Conceptualizing human microbiota: from multicelled organ to ecological community

Abstract

The microbiota of a typical, healthy human contains 10 times as many cells as the human body and incorporates bacteria, viruses, archea, protozoans, and fungi. This diverse microbiome (the collective genomes of the microbial symbionts that inhabit a human host) is essential for human functioning. We discuss the unstated assumptions and implications of current conceptualizations of human microbiota: (1) a single unit that interacts with the host and the external environment; a multicelled organ; (2) an assemblage of multiple taxa, but considered as a single unit in its interactions with the host; (3) an assemblage of multiple taxa, which each interacts with the host and the environment independently; and (4) a dynamic ecological community consisting of multiple taxa each potentially interacting with each other, the host, and the environment. Each conceptualization leads to different predictions, methodologies, and research strategies.

Figure 1

Four conceptualizations of human microbiota that focus to varying degrees on structure and/or function of the microbiota as a whole or of the component microbial taxa. Assumptions and implications of the extremes of simplicity and tractability on one hand (the multicelled organ conceptualization, Figure 1(a)) and complexity and relative intractability (the dynamic ecological community conceptualization, Figure 1(d)) are described in Table 1. All the interactions (linking arrows) are mediated to some extent by changes in the internal environment, which is not shown to enhance clarity. Mechanisms underlying the various interactions, including the role of internal environment, are depicted in Figure 2.

Figure 2

Potential mechanisms of interactions between external environment, host and the microbiota in the multicelled organ conceptualization of human microbiota.