The ecosystem services of animal microbiomes

Abstract

Microbiologists often evaluate microbial community dynamics by formulating functional hypotheses based on ecological processes. Indeed, many of the methods and terms currently used to describe animal microbiomes derive from ecology and evolutionary biology. As our understanding of the composition and functional dynamics of "the microbiome" grows, we increasingly refer to the host as an ecosystem within which microbial processes play out. Even so, an ecosystem service framework that extends to the context of the host has thus far been lacking. Here, we argue that ecosystem services are a useful framework with which to consider the value of microbes to their hosts. We discuss those "microbiome services" in the specific context of the mammalian gut, providing a context from which to develop new hypotheses and to evaluate microbial functions in future studies and novel systems.

Primate microbiomes over time: Longitudinal answers to standing questions in microbiome research

“…Community ecology offers many theories and processes to understand gut microbiome dynamics (e.g., Costello, Stagaman, Dethlefsen, Bohannan, & Relman, ; Koskella, Hall, & Metcalf, ; McKenney et al, ; Sprockett, Fukami, & Relman, ; Walter & Ley, ). Ecological communities are examples of complex adaptive systems where large‐scale patterns such as diversity‐stability, diversity‐productivity, and species‐energy relationships emerge from interactions among species (Preston, ; Levin, ).…”

“…The gut microbiome's composition and diversity is shaped by many factors, including the host's evolutionary history, lifestyle, diet, and social interactions (e.g., David et al, ; Moeller, Caro‐Quintero, et al, ; Moeller, Foerster, et al, ). Some of these compositional differences may have functional consequences for the services gut microbiomes provide to their hosts, including the host's ability to digest complex carbohydrates, detoxify plant secondary compounds, and resist infectious diseases (Kohl & Dearing, ; McKenney, Koelle, Dunn, & Yoder, ).…”

Effects of captivity, diet, and relocation on the gut bacterial communities of white‐footed mice

“…These communities of microbes in a host are collectively known as the microbiota. The gut microbiota can play a role in host development, digestion, immunity, and behavior (McKenney, Koelle, Dunn, & Yoder, 2018; Suzuki, 2017) and can therefore influence the survival of relocated animals. Host‐associated microbiota are highly dynamic communities, and disrupting their equilibrium can lead to negative direct or indirect effects on their host (Hooks & Malley, 2017; reviewed in West et al, 2019) such as impaired immune function and metabolic disorders (Clayton et al, 2016; Krynak, Burke, Martin, & Dennis, 2017; Rosshart et al, 2017; Wasimuddin et al, 2017).…”

Can the microbiome influence host evolutionary trajectories?

“…Environmental factors, like diet or climate, also substantially influence the reservoir of possible microbial partners, leading to changes in the microbiome independent of any host evolution [38][39][40] . Host phenotypes also may be more strongly shaped by distinct microbial variation early in life, but because microbial dynamics operate at shorter timescales than host generations, those relevant microbes may not be faithfully transmitted across host generations 8,41,42 . Such complexities muddle the inheritance of the microbiome, challenging how frequently the microbiome could influence host evolution [6][7][8][9]25 .…”

“…Second, the null model should consider the balance in evolutionary interests between host and microbiome. Hosts and microbiomes will rarely have perfectly aligned evolutionary interests, suggesting a balance between cooperation and conflict 6,8,41 . For example, intergenomic conflict is likely to have important consequences for host-microbe coevolution because environmentally acquired microbes face vastly different evolutionary pressures inside and outside of hosts.…”