Collaborative Research: Within-host Microbial Communities: Experimentally Scaling Interaction Dynamics Across Sites, Regions, and Continents

The fungal, bacterial, and viral microbial communities embedded within organisms are extremely diverse and encode the vast majority of genes in the biosphere. For example, microbes in a human account for 100 times more genes than those of their host; similar results are emerging for virtually all free-living organisms. Disease is the best studied host-microbe interaction, but microbes inside hosts also are responsible for critical functions such as disease resistance as well as nutrient uptake and defense against herbivores (plants), and digestion and reduced inflammatory responses (animals). Yet, in spite of the tremendous diversity and importance of microbes to free-living organisms, there is no predictive understanding of the factors controlling within-host microbial community composition or the spatial scales at which environmental changes affect host and microbial community interactions and functions. Even as human activities lead to increased nitrogen and phosphorus inputs and increased rates of species invasions and extinctions, impacting biological systems at scales ranging from individuals to continents, we know little of the effects of these changes on microbial communities within hosts. This award will provide the first systematic understanding of the responses of plant microbial communities to these pervasive environmental changes on a global scale and provide critically important information on the potential role of microbes in plant productivity, knowledge necessary for feeding a growing human population (9 billion by 2050). This award provides funds to use experiments of unprecedented scale to examine the environmental factors controlling a plant host's fungal, bacterial, and viral microbes at scales ranging from individual plants to regional and global bioclimatic and soil gradients. Using quantitative models to examine multi-scale empirical data, the project team's work will answer three questions. 1) What factors most strongly control microbial communities within hosts across global, continental, regional, and local scales? 2) How does the within-host microbial community affect host reproduction and susceptibility to disease-causing microbes? And 3) how do the symbiotic microbial communities within a host affect the growth, competitive ability, and successful transmission of microbes? The research will encompass replicated experiments in 30 grasslands spanning six continents, representing globally-relevant variation in soil nutrients. Concurrent collection of data from locally common grass hosts as well as a planted crop host (barley) within experimental nutrient and herbivory treatments will be used to discern the effects of symbiotic microbes on plant host health and to distinguish these from other large-scale factors such as climate and the specific microbes found in each location. High-throughput sequencing will be used to determine variation in within-host microbial communities at scales ranging from meters to continents. Manipulative experiments and data modeling will clarify the effect of microbial communities on host reproduction, resistance to microbial disease, and the spread of microbes and disease.

Broader Impacts: Grassland communities cover 30% of Earth's ice-free surface, and occur across greatly varying climatic conditions. Grasslands are essential ecosystems that provide food and forage for domesticated and wild animal populations. In this research, grasslands provide an experimental system with which to understand the ecological processes driving microbial community composition and its effects on plant host growth and reproduction. Results of this work have great potential for refining medical and agricultural applications by illuminating the role of microbial communities in the health of their hosts, and the scales at which environment, space, and time most affect host-microbe interactions. Results may identify novel mechanisms of plant resistance to crop pathogens and will contribute significantly to existing microbial sequence databases linked to LTER and NEON sites and priorities. The research group will communicate this work to K-12 children, undergraduates, and the general public via collaborations with Cedar Creek LTER and the Bell Museum of Natural History. All microbial data and living culture collections will be made publicly available, further enhancing research infrastructure and providing a rich resource for further discovery. As always, the project PIs will prioritize involvement of underrepresented groups and disseminate results in peer-reviewed journals.