Microbial mitigation–exacerbation continuum: a novel framework for microbiome effects on hosts in the face of stress

Abstract

Abstract. A key challenge to understanding microbiomes and their role in ecological processes is contextualizing their effects on host organisms, particularly when faced with environmental stress. One influential theory, the Stress Gradient Hypothesis, might predict that the frequency of positive interactions increases with stressful conditions such that microbial taxa would mitigate harmful effects on host performance. Yet, equally plausible is that microbial taxa could exacerbate these effects. Here, we introduce the Mitigation-Exacerbation Continuum as a novel framework to conceptualize microbial mediation of stress. We (1) use this continuum to quantify microbial mediation of stress for six plant species and (2) test the association between these continuum values and natural species' abundance. We factorially manipulated a common stress (allelopathy) and the presence of soil microbes to quantify microbial effects in benign and stressed environments for two critical early life-history metrics, seed germination and seedling biomass. Although we found evidence of both mitigation and exacerbation among the six species, exacerbation was more common. Across species, the degree of microbial-mediated effects on germination explained >80% of the variation of natural field abundances. Our results suggest a critical role of soil microbes in mediating plant stress responses, and a potential microbial mechanism underlying species abundance.

Familiar soil conditions help Pinus ponderosa seedlings cope with warming and drying climate

“…The microbial mitigation-exacerbation hypothesis proposes that in response to a stressor, soil microbes may either mitigate or exacerbate stress. The net effects of soil biota are predicted to shift in the direction of mitigation as stress increases, and in the direction of exacerbation in benign, low-stress sites (David et al 2018). This prediction is based upon comparing the effect of live soil biota to sterile soils.…”

“…Fungal symbionts may even facilitate widespread biological invasions of the genus Pinus in what is known as coinvasion (Dickie et al 2010(Dickie et al , 2017. These diverse examples of the influence of soil biota on plant growth are likely dependent on the environmental context (David et al 2018). David et al (2018) coined the idea that in stressful, resource-poor environments microbes may mitigate the effect of stressful environments, while in benign, resource-rich environments they may exacerbate stress (the microbial mitigationexacerbation hypothesis).…”

“…These diverse examples of the influence of soil biota on plant growth are likely dependent on the environmental context (David et al 2018). David et al (2018) coined the idea that in stressful, resource-poor environments microbes may mitigate the effect of stressful environments, while in benign, resource-rich environments they may exacerbate stress (the microbial mitigationexacerbation hypothesis). This complements well-supported ideas that facilitative plant-plant interactions are more common in stressful environments and competitive plant-plant interactions tend to dominate benign environments (the stress gradient hypothesis) (Callaway & Aschehoug 2000;Revillini et al 2016;van der Putten et al 2016;Lekberg et al 2018).…”

Host evolutionary history and ecological context modulate the adaptive potential of the microbiome

“…First, our work contributes to the growing body of literature that environmentally acquired microbes are important in stressful environments. Stressful environments are predicted to increase the relative importance of mutualisms [26][27][28], though how often the microbiome behaves evolutionarily like a traditional mutualism remains contentious [4,5,72]. In plants, stress-adapted soil microbiomes improve germination and seedling survival in stressful environments [73,74], highlighting the importance of early life traits like we also observed for development.…”

“…While the above studies identify key host genotype x microbiome interactions, missing are the environmental effects. Environmental stressors may increase the relative importance of microbial costs or benefits [26][27][28]. For Drosophila, the microbiome may be critical to mitigate dietary stressors, but few studies have tested the role of the microbiome in dietary adaptation.…”