The Application of Ecological Theory Toward an Understanding of the Human Microbiome

Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA 94305, USA.
Science (Impact Factor: 33.61). 06/2012; 336(6086):1255-62. DOI: 10.1126/science.1224203
Source: PubMed


The human-microbial ecosystem plays a variety of important roles in human health and disease. 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 variability within and between hosts. We explore three core scenarios of human microbiome assembly: development in infants, representing assembly in previously unoccupied habitats; recovery from antibiotics, representing assembly after disturbance; and invasion by pathogens, representing assembly in the context of invasive species. Judicious application of ecological theory may lead to improved strategies for restoring and maintaining the microbiota and the crucial health-associated ecosystem services that it provides.

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Available from: Keaton Stagaman, Oct 14, 2015
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    • "Another key element shaping the microbiota relates to nutritional factors in early life. There is an increased abundance of certain Bifidobacterium spp, which thrive on human milk oligosaccharides (Zivkovic et al., 2011), in infants who are exclusively breastfed (Costello et al., 2012, Wang et al., 2013). Human milk microbiota also appears to be a direct source of Bifidobacteria and Lactobacillus in addition to its prebiotic properties (Jimenez et al., 2012, Fernandez et al., 2013). "
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    ABSTRACT: The prenatal and postnatal early-life periods are both dynamic and vulnerable windows for brain development. During these important neurodevelopmental phases, essential processes and structures are established. Exposure to adverse events that interfere with this critical sequence of events confers a high risk for the subsequent emergence of mental illness later in life. It is increasingly accepted that the gastrointestinal microbiota contributes substantially to shaping the development of the central nervous system. Conversely, several studies have shown that early-life events can also impact on this gut community. Due to the bidirectional communication between the gut and the brain, it is possible that aberrant situations affecting either organ in early life can impact on the other. Studies have now shown that deviations from the gold standard trajectory of gut microbiota establishment and development in early life can lead to not only disorders of the gastrointestinal tract but also complex metabolic and immune disorders. These are being extended to disorders of the central nervous system and understanding how the gut microbiome shapes brain and behavior during early life is an important new frontier in neuroscience.
    Neuroscience 10/2015; DOI:10.1016/j.neuroscience.2015.09.068 · 3.36 Impact Factor
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    • "In comparing the temporal dynamics of the oral microbiota in healthy and ECC children, we showed that plaque and saliva microbiota age of unrelated healthy children can explain over 50% of the variance in microbiota. The age-dependent changes observed could be caused by biological changes in tissues around the teeth during exfoliation of teeth (Crielaard et al., 2011), contact with external microbes (Kö nö nen, 2000), and/or development of immune systems (Costello et al., 2012), etc. Furthermore, the age-associated development of the healthy oral microbiota appears to be driven in part by changes in the relative abundance of taxa rather than the acquisition/loss of unique taxa with age, similar to the development of the skin microbiota at different ages (Song et al., 2013) but different from the gut microbiota at the age of 0–2 (Subramanian et al., 2014). "
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    ABSTRACT: Microbiota–based prediction of chronic infections is promising yet not well-established. Early Childhood Caries (ECC) is the most common infection in children. Here we simultaneously tracked microbiota development at plaque and saliva in 50 four-year-old preschoolers for two years; children either stayed healthy, transitioned into cariogenesis or experienced caries exacerbation. Caries onset delayed microbiota development, which is otherwise correlated with aging in healthy children. Both plaque and saliva microbiota are more correlated with changes in ECC severity (dmfs) during onset than progression. By distinguishing between aging- and disease-associated taxa and exploiting the distinct microbiota dynamics between onset and progression, we developed a model, Microbial Indicators of Caries, to diagnose ECC from healthy samples with 70% accuracy and predict, with 81% accuracy, future ECC onsets for samples clinically perceived as healthy. Thus, caries onset in apparently healthy teeth can be predicted using microbiota, when appropriately de-trended for age.
    Cell Host & Microbe 09/2015; DOI:10.1016/j.chom.2015.08.005 · 12.33 Impact Factor
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    • "In the present study, we assess the ability of neutral models to explain the distribution of microorganisms among a population of zebrafish, and then determine the conditions leading to departures from neutral behavior. In doing so, we adopt a conceptual framework in which we consider the microorganisms associated with individual zebrafish hosts to be local communities that are a part of a broader metacommunity consisting of the microorganisms associated with all of the hosts in the population (Leibold et al., 2004; Costello et al., 2012). We hypothesized that the ability of hosts to differentially select their microbial inhabitants increases with developmental age, thereby decreasing the relative importance of neutral processes. "
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    ABSTRACT: Despite their importance to host health and development, the communities of microorganisms associated with humans and other animals are characterized by a large degree of unexplained variation across individual hosts. The processes that drive such inter-individual variation are not well understood. To address this, we surveyed the microbial communities associated with the intestine of the zebrafish, Danio rerio, over developmental time. We compared our observations of community composition and distribution across hosts with that predicted by a neutral assembly model, which assumes that community assembly is driven solely by chance and dispersal. We found that as hosts develop from larvae to adults, the fit of the model to observed microbial distributions decreases, suggesting that the relative importance of non-neutral processes, such as microbe-microbe interactions, active dispersal, or selection by the host, increases as hosts mature. We also observed that taxa which depart in their distributions from the neutral prediction form ecologically distinct sub-groups, which are phylogenetically clustered with respect to the full metacommunity. These results demonstrate that neutral processes are sufficient to generate substantial variation in microbiota composition across individual hosts, and suggest that potentially unique or important taxa may be identified by their divergence from neutral distributions.The ISME Journal advance online publication, 21 August 2015; doi:10.1038/ismej.2015.142.
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