Integrating Ecological and Engineering Concepts of Resilience in Microbial Communities

Abstract

Many definitions of resilience have been proffered for natural and engineered ecosystems, but a conceptual consensus on resilience in microbial communities is still lacking. We argue that the disconnect largely results from the wide variance in microbial community complexity, which range from compositionally simple synthetic consortia to complex natural communities, and divergence between the typical practical outcomes emphasized by ecologists and engineers. Viewing microbial communities as elasto-plastic systems that undergo both recoverable and unrecoverable transitions, we argue that this gap between the engineering and ecological definitions of resilience stems from their respective emphases on elastic and plastic deformation, respectively. We propose that the two concepts may be fundamentally united around the resilience of function rather than state in microbial communities and the regularity in the relationship between environmental variation and a community's functional response. Furthermore, we posit that functional resilience is an intrinsic property of microbial communities and suggest that state changes in response to environmental variation may be a key mechanism driving functional resilience in microbial communities.

Keywords: microbial communities; microbial ecology; networks; resilience; resistance; robustness; stability.

Figure 1

(A) A basic concept of stability-related properties. Against external and internal perturbations, the system adapts its state, which in turn may affect its functioning. Stability-related concepts such as resilience, resistance, and robustness are higher-order properties characterized by the system's response to imposed perturbations in terms of state, S or function F. In contrast, homeostasis is specifically confined to the system's ability to maintain or recover its state. (B) Resilience in compositionally complex, natural communities (left panel) and structurally simple, engineered consortia (right panel). On the left panel, the sequential changes from S₁ to S₃ and from F₁ to F₂, respectively, represent a temporal transition in state and function, right after disturbance. The linkage between function and state becomes weak on the flat bottom. The right panel shows the change of the profile from natural (dotted line) to engineered settings (solid line). (C) Stability landscape displaying the transition in state and function by perturbations. Three distinct wells denote domains of attractions (or regimes). The shift to a new regime may cause a significant change in state, but not in function (e.g., the transition between F₁ and F₂) or both in state and function (e.g., the transition between F₂ and F₃). (D) Hysteresis behaviors in microbial communities. The solid and dotted lines denote stable and unstable steady states, and the shaded area represents the infeasible domain that is inaccessible. Two stable branches (i.e., lower and upper) represent the reproducibly-observed relationship between environmental variables and community function. In the left panel, the community is initially on a lower, stable branch (i.e., F₁). With the gradual change in an environmental variable, the community accordingly changes its composition and functional values; when it crosses a tipping point, the community undergoes abrupt changes in composition and function and arrives at an upper branch (i.e., F₁). The original state and function are recovered when environmental variables decrease back through another drastic change in composition and function along the opposite direction on crossing another tipping point. In contrast, the right panel shows the case where recovery is impossible, e.g., due to the loss of member species or function during transition that results in a change in the shape of the hysteresis curve (as indicated by red line). In the case of repeated perturbation, member species or functions may be sequentially lost, and we expect the shape of the hysteresis curve to change incrementally over time in coordination with a community's compositional or functional drift.