.nasa.gov/news/fact_sheets/mars-science-laboratory.pdf (accessed May 20, 2012). Nee, S. 2004. More than meets the eye. Nature 429(6994):804-805. Nicholson, J. K., E. Holmes, and I. D. Wilson. 2005. Gut microorganisms, mammalian metabolism and personalized health care. Nature Reviews Microbiology 3(5):431-438. Nicholson, J. K., E. Holmens, J. Kinross, R. Burcelin, G.Gibson, W. Jia, and S. Pettersson. 2012. Host-gut microbiota metabolic interactions. Science 336:1262. Njoroge, J., and V. Sperandio. 2009. Jamming bacterial communication: New approaches for the treatment of infectious diseases. EMBO Molecular Medicine 1(4):201-210.

OCR for page 1
WORKSHOP OVERVIEW 93 Nogueira, T., D. J. Rankin, M. Touchon, F. Taddei, S. P. Brown, and E. P. Rocha. 2009. Horizontal gene transfer of the secretome drives the evolution of bacterial cooperation and virulence. Cur- rent Biology 19(20):1683-1691. NRC (National Research Council). 2007. Metagenomics: Revealing the secrets of our microbial planet (2007) by the committee on metagenomics: Challenges and functional applications. Washington, DC: The National Academies Press. Nyholm, S. V., and M. J. McFall-Ngai. 2004. The winnowing: Establishing the squid- Vibrio symbio- sis. Nature Reviews Microbiology 2(8):632-642. Olsen, E. 2011. Illuminating the perils of pollution, nature's way. New York Times. http://www.ny- times.com/2011/12/20/science/a-pollution-fight-powered-by-bioluminescent-sea-creatures.html (accessed June 14, 2012). Pace, N. R. 1997. A molecular view of microbial diversity and the biosphere. Science 276:734-740. ------. 2009. Mapping the tree of life: Progress and prospects. Microbiology and Molecular Biology Reviews 73(4):565-576. Paine, R. T., M. J. Tegner, and E. A. Johnson. 1998. Compounded perturbations yield ecological surprises. Ecosystems 1:535-545. Parniske, M. 2008. Arbuscular mycorrhiza: The mother of plant root endosymbioses. Nature Reviews Microbiology 6(10):763-775. Parsek, M. R., and E. P. Greenberg. 2005. Sociomicrobiology: The connections between quorum sensing and biofilms. Trends in Microbiology 13(1):27-33. Pennisi, E. 2011. Girth and the gut (bacteria). Science 332(6025):32-33. ------. 2012. Light in the deep. Science 335:1160-1163. Pfeiffer, T., S. Schuster, and S. Bonhoeffer. 2001. Cooperation and competition in the evolution of ATP-producing pathways. Science 292(5516):504-507. Plotkin, J. B., J. Dushoff, and S. A. Levin. 2002. Hemagglutinin sequence clusters and the antigenic evolution of influenza A virus. Proceedings of the National Academy of Sciences of the Untied States of America 99(9):6263-6268. Polz, M. F., J. A. Ott, M. Bright, and C. M. Cavanaugh. 2000. When bacteria hitch a ride: Associations between sufur-oxidizing bacteria and eukaryotes represent spectacular adaptations to environ- mental gradients. ASM News 66:531-539. Poole, S. J., E. J. Diner, S. K. Aoki, B. A. Braaten, C. t'Kint de Roodenbeke, D. A. Low, and C. S. Hayes. 2011. Identification of functional toxin/immunity genes linked to contact-de- pendent growth inhibition (CDI) and rearrangement hotspot (RHS) systems. PLoS Genetics 7(8):e1002217. Popa, R., A. R. Smith, J. Boone, and M. Fisk. 2012. Olivine-respiring bacteria isolated from the rock-ice interface in a lava-tube cave, a Mars analog environment. Astrobiology 12(1):9-18. Qin, J., R. Li, J. Raes, M. Arumugam, K. S. Burgdorf, C. Manichanh, T. Nielsen, N. Pons, F. Levenez, T. Yamada, D. R. Mende, J. Li, J. Xu, S. Li, D. Li, J. Cao, B. Wang, H. Liang, H. Zheng, Y. Xie, J. Tap, P. Lepage, M. Bertalan, J. M. Batto, T. Hansen, D. Le Paslier, A. Linneberg, H. B. Nielsen, E. Pelletier, P. Renault, T. Sicheritz-Ponten, K. Turner, H. Zhu, C. Yu, M. Jian, Y. Zhou, Y. Li, X. Zhang, N. Qin, H. Yang, J. Wang, S. Brunak, J. Dore, F. Guarner, K. Kristiansen, O. Pedersen, J. Parkhill, J. Weissenbach, P. Bork, and S. D. Ehrlich. 2010. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464(7285):59-65. Rainey, P. B. 2007. Unity from conflict. Nature 446(7136):616. Rainey, P. B., and B. Kerr. 2010. Cheats as first propagules: A new hypothesis for the evolution of in- dividuality during the transition from single cells to multicellularity. Bioessays 32(10):872-880. Rainey, P. B., and K. Rainey. 2003. Evolution of cooperation and conflict in experimental bacterial populations. Nature 425(6953):72-74. Rasko, D. A., and V. Sperandio. 2010. Anti-virulence strategies to combat bacteria-mediated disease. Nature Reviews Drug Discovery 9(2):117-128.

