Ecology of bacteria in the human gastrointestinal tract—identification of keystone and foundation taxa

Abstract

BackgroundDetermining ecological roles of community members and the impact of specific taxa on overall biodiversity in the gastrointestinal (GI) microbiota is of fundamental importance. A step towards a systems-level understanding of the GI microbiota is characterization of biotic interactions. Community time series analysis, an approach based on statistical analysis of changing population abundances within a single system over time, is needed in order to say with confidence that one population is affecting the dynamics of another.ResultsHere, we characterize biotic interaction structures and define ecological roles of major bacterial groups in four healthy individuals by analysing high-resolution, long-term (>180 days) GI bacterial community time series. Actinobacteria fit the description of a keystone taxon since they are relatively rare, but have a high degree of ecological connectedness, and are positively correlated with diversity both within and between individuals. Bacteriodetes were found to be a foundation taxon in that they are numerically dominant and interact extensively, in particular through positive interactions, with other taxa. Although community structure, diversity and biotic interaction patterns were specific to each individual, we observed a strong tendency towards more intense competition within than between phyla. This is in agreement with Darwin’s limiting similarity hypothesis as well as a published biotic interaction model of the GI microbiota based on reverse ecology. Finally, we link temporal enterotype switching to a reciprocal positive interaction between two key genera.ConclusionsIn this study, we identified ecological roles of key taxa in the human GI microbiota and compared our time series analysis results with those obtained through a reverse ecology approach, providing further evidence in favour of the limiting similarity hypothesis first put forth by Darwin. Larger longitudinal studies are warranted in order to evaluate the generality of basic ecological concepts as applied to the GI microbiota, but our results provide a starting point for achieving a more profound understanding of the GI microbiota as an ecological system.Electronic supplementary materialThe online version of this article (doi:10.1186/s40168-015-0107-4) contains supplementary material, which is available to authorized users.

A High-Fat High-Sucrose Diet Rapidly Alters Muscle Integrity, Inflammation and Gut Microbiota in Male Rats

“…Here, it appears that certain microbial groups were more sensitive to the abrupt change in diet, as evidenced by significant deviations from the chow-fed control animals at earlier time-points. However, the gut microbial community is a complex ecosystem, where each microbial taxa may play a different role in establishing its overall composition25. Furthermore, studies indicate that while diet can induce rapid changes in gut microbiota composition, these alterations may be transient due to the high resiliency of the gut microbiota community composition, and can thus return to a stable state26.…”

Enterococcus faecalisreadily colonizes the entire gastrointestinal tract and forms biofilms in a germ-free mouse model

“…levels is lost in fecal sequencing -factors that will be increasingly important as we unravel the details of interspecies relationships in the gut microbiome. 41 To put this research in its historical context, it is important to note that, alone, this germ-free mouse GI tract model is not especially novel: pioneering work in characterization and the dynamics of the mammalian microbiota was done in the late 1960s and early 1970s, notably by the Costello, Dubos, and Schaedler labs at Rockefeller University and continuing with Savage's work at the Universities of Illinois and Tennessee. 4,15,30,40,42,43 Nor did these labs limit themselves to fecal enumeration -within the significant technological limitations of the time they did some careful light and electron microscopy revealing the earliest bacterial spatial and distributional information in the developing murine gut.…”

Invasions of Host-Associated Microbiome Networks

“…Identification of keystone and foundational species using network inference and time series metagenomics data (Fisher and Mehta 2014) and (Trosvik and de Muinck 2015) Experimental example: A low-abundance biofilm species orchestrates periodontal disease Removal of keystone species and fragmentation of food webs can destabilise food webs (Solé and Montoya 2001;Proulx et al 2005) If an invader removes a keystone species or a foundational species this can have strong effects on the community Note: the trophic position into which the invader enters matters to the initial phases of the introduction (Romanuk et al 2009) (Hajishengallis et al 2011) Weak vs. strong interactions (links)…”