A Developing Symbiosis: Enabling Cross-Talk Between Ecologists and Microbiome Scientists

Abstract

Like all interactions, the success of cross-discipline collaborations relies on effective communication. Ecology offers theoretical frameworks and lexicons to study microbiomes. Yet some of the terms and concepts borrowed from ecology are being used discordantly by microbiome studies from their traditional definitions. Here we define some of the ecological terms and concepts as they are used in ecology and the study of microbiomes. Where applicable, we have provided the historical context of the terms, highlighted examples from microbiome studies, and considered the research methods involved. We divided these concepts into four sections: Biomes, Diversity, Symbiosis, and Succession. Biomes encompass the interactions within the biotic and abiotic features of an environment. This extends to the term "microbiome," derived from "biome," and includes an environment and all the microbes within it. Diversity encompasses patterns of species richness, abundance, and biogeography, all of which are important to understanding the distribution of microbiomes. Symbiosis emphasizes the relationships between organisms within a community. Symbioses are often misunderstood to be synonymous with mutualism. We discard that implication, in favor of a broader, more historically accurate definition which spans the continuum from parasitism to mutualism. Succession includes classical succession, alternative stable states, community assembly frameworks, and r/K-selection. Our hope is that as microbiome researchers continue to apply ecological terms, and as ecologists continue to gain interest in microbiomes, each will do so in a way that enables cross-talk between them. We recommend initiating these collaborations by using a common lexicon, from which new concepts can emerge.

Keywords: diversity; ecology; microbiome; succession; symbiosis.

FIGURE 1

Biome and Microbiome. A biome encompasses all organisms and abiotic conditions of an ecosystem, and microbiomes are nested within it. In the illustrated example, a temperate coniferous forest biome (left) contains organisms including pine trees and elk, as well as abiotic conditions such as rainfall, temperature, oxygen availability, and soil pH. The biome also contains countless microbial species, and each microbiome within it contains a subset of these. For example, the pine needle microbiome (top right) contains microorganisms and abiotic conditions found in or around pine needles, and the elk oral microbiome (bottom right) contains microorganisms and abiotic conditions found in the mouths of elk. In this way, “pine needle microbiome” refers to the organisms and abiotic conditions within and around pine needles in general. The example depicted is only one sample, just as one human gut is just a sample of the broader human gut microbiome.

FIGURE 2

Symbiotic relationship continuum. Symbiotic relationships encompass multiple dimensions of effect, represented here on two axes. If a symbiosis has a positive (blue) effect for a microbe, and a negative (red) effect for the host, this is known as parasitism (top right corner). However, each type of symbiosis shown does not occupy a discrete factorial combination of positive and negative effects. Instead, some symbioses may have more positive or negative effects for a symbiont or host than others, and these may shift depending upon their environmental context as shown in the figure by the gradation of red and blue values between the two axes. For example, two different symbioses may both be mutualistic (mutually positive, bottom right), but one of those relationships may stray slightly more toward commensalism. This figure is adapted from Bronstein (1994).

FIGURE 3

Succession and Alternative Stable States. Microbial communities within the gut can be disrupted by a disturbance event like antibiotic treatment. In this figure, the starting community represents the microbial community in the gut before antibiotic treatment. Antibiotic treatment changes the composition of the gut bacteria. After the treatment, the community re-assembles. The left column represents succession culminating in a climax community that mirrors the original starting community. Under historical definitions of the word “succession” (sensu Clements, 1916), this re-assembly to a deterministic climax community would be the only trajectory called succession. However, under modern usage of the term, succession includes the possibility of alternative stable states (Beisner et al., 2003), which are shown in the middle and right columns. In these cases, different stable communities may be reached depending on the order of species arrival into the disturbed environment. Each alternative stable state has resilience, which is symbolized by the curved arrows.