OCR for page 1
94 THE SOCIAL BIOLOGY OF MICROBIAL COMMUNITIES Rasko, D. A., M. J. Rosovitz, G. S. Myers, E. F. Mongodin, W. F. Fricke, P. Gajer, J. Crabtree, M. Sebaihia, N. R. Thomson, R. Chaudhuri, I. R. Henderson, V. Sperandio, and J. Ravel. 2008. The pangenome structure of Escherichia coli: Comparative genomic analysis of E. coli commensal and pathogenic isolates. Journal of Bacteriology 190(20):6881-6893. Ratcliff, W. C., R. F. Denison, M. Borrello, and M. Travisano. 2012. Experimental evolution of mul- ticellularity. Proceedings of the National Academy of Sciences of the United States of America 109(5):1595-1600. Reid, A., and M. Buckley. 2011. The rare biosphere. Washington, DC: American Academy of Microbiology. Relman, D. A. 2005. Session II: Ecology of host-microbe interactions. Paper presented at the Forum on Microbial Threats Workshop, Ending the War Metaphor: The Changing Agenda for Unravel- ing the Host-Microbe Relationship, Washington, DC, Institute of Medicine, Forum on Microbial Threats, March 17. ------. 2012. Learning about who we are. Nature 486:194-195. Riely, B. K., J. H. Mun, and J. M. Ane. 2006. Unravelling the molecular basis for symbiotic signal transduction in legumes. Molecular Plant Pathology 7(3):197-207. Rivers, T. M. 1937. Viruses and Koch's postulates. Journal of Bacteriology 33:1-12. Robinson, C. J., B. J. Bohannan, and V. B. Young. 2010. From structure to function: The ecol- ogy of host-associated microbial communities. Microbiology and Molecular Biology Reviews 74(3):453-476. Russian drill penetrates 14-million-year-old Antarctic lake. 2012. Wired. http://www.wired.com/ wiredscience/2012/02/lake-vostok-drilled/ (accessed September 26, 2012). Sandoz, K. M., S. M. Mitzimberg, and M. Schuster. 2007. Social cheating in Pseudomonas aerugi- nosa quorum sensing. Proceedings of the National Academy of Sciences of the United States of America 104(40):15876-15881. Scheffer, M., J. Bascompte, W. A. Brock, V. Brovkin, S. R. Carpenter, V. Dakos, H. Held, E. H. van Nes, M. Rietkerk, and G. Sugihara. 2009. Early-warning signals for critical transitions. Nature 461(7260):53-59. Scott, J. J., D. C. Oh, M. C. Yuceer, K. D. Klepzig, J. Clardy, and C. R. Currie. 2008. Bacterial protec- tion of beetle-fungus mutualism. Science 322(5898):63. Shade, A., and J. Handelsman. 2011. Beyond the Venn diagram: The hunt for a core microbiome. Environmental Microbiology 14(1):4-12. Shank, E. A., and R. Kolter. 2009. New developments in microbial interspecies signaling. Current Opinion in Microbiology 12(2):205-214. Sharon, I. M. J. Morowitz. B. C. Thomas, E. K. Costello, D. A. Relman, and J. F. Banfield. 2012. Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization. Genome Research [Epub ahead of print]. Slatkin, M. 1987. Gene flow and the geographic structure of natural populations. Science 236(4803): 787-792. Smith, J. 2001. The social evolution of bacterial pathogenesis. Proceedings of the Royal Society of London B 268:61-69. Stewart, F. J., I. L. G. Newton, and C. M. Cavanaugh. 2005. Chemosynthetic endosymbioses: Adapta- tions to oxicanoxic interfaces. Trends in Microbiology 13(3):439-448. Stewart, P. S., and M. J. Franklin. 2008. Physiological heterogeneity in biofilms. Nature Reviews Microbiology 6(3):199-210. Stolper, D. A., N. P. Revsbech, and D. E. Canfield. 2010. Aerobic growth at nanomolar oxygen con- centrations. Proceedings of the National Academy of Sciences of the United States of America 107(44):18755-18760. Strassmann, J. 2012a. The language of sociomicrobiology: Report from a meeting for the Forum on Microbial Threats. http://sociobiology.wordpress.com/2012/03/08/273/ (accessed April 14, 2012).

