Microbes are the most common form of life on Earth and, unsurprisingly, their interactions with each other as well as plants and animals shape almost every level of biological organization from individual organisms to global level processes like the carbon cycle. However, even though we recognize that microbes are integral to ecosystem functioning and trillions of dollars of the ecosystem services we rely on across the globe, we know surprisingly little about how microbial communities and interactions function. This is especially pertinent given that ecosystems across the world are being pushed to new extremes under human-induced global change. Consequently, the vast gap in our knowledge of mechanisms underlying microbial communities and interactions likely means we are running into new climate extremes with almost no idea about whether these fundamental communities can continue to support ecosystems or exacerbate their breakdown.
My research in Michelle E. Afkhami’s lab focuses on understanding how microbes reorganize their interactions in response to ever increasing levels of global change. I take a multi-level, holistic approach in understanding the mechanisms underlying restructuring of microbial interactions under stress by studying, for example, 1) changes in stability of whole microbial communities along natural stress gradients, 2) how limitations along many environmental characteristics like temperature and nutrient content potentially makes microbes more susceptible to disturbances, and 3) how environmental stress has shaped the evolution of host genomes to mediate stress relief provided by microbes.
(1) Environmental stress is destabilizing microbial communities.
A major question in the ecology of microbiomes in new stressful environments revolves around how resistant/resilient microbial communities are in response to stress. We addressed this by comparing how microbes associate with one another across a well-characterized and highly replicated natural stress gradient (i.e., water and nutrient stress gradient) at Archbold Biological Station in Central Florida along the Lake Wales Ridge.
We found that, as communities experience more long-term stress, they become less compartmentalized and become more dominated by positive associations both of which are important characteristics of unstable communities. What this effectively means is that communities that experience long-term stress may be good at mediating that specific long-term stressor, but they are less able to withstand disturbances and/or new stressors. The overrepresentation of positive associations in high stress communities likely reflects reliance on microbial partners to manage that stress. For example, approximately 67% of fungal communities in our highest stress environment were plant-beneficial fungi – ectomycorrhizae. However, that means the abundance of positively associated taxa in high stress environments are inextricably linked. A disturbance to one of those partners means a disturbance to the other(s) because the other microbe(s) rely on the disturbed partner to persist under high stress which can be further intensified by the loss of compartmentalization.
(2) Important microbes are more limited in the environments they can withstand.
“Microbes are everywhere” is a common refrain, but where specific microbes can exist is an open question. We asked how microbial niches – the range in environmental conditions that microbes can withstand – are shaped along many environmental characteristics. What we found was that >90% of microbes have only one of two opposing types of niches: 1) multidimensional generalization in which microbes can withstand a diverse array of environmental conditions along all of our tested characteristics (the “Microbes are everywhere” adherents) and 2) multidimensional specialists in which microbes find tolerable vary narrow ranges along all of our tested characteristics (the extremely sensitive microbes).
The limitations into these two niche types are not just a quirk of microbial ecology but have significant implications for whole communities. While multidimensional specialists are likely more susceptible to environmental disturbances because they can only withstand very narrow ranges of environmental conditions, they are surprisingly more central to their communities providing important services such as pollutant detoxification, nutrient cycling, etc. The takeaway here is that microbial communities may again struggle to limit effects of disturbance because the most structurally important microbes are limited in the kinds of conditions they can withstand.
(3) Gene family expansions shape the gene expression and population genetics underlying plant host regulation of microbial partners.
Macroorganisms like plants and animals host microbes to alleviate environmental stress. But, how beneficial or whether the host-microbe interaction is beneficial at all depends on the environmental context in which the interaction occurs (i.e., context-dependency). Context-dependency is a universal feature of all interspecific interactions. However, we are missing a mechanistic framework to identify the specific players (e.g., molecular pathways) that regulate interspecific interactions in different contexts.
My work has found that gene family expansions are integral to the regulation of context-dependency in the ecologically and agriculturally significant interaction between plants and arbuscular mycorrhizal (AM) fungi. By expanding gene families important in the interaction of plants and AM fungi, plants create the necessary genetic complexity to regulate gene expression in response to multiple environmental cues, restriction to specific cell types, etc. We found that these larger gene families contain more genes that are expressed context-dependently thus highlighting that extant plants are disproportionately targeting larger gene families during AM symbiosis under environmental stress. In fact, these larger gene families are so important for AM symbiosis that they experience stronger selective pressure by changes in soil chemistry in >100 naturally-occurring populations of the model legume Medicago truncatula and contain more genetic variation associated with fitness benefits of interacting with AM fungi across >200 naturally-occurring populations of M. truncatula. Thus, my work demonstrates an important ecoevolutionary principle of context-dependency in host-microbe interactions that could be generalized to other kinds of host-microbe associations beyond just the one between plants and AM fungi.
