Collaborative Research: Linking microbial social interactions within soil aggregate communities to ecosystem C, N, and P cycling

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Most people would never imagine that single-celled bacteria could recognize their neighbors, communicate with one another, and make decisions about whether to cooperate. Curiously, evