Microbial Ecology in States of Health and Disease Workshop Summary (2014) / Chapter Skim
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A5 The application of ecological theory toward an understanding of the human microbiome--Elizabeth K. Costello, Keaton Stagaman, Les Dethlefsen, Brendan J. M. Bohannan, and David A. Relman
A5 The application of ecological theory toward an understanding of the human microbiome--Elizabeth K. Costello, Keaton Stagaman, Les Dethlefsen, Brendan J. M. Bohannan, and David A. Relman
Pages 164-183
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From page 164... ...
Each person can be viewed as an island-like "patch" of habitat occupied by microbial assemblages formed by the fundamental processes of community ecology: dispersal, local diversification, environmental selection, and ecological drift. Community assembly theory, and metacommunity theory in particular, provides a framework for understanding the ecological dynamics of the human microbiome, such as compositional 17 From "The application of ecological theory toward an understanding of the human microbiome," Science 336(6086)
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Here, we explore how community assembly theory can be used to understand the human-associated microbiota and its role in health and disease. Ecological Processes Within Humans The essential building blocks of community assembly theory encompass the processes that create and shape diversity in local assemblages: dispersal, diversification, environmental selection, and ecological drift (Vellend, 2010)
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Large microbial population sizes, high growth rates, and strong selective regimes, all of which can be found in the human body, result in rapid microbial adaptation via mutation or recombination. Recombination via horizontal gene transfer may be especially common among members of the human microbiota, especially those sharing the same ecological niche (e.g., body site)
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. Metacommunity Theory and the Human Microbiome Various theoretical frameworks are used to study community assembly; one key framework is neutral theory (Hubbell, 2001)
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For example, differences between body habitats may be best explained by environmental selection, differences between siblings for the same habitat may be best explained by historical contingency, differences between monozygotic twins prior to weaning highlight the role of stochasticity, and differences between neonates born by cesarean section versus vaginal delivery are likely to be explained by dispersal limitation. [Adapted from (Chase, 2003; Fukami, 2010)
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Human populations can be viewed likewise, with host-to-host dispersal linking microbial communities. Metacommunity theory is especially helpful for understanding the relative importance of dispersal and environmental selection in shaping host-associated communities (Mihaljevic, 2012)
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Postnatal Acquisition and Development of the Human Microbiome Babies are born essentially sterile and acquire their microbiome from their surroundings. The postnatal assembly of the human microbiota plays an important role in infant health, providing resistance to pathogen invasion, immune stimulation, and other important developmental cues early in life (Mackie et al., 1999)
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gut or vaginal microbiota may occur later in cesarean section infants, at low density or low frequency, but may be inadequate for outcompeting already established strains. For example, cesarean section infants display reduced abundances and/or incidences of colonization by the genera Bacteroides and Bifidobacterium early in development relative to infants born by vaginal delivery (Bennet and Nord, 1987; Penders et al., 2006)
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Differences attributable to early exposures such as delivery mode fade as microbiota compositions become more canalized. Life events such as illness, diet modification, and antibiotic therapy can still impose disturbances, although specific compositions appear to recover.
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The depth of a basin indicates the likelihood of a community remaining in that basin despite frequent "buffeting" by minor disturbance (Walker et al., 2004) and hence the relative stability of the community state.
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. However, antibiotic resistance among the microbiota is one of several mechanisms that may act to enhance the resilience of indigenous communities, hence preserving their beneficial ecosystem services.
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. Overall, research suggests that the human gut microbiota of generally healthy adults is largely, but not entirely, resilient to short courses of antibiotic therapy, whereas clinical evidence indicates that extended or repeated courses are more likely to result in serious complications such as the invasion and bloom of Clostridium difficile (Owens et al., 2008)
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; (ii) antimicrobial peptides and mucosal antibodies in the mucus layer that further hinder bacterial colonization of the epithelium (Duerkop et al., 2009)
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. By viewing pathogens as invasive species, we see that the contexts in which they are able to cause disease are the same as those required for any other species that invades and proliferates in a community.
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in a specific manner without causing additional disturbance to the community will be very important for preventing and treating disease caused by invasive species. Translating Ecological Understanding into Clinical Practice An improved understanding, informed by ecological theory, of how microbiomes assemble could alter clinical practice by changing the perspective clinicians bring to the treatment of infectious disease and chronic inflammatory disorders.
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We envision clinical medicine focused on managing the human body and its associated microbiome to preserve these ecosystem services. How might this be accomplished?
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I Prosser et al., The role of ecological theory in microbial ecology.
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R Gaskins, Developmental microbial ecology of the neonatal gastrointes tinal tract.
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10.1136/sti.2009.040592 M Arumugam et al., MetaHIT Consortium, Enterotypes of the human gut microbiome.
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E Elinavet al., NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis.
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