The Social Biology of Microbial Communities Workshop Summary (2012) / Chapter Skim
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Workshop Overview
Workshop Overview
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. 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)
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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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Forum on Microbial Threats hosted a public workshop to explore the emerging science of the "social biology" of microbial communities. Workshop presentations and discussions embraced a wide spectrum of topics, experimental systems, and theoretical perspectives representative of the current, multifaceted exploration of the microbial frontier.
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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)
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Studies of such interactions among multicellular organisms inform the disciplines of social biology7 and ecology.8 While theoretical constructs derived from observations of the macroscopic world offer ways to interpret microbial 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 capabilities of individual members.
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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.
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The stalk aids in the dispersal of the remaining cells, which differentiate into spores. The social biology of D
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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 morphology that promotes colonization to one that promotes the maintenance of an exclusive association with V
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and its luminous bacterial symbiont Vibrio fischeri (B) forms within the squid'sFigure WO-3 light organ (C and D)
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SOURCE: Reprinted by permission from Macmillan Publishers Ltd: Nature Reviews Microbiology, Nyholm and McFall-Ngai (2004) , copyright 2004.
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. 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)
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. A recent effort to catalog the genes of the adult human gut microbiome identified 3.3 million nonredundant microbial genes in fecal samples obtained from 124 individuals, suggesting the presence FIGURE WO-6 The microbiome Figure WO-6.eps of various anatomical locations of the human body.
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. While the relationship between humans and the microbial inhabitants of their gastrointestinal tracts tends to be mutually beneficial, shifts in microbial gene expression may result in immune responses that precipitate disease states such as inflammatory bowel disease, which is characterized by an unregulated immune response to gut microbes (Littman and Pamer, 2011)
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TABLE WO-1 Social Traits Exhibited by Bacteria Compared with Examples from Vertebrates and Invertebrates Higher Organism Cooperative Behavior Group-Derived Benefits Microbe Examples Comparisons Chemical Coordinated population Vibrio fischeri, Pheromone production communication behavior Pseudomonas in many social animals (quorum sensing) aeruginosa, Staphylococcus aureus, etc.
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Louis, who both raised and answered this question as follows (Dr. Strassman's contribution to the workshop summary report can be found in Appendix A, pages 509-533)
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We can use that knowledge, but we can also do things much more quickly and with a much less biased eye by studying bacteria." As a result, he predicted, observations of microbial social biology will eventually produce hypotheses to be tested in macroscopic species. Microbial Communication Key to microbial interactions with other organisms and their surroundings are a range of microbial strategies for sensing and responding to environmental conditions (Bassler and Losick, 2006; IOM, 2009)
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Additional workshop presentations summarized later in this overview described a range of mechanisms by which microbes interact with members of their own species and with other microbes, with host macroorganisms, and with their environment. Quorum sensing17 Many microorganisms -- as well as some cell types within multicellular organisms -- secrete small signaling molecules and sense their concentration in the environment (Xavier, 2011)
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Greenberg uses the bacterium Pseudomonas aeruginosa as a model to study the evolution of cooperative behavior and understand how quorum sensing is embedded in the complex regulatory networks of a cell. This microbe is "found wherever we look for it: in the soil, the water, on plants, invertebrates, and people," he noted.
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Indeed, it turns out that quorum sensing also controls the ability of the bacterium to catabolize adenosine -- and that the addition of adenosine to growth medium for P aeruginosa suppresses the emergence of quorum-sensing mutants.
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Cooperation can happen without quorum sensing, he said, although the relative benefits and costs of quorum sensing as a means to control cooperation remain to be determined. "This is a science in its infancy," Greenberg observed.
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. Bioluminescence can appear as a "persistent glow of bioluminescent bacteria to brief flashes from lanternfish light organs" (Widder, 2010)
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has a large preorbital light organ)
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. For free-living bacteria where the adaptive value is less evident, she noted that organisms often form communities on the surface of fish fecal pellets and suggested that the collective glow they produce (on cue from quorum sensing)
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24 THE SOCIAL BIOLOGY OF MICROBIAL COMMUNITIES FIGURE WO-9 The burglar alarm jellyfish (top) lights up blue (lower left)
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. Individual Population Community Physiology: Demographics: Community ecology: Differential gene Birth, death, immigration, Interspecific interactions Ecology expression in response emigration that shape community to change structure and function Population genomics: Metagenomics: Fine-scale mapping of Genomics individual genomes Comparative genomic Genetic potential of collective analyses to assess variation members of community Bacterial genetics: Population genetics: Community genetics: Role of genes under Allele frequency Interplay between genetic Genetics various conditions distribution composition of community and ecological community properties FIGURE WO-10 Progression from studies on the individual scale to studies on the community scale.
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amplification with primers that hybridize to highly conserved regions in bacterial or archaeal 16S rRNA genes (or eukaryotic microbial 18S rRNA genes) followed by cloning and sequencing yields an initial description of species present in a microbial community.
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. SOURCES: http://commonfund.nih.gov/index.aspx; http://www.hmpdacc.org/reference_ genomes/reference_genomes.php; The Human Microbiome Jumpstart Reference Strains Consortium (2010)
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The Role of Oxygen in the Structure and Function of Microbial Communities "One of the spectacular features of microorganisms is their capacity to couple all kinds of chemical reactions," observed Thomas Schmidt of Michigan State University (Dr. Schmidt's contribution to the workshop summary report can be found in Appendix A, pages 470-483)
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29 Lining of cavities exposed to the external environment and internal organs that are covered in epithelium and are involved in absorption and secretion. 30 To gain insight into the metagenome -- the genes and genomes present within a microbial community -- researchers isolate DNA from these communities and sequence it in a "shotgun fashion": the organisms' genomes are fragemented into small pieces that can be sequenced.
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Cavanaugh's contribution to the workshop summary report can be found in Appendix A, pages 128-136)
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Fila mentous epsilon proteobacterial symbionts cover the exterior of the hydrothermal vent-dwelling shrimp, Rimicaris exoculata (A and B)
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Based on their study of bacterial symbionts of vent-dwelling shrimp and tubeworms, Cavanaugh's group developed a "positive qualitative feedback model" by which the free-living population of symbiotic bacteria increases relative to nonsymbiotic microbes in the environment as a result of "inoculation" by the host-associated symbionts; at 32 Cavanaugh noted that sulfide is able to be oxidized chemically in the presence of oxygen. The tubeworm hemoglobin binds the oxygen and sulfide separately (Flores et al., 2005)
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Handelsman's contribution to the workshop summary report can be found in Appendix A, pages 242-275)
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cereus may suppress disease by changing the microbial community on the root and, consequently, the exudates from it. By comparing the physiological traits associated with communities of aerobic bacteria isolated from soy seedling roots treated with B
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. global shift in community composition occurs after B
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The ability to determine evolutionary relationships among organisms and to depict them as a tree of life has revolutionized our understanding of microbes in the world, said speaker Jonathan Eisen of the University of California, Davis (Dr. Eisen's contribution to the workshop summary report can be found in Appendix A, pages 180-212)
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1997. A Molecular View of Microbial Diversity and the Biosphere.
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Phylogenetic analysis not only tells us what we know about microbial diversity, but also helps reveal what we do not know, Eisen noted. For example, despite the discovery of dozens of major lineages of bacteria, archaea, or eukaryotes by phylogenetic analysis, most of the available genome sequences come from only a small number of those lineages.
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" (Dr. Banfield's contribution to the workshop summary report can be found in Appendix A, pages 97-114)
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AMD biofilms: Using model communities to study microbial evolution and ecological complexity in nature, 4(5) :599-610, copyright 2010.
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She and her colleagues are FIGURE WO-17 Microbial community proteomics: functional assays in situ. SOURCE: Banfield (2012)
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The difference between strains suggests that each strain plays a distinct ecological role in the nascent microbial community of the infant gut. Proteomic information supports the conclusion that the two strains are functionally different, Banfield reported.
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The micro Figure WO-18.eps bial orchestra analogy showing relatedness of individual community members in acid mine drainage biofilms with corresponding instrumental bitmap groups. SOURCE: Wilmes et al., FEMS Microbiology Reviews, "The dynamic genetic repertoire of microbial communities," 33(1)
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. The apparent fluidity of gene exchange among microbes raises important topics for ongoing inquiry, such as how frequently and under what conditions it occurs, the extent to which lateral gene transfer contributes to the evolution of microbial communities and host-microbe relationships, and the potential of lateral gene transfer among microbes to influence microbial functions such as pathogenicity, virulence, antibiotic resistance, as well as host metabolism.
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. Workshop speakers addressed the broad topic of microbial interactions from several perspectives: by exploring the variety of mechanisms by which microbes interact with each other, their hosts, and the environment; by describing specific microbial interactions across a range of ecological contexts; and by considering how ecology and natural selection have shaped microbial interactions and potentially led to the emergence of multicellular organisms.