OCR for page 1
WORKSHOP OVERVIEW 95 ------. 2012b. Session II: Evolution of cooperation and control of cheating in the social amoeba: Dictyostelium discoideum. Paper presented at the Forum on Microbial Threats Workshop, The Social Biology of Microbial Communities, Washington, DC, Institute of Medicine, Forum on Microbial Threats, March 6. Suen, G., J. J. Scott, F. O. Aylward, S. M. Adams, S. G. Tringe, A. A. Pinto-Tomas, C. E. Foster, M. Pauly, P. J. Weimer, K. W. Barry, L. A. Goodwin, P. Bouffard, L. Li, J. Osterberger, T. T. Harkins, S. C. Slater, T. J. Donohue, and C. R. Currie. 2010. An insect herbivore microbiome with high plant biomass-degrading capacity. PLoS Genetics 6(9). Suen, G., C. Teiling, L. Li, C. Holt, E. Abouheif, E. Bornberg-Bauer, P. Bouffard, E. J. Caldera, E. Cash, A. Cavanaugh, O. Denas, E. Elhaik, M. J. Fave, J. Gadau, J. D. Gibson, D. Graur, K. J. Grubbs, D. E. Hagen, T. T. Harkins, M. Helmkampf, H. Hu, B. R. Johnson, J. Kim, S. E. Marsh, J. A. Moeller, M. C. Munoz-Torres, M. C. Murphy, M. C. Naughton, S. Nigam, R. Overson, R. Rajakumar, J. T. Reese, J. J. Scott, C. R. Smith, S. Tao, N. D. Tsutsui, L. Viljakainen, L. Wissler, M. D. Yandell, F. Zimmer, J. Taylor, S. C. Slater, S. W. Clifton, W. C. Warren, C. G. Elsik, C. D. Smith, G. M. Weinstock, N. M. Gerardo, and C. R. Currie. 2011. The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle. PLoS Genetics 7(2):e1002007. Tero, A., S. Takagi, T. Saigusa, K. Ito, D. P. Bebber, M. D. Fricker, K. Yumiki, R. Kobayashi, and T. Nakagaki. 2010. Rules for biologically inspired adaptive network design. Science 327 (5964):439-442. Tremaroli V., and F. Bckhed. 2012. Functional interactions between the gut microbiota and host metabolism. Nature 489(7415):242-249. Turnbaugh, P. J., R. E. Ley, M. Hamady, C. M. Fraser-Liggett, R. Knight, and J. I. Gordon. 2007. The Human Microbiome Project. Nature 449(7164):804-810. Venter, J. C., K. Remington, J. F. Heidelberg, A. L. Halpern, D. Rusch, J. A. Eisen, D. Wu, I. Paulsen, K. E. Nelson, W. Nelson, D. E. Fouts, S. Levy, A. H. Knap, M. W. Lomas, K. Nealson, O. White, J. Peterson, J. Hoffman, R. Parsons, H. Baden-Tillson, C. Pfannkoch, Y. H. Rogers, and H. O. Smith. 2004. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304(5667):66-74. Walker, B., C. S. Holling, S. R. Carpenter, and A. Kinzig. 2004. Resilience, adaptability and trans- formability in socialecological systems. Ecology and Society 9(2):1-9. Warnecke, F., P. Luginbuhl, N. Ivanova, M. Ghassemian, T. H. Richardson, J. T. Stege, M. Cayouette, A. C. McHardy, G. Djordjevic, N. Aboushadi, R. Sorek, S. G. Tringe, M. Podar, H. G. Martin, V. Kunin, D. Dalevi, J. Madejska, E. Kirton, D. Platt, E. Szeto, A. Salamov, K. Barry, N. Mikhailova, N. C. Kyrpides, E. G. Matson, E. A. Ottesen, X. Zhang, M. Hernandez, C. Murillo, L. G. Acosta, I. Rigoutsos, G. Tamayo, B. D. Green, C. Chang, E. M. Rubin, E. J. Mathur, D. E. Robertson, P. Hugenholtz, and J. R. Leadbetter. 2007. Metagenomic and functional analysis of hindgut micro- biota of a wood-feeding higher termite. Nature 450(7169):560-565. Waters, C. M., and B. L. Bassler. 2005. Quorum sensing: Cell-to-cell communication in bacteria. Annual Review of Cell and Developmental Biology 21:319-346. Weber, N. A. 1966. Fungus-growing ants. Science 153:587-604. West, S.A., and A. Gardner. 2010. Altruism, spite, and greenbeards. Science 327 (5971):1341-1344. West, S. A., A. S. Griffin, A. Gardner, and S. P. Diggle. 2006. Social evolution theory for microorgan- isms. Nature Reviews Microbiology 4(8):597-607. West, S. A., S. P. Diggle, A. Buckling, and A. L. Griffin. 2007a. The social lives of microbes. Annual Review of Ecology, Evolution, and Systematics 38:53-77. West, S. A., A. S. Griffin, and A. Gardner. 2007b. Social semantics: Altruism, cooperation, mutual- ism, strong reciprocity and group selection. Journal of Evolutionary Biology 20(2):415-432. Widder, E. A. 2010. Bioluminescence in the ocean: Origins of biological, chemical, and ecological diversity. Science 328(5979):704-708. Wilmes, P., S. L. Simmons, V. J. Denef, and J. F. Banfield. 2009. The dynamic genetic repertoire of microbial communities. FEMS Microbiology Review 33(1):109-132.

OCR for page 1
96 THE SOCIAL BIOLOGY OF MICROBIAL COMMUNITIES Wu, D., P. Hugenholtz, K. Mavromatis, R. Pukall, E. Dalin, N. N. Ivanova, V. Kunin, L. Goodwin, M. Wu, B. J. Tindall, S. D. Hooper, A. Pati, A. Lykidis, S. Spring, I. J. Anderson, P. D'Haeseleer, A. Zemla, M. Singer, A. Lapidus, M. Nolan, A. Copeland, C. Han, F. Chen, J. F. Cheng, S. Lucas, C. Kerfeld, E. Lang, S. Gronow, P. Chain, D. Bruce, E. M. Rubin, N. C. Kyrpides, H. P. Klenk, and J. A. Eisen. 2009. A phylogeny-driven genomic encyclopaedia of bacteria and archaea. Nature 462(7276):1056-1060. Wu, G. D., J. Chen, C. Hoffmann, K. Bittinger, Y. Y. Chen, S. A. Keilbaugh, M. Bewtra, D. Knights, W. A. Walters, R. Knight, R. Sinha, E. Gilroy, K. Gupta, R. Baldassano, L. Nessel, H. Li, F. D. Bushman, and J. D. Lewis. 2011. Linking long-term dietary patterns with gut microbial entero- types. Science 334(6052):105-108. Xavier, J. B. 2011. Social interaction in synthetic and natural microbial communities. Molecular & Systems Biology 7:483. Xavier, J. B., W. Kim, and K. R. Foster. 2011. A molecular mechanism that stabilizes cooperative secretions in Pseudomonas aeruginosa. Molecular Microbiology 79(1):166-179. Yong, E. 2012. Gut microbial "enterotypes" become less clear-cut. Nature. http://www.nature.com/ news/gut-microbial-enterotypes-become-less-clear-cut-1.10276 (accessed September 26, 2012). Zarubin, M., S. Belkin, M. Ionescu, and A. Genin. 2012. Bacterial bioluminescence as a lure for marine zooplankton and fish. Proceedings of the National Academy of Sciences of the United States of America 109(3):853-857. Zhang, X., and J. R. Leadbetter. 2012. Evidence for cascades of perturbation and adaptation in the metabolic genes of higher termite gut symbionts. mBio (in press). Zhang, X., E. G. Matson, and J. R. Leadbetter. 2011. Genes for selenium dependent and independent formate dehydrogenase in the gut microbial communities of three lower, wood-feeding termites and a wood-feeding roach. Environmental Microbiology 13:307-323. Zhang, X.-X., and P. B. Rainey. In preparation. The asocial biology of pyoverdin-producing pseudomonas.