Our microbial selves: what ecology can teach us

Abstract

Advances in DNA sequencing have allowed us to characterize microbial communities--including those associated with the human body--at a broader range of spatial and temporal scales than ever before. We can now answer fundamental questions that were previously inaccessible and use well-tested ecological theories to gain insight into changes in the microbiome that are associated with normal development and human disease. Perhaps unsurprisingly, the ecosystems associated with our body follow trends identified in communities at other sites and scales, and thus studies of the microbiome benefit from ecological insight. Here, we assess human microbiome research in the context of ecological principles and models, focusing on diversity, biological drivers of community structure, spatial patterning and temporal dynamics, and suggest key directions for future research that will bring us closer to the goal of building predictive models for personalized medicine.

Figure 1

The human microbiome meets ecology. The human body can be visualized as an ecosystem that is subject to the ecological processes that structure communities, including dispersal, invasion, succession and meta-community dynamics. At the local level, interactions with members of the resident microbial and phage community, such as competition and predation, probably shape the structure of the community, whereas the meta-community structure might be more influenced by interactions among communities, such as dispersal and invasion, and stochastic events, such as disturbance. These types of interaction can extend beyond the meta-community to the ecosystem when more than one individual is considered, and they can also vary temporally. Further studies of the human microbiome will help to determine the effects of these processes on microbial interactions over space and time, including intra- and inter-personal variation and development from birth, and ultimately lead to a more-comprehensive understanding of our microbial selves.

Figure 2

New technologies reveal new pictures of human-associated microbial communities. With the development of new technologies—including but not limited to high-throughput sequencing—the increase in the amount of data we can gather has allowed us to better test and understand the ecological processes acting within our microbial selves and, in turn, will help to frame future work within an ecological context. The colour of each star indicates the methodologies used in the different studies: dark blue, microscopic observation; blue, culturing; green, Sanger sequencing; red, pyrosequencing; yellow, metagenome sequencing (Eckburg et al, 2005; Moore & Moore, 1994; Savage, 1977). Estimates are based on a rough count of individuals reported in studies and articles describing human-associated microbes or communities, and are probably underestimates of the numbers of subjects.

Figure 3

Variability of the human microbiota. The plot shows the first two axes of the principal coordinate analysis (PCoA), which capture the differences and similarities between communities in each biological sample. The area of each polygon represents the variability within clusters of the samples in each study, indicating that the human microbiome separation is due to its origin (gut, skin, mouth and urogenital) and that there is as much variation over time in one person as there is between adults in a community. Samples from Costello et al (2009), 27 sites in 7–9 healthy adults are shown in red and samples from Caporaso et al (2011a), 3 sites in two adults over 1 year, are shown in blue.