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Sperandio's contribution to the workshop summary report can be found in Appendix A, pages 484-508)
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. Her work builds on the well-established concept of quorum sensing as a means for bacteria to assess local population density and coordinate the expression of critical genes, including those that encode virulence factors (Njoroge and Sperandio, 2009)
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The workshop presentations summarized in this section further illustrate the intricacy and specificity of microbial interactions, and the mechanisms that make
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Swarming Bacteria as Agents of Microbial Dispersal An intriguing interspecies communication between bacteria and fungi was described by speaker Colin Ingham of Wageningen University, The Netherlands (Dr. Ingham's contribution to the workshop summary report can be found in Appendix A, pages 304-322)
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SOURCE: King (2011) ; image provided courtesy of Colin Ingham and Eshel Ben-Jacob.
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resource optimization," and he suggested that future studies could explore whether this form of colonial life is beneficial with regard to efficient foraging and distribution of nutrients from disparate sources throughout the colony. The Fungal Gardens of the Leaf-Cutter Ants The leaf-cutter ant occupies the center of an outstanding model of complex and dynamic interactions linking microbes, multicellular organisms, and the
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Currie's contribution to the workshop summary report can be found in Appendix A, pages 137-180)
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2006. Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ants.
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Leadbetter's contribution to the workshop summary report can be found in Appendix A, pages 323-360)
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. By comparing gene diversity in a wide range of termite host species, Leadbetter explored how environmental factors such as changes in termite biology, diet, and symbiont community composition may have impacted the evolution of the gut microbial communities of higher termites (Zhang and Leadbetter, 2012)
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56 FIGURE WO-23 Inferred evolutionary history for fdhF in the symbiotic gut microbial communities of lignocellulose-feeding insects. LCA, last common ancestor; FDH, formate dehydrogenase; Sec, selenocysteine functional variants of fdhF; Cys, cysteine functional variants of fdhF; Figure WO-23.eps and AGR, Amitermes-Gnathamitermes-Rhynchotermes.
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. As illustrated by these examples, although coevolution between host and symbionts is an important force shaping mutualisms, other forces such as the loss of microbial community members or the relaxation and reemergence of nutritional pressures may also impact the evolution of a mutualism.
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with In this old typestudy, Strassmann masked and colleagues and new type artificially entered constructed low-relatedness conditions and allowed evolution to proceed for 31 generations of fruiting body formation. They assessed the cheating ability of the evolved lines in social compe tition with their ancestors, during fruiting body formation.
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aeruginosa as a model system for studying the selective pressures involved in this collective trait (Dr. Xavier's contribution to the workshop summary report can be found in Appendix A, pages 546-579)
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Speaker Paul Rainey, of the New Zealand Institute for Advanced Study and the Max Planck Institute for Evolutionary Biology, and his coworkers have examined the cyclical process of cooperation and cheating in bacteria as a possible route to multicellularity (Dr. Rainey's contribution to the workshop summary report can be found in Appendix A, pages 409-425)
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WORKSHOP OVERVIEW 61 FIGURE WO-26 A putative life cycle for mat-forming bacteria. We start with a single bacterium (given in blue)
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Ecological changes in the gut microbiota have been associated with such diseases as allergy, inflammatory bowel disease (IBD) , and cancer, as well as two internationally
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Relman's contribution to the workshop summary report can be found in Appendix A, pages 426-469)
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. 46 These microbial genes were detected in fecal samples obtained from 124 individuals, suggesting the presence of 1,000 to 1,150 prevalent bacterial species.
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According to Relman, patterns of microbial community composition differ between healthy individuals and those with disorders such as obesity, IBD, chronic periodontitis, Crohn's disease, and bacterial vaginosis (Dethlefsen et al., 2007; Ley et al., 2006b; Turnbaugh et al., 2006)
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Each of the evolutionary scenarios presented below depicts the forces of natural selection acting within a specific and influential ecological context, such as resource availability. The role of heterogeneous ("patchy")
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Brown characterized virulence of a microorganism as the ability to cause damage to the host, and noted that a disproportionate number of genes encoding secreted, host-harming microbial products, known as virulence factors, are found on mobile genetic elements. "This supports the idea of virulence being intrinsically a cooperative trait," he said, although the nature of the advantage provided by virulence seems paradoxical.
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This is a hypothesis now being tested in his laboratory using Pseudomonas aeruginosa in what he described as an evolutionary screen for virulence traits. Such a screen could have general application in determining how easily microbes develop resistance to antivirulence drugs, he said.
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. Social evolutionary theory provides a framework for analyzing the selective forces that shape microbial interactions such as cooperation, but it is important to recognize that microbial behaviors take place in ecological contexts that researchers are only beginning to define.
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Evolutionary Transitions Through Higher-Level Selection Plausible on its face, the progression from multicellular microbial communities -- with their previously noted capacities for intercellular communication, collective action, and division of labor -- to multicellular organisms is difficult to reconcile with the central Darwinian concept of individuality, Rainey noted. "Any set of entities that have variation, reproduction, and heredity will evolve by natural selection," he said.
