Conceptual Exchanges for Understanding Free-Living and Host-Associated Microbiomes

Abstract

Whether a microbe is free-living or associated with a host from across the tree of life, its existence depends on a limited number of elements and electron donors and acceptors. Yet divergent approaches have been used by investigators from different fields. The "environment first" research tradition emphasizes thermodynamics and biogeochemical principles, including the quantification of redox environments and elemental stoichiometry to identify transformations and thus an underlying microbe. The increasingly common "microbe first" research approach benefits from culturing and/or DNA sequencing methods to first identify a microbe and encoded metabolic functions. Here, the microbe itself serves as an indicator for environmental conditions and transformations. We illustrate the application of both approaches to the study of microbiomes and emphasize how both can reveal the selection of microbial metabolisms across diverse environments, anticipate alterations to microbiomes in host health, and understand the implications of a changing climate for microbial function.

Keywords: biogeochemistry; host-microbiome; microbial metabolisms; microbiome; oxidation state; redox; stoichiometry.

FIG 1

The portrayal of some habitats classified by whether electron acceptors (red) and donors (blue) for chemotrophic metabolism are relatively scarce or abundant. When electron donors are scarce, lithotrophic metabolisms, or the use of inorganic substrates, occurs. Placing habitats in this simplified diagram illustrates the selective pressures and observations that are common to both host-associated and free-living microbes. It also highlights how changes to a system may be mediated by changes to electron acceptors and donors. For example, gut dysbiosis is associated with an increasing number of electron acceptors. Warming aquatic systems, via climate change, may reduce the distribution of well-oxygenated habitats and thus oxygen as an electron acceptor (figure by Brooks Bays).