Historical Contingency in Microbial Resilience to Hydrologic Perturbations

Hyun-Seob Song,Timothy D Scheibe,Emily B Graham,James C Stegen

doi:10.3389/frwa.2021.590378

Abstract

Development of reliable biogeochemical models requires a mechanistic consideration of microbial interactions with hydrology. Microbial response to and its recovery after hydrologic perturbations (i.e., resilience) is a critical component to understand in this regard, but generally difficult to predict because the impacts of future events can be dependent on the history of perturbations (i.e., historical contingency). Fundamental issues underlying this phenomenon include how microbial resilience to hydrologic perturbations is influenced by historical contingency and how their relationships vary depending on the characteristics of microbial functions. To answer these questions, we considered a simple microbial community composed of two species that redundantly consume a common substrate but specialize in producing distinct products and developed a continuous flow reactor model where the two species grow with trade-offs along the flow rate. Simulations of this model revealed that (1) the history of hydrologic perturbations can lead to the shifts in microbial populations, which consequently affect the community's functional dynamics, and (2) while historical contingency in resilience was consistently predicted for all microbial functions, it was more pronounced for specialized functions, compared to the redundant function. As a signature of historical contingency, our model also predicted the emergence of hysteresis in the transitions across conditions, a critical aspect that can affect transient formation of intermediate compounds in biogeochemistry. This work presents microbial growth traits and their functional redundancy or specialization as fundamental factors that control historical contingencies in resilience.

Highlights

Interactions between hydrologic and microbial processes control the cycling of dissolved organic matter and other chemical substrates (Covino et al, 2018) in biogeochemical hotspots such as river corridors (Singer et al, 2016; Graham et al, 2019)
Using a model of microbial community growing in a homogenous continuous flow reactor (Figure 1A), we test the following hypotheses: (H1) distinct growth traits and their trade-offs along the flow rate gradient (Figure 1B) leads to the shifts in the community composition subject to hydrologic perturbations with different intervals, (H2) the resulting microbial communities dominated by species 1 or 2 will show distinct responses to future perturbations (Figure 1C), and (H3) the extent of historical contingencies in microbial functions depend on their redundancy or specialization, i.e., whether a given functions is performed in common among multiple species or uniquely associated with specific organisms
A growing body of data indicate critical effects of historical contingency in biogeochemistry and microbial ecology, but theoretical frameworks that can predict the sophisticated behavior of environmental systems are still lacking

Summary

Introduction

Interactions between hydrologic and microbial processes control the cycling of dissolved organic matter and other chemical substrates (Covino et al, 2018) in biogeochemical hotspots such as river corridors (Singer et al, 2016; Graham et al, 2019). Predictive biogeochemical modeling necessitates development of reliable models of the dynamics of microbial populations and their interactions with hydrology For this purpose, it is important to understand how hydrologic inputs alter microbial diversity, abundances, interactions, spatial organization, and functions. Microbial enzyme activity and respiration in soil that increased with moisture were shown to be constrained by previous climate such as precipitation history (Averill et al, 2016; Hawkes et al, 2017). As another example, soil systems showed an enhanced protection of plants against a pathogen through the induced presence of disease-suppressive microbes by pre-exposure to the same pathogen in the past, just like an adaptive human immune system (Raaijmakers and Mazzola, 2016). While a current trend is to increasingly incorporate microbial physiology and processes into biogeochemical models (Wieder et al, 2013; Wang et al, 2017), accounting for historical contingencies still remains a challenge due to the lack of understanding of controlling aspects in microbial systems, severely limiting our ability to reliably predict biogeochemical function (Widder et al, 2016)

Methods

Results

Conclusion