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Developing Theoretical and Experimental Frameworks Levin and Relman described theoretical and experimental frameworks for generating and testing hypotheses on structure-function relationships and interactions in microbial communities. Such investigations could take advantage of a wealth of analytical tools and mathematical models, as well as technologies such as genomics and proteomics for characterizing microbial community composition and function.
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Anderson argued that a reductionistic approach to understanding the behavior of a complex adaptive system -- for example, attempting to predict the behavior of an entire microbial community from knowledge of the behavior of individual community members -- would prove inadequate (Anderson, 1972)
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6 bitmaps with vector labels dendritiformis bacteria. To self-engineer their colonial structure these bacteria regulate the balance between attractive and repulsive chemotactic signaling as well as their food chemotaxis.
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. Complex adaptive systems can achieve robustness -- often called resilience in ecology -- through both rigidity (by resisting change from normal function)
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From Plotkin et al., 2002, Hemagglutinin sequence clusters and the antigenic evolution of influenza A virus, Volume 99, DOI: 10.1073/pnas.082110799, reprinted with permission from Proceedings of the National Academy of Sciences.
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. These studies have revealed the human gut microbiota to be a "dynamic ecological system" with considerable resilience.
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A more complete understanding of these factors could lead to ways to measure resilience as a gauge of host health, and perhaps to the ability to increase the resilience of the gut community through manipulation. Computer simulations and predictive mathematical models can be used to explore microbial community dynamics in complex communities and environmental settings.
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Holmes' contribution to the workshop summary report can be found in Appendix A, pages 275-304)
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Noting that scientific institutions will need to be reorganized to support transdisciplinarity, forum member George Poste, of Arizona State University and Complex Adaptive Systems Initiative, Inc., decried "the anachronism of the contemporary training curriculum, and also the fragmentation of grant agencies to be able to deal with this type of very complex transdisciplinary research."
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As West and coauthors observe, progress in the field of social biology "is often hindered by poor communication between scientists, with different people using the same term to mean different things, or different terms to mean the same thing. This can obscure what is biologically important, and what is not." In addition, "the potential for such semantic confusion is greatest with interdisciplinary research" (West et al., 2007b)
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Strassmann reminded participants that although the words used in social biology are weighted by possible human interpretations, the field is "a really new and exciting field of understanding how selection operates." Underlying the language of social biology is the important understanding that "natural selection operating on social behaviors is really powerful and takes into account competition among individuals in social contexts." Insights into Life on Earth and Other Worlds The sea change that accompanies the shift to viewing microbial communities as the unit of study will extend to the obvious and subtle implications of this work. Microorganisms drive some of the largest-scale phenomena on the planet, from the conversion of energy from the sun to nitrogen fixation in plants.
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82 THE SOCIAL BIOLOGY OF MICROBIAL COMMUNITIES FIGURE WO-31 In 1977, the deep-ocean submersible Alvin led scientists to discover tubeworms living at the edges of hydrothermal vents in the deep sea. Figure WO-31 SOURCE: University of Washington; NOAA/OAR/OER.
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Viable Pseudomonas bacterial species were recently isolated from a lava tube in the Cascade Mountains in Oregon. At an elevation of 5,000 feet, the bacteria were found deep inside the icy cave, an environment believed to be similar to some of the surface environments on Mars (Popa et al., 2012)
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Behind the growing margin, the spreading mycelium resolved into a network of tubes interconnecting the food sources. The horizontal width of each panel is 17 cm.
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Metagenomic analysis of the gut community of a wood-feeding, higher termite species has revealed a rich reservoir of genes coding for enzymes relevant to wood degradation and the conversion of lignocelluloses into biofuels (Warnecke et al., 2007)
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In total, Currie and coworkers have identified seven novel small molecules 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.
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. WORKSHOP OVERVIEW REFERENCES Ackerman, J
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Paper presented at the Forum on Microbial Threats Workshop, The Social Biology of Microbial Communities, Washington, DC, March 7. Bassler, B
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2008. The pervasive effects of an antibi otic on the human gut microbiota, as revealed by deep 16S rRNA sequencing.
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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.
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Washington, DC: Workshop summary. The National Academies Press.
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2010. Ecological distribution and population physiology defined by proteomics in a natural microbial community.
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2010. A human gut microbial gene catalogue established by metagenomic sequencing.
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2007. Social cheating in Pseudomonas aerugi nosa quorum sensing.
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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.
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In preparation. The asocial biology of pyoverdin-producing pseudomonas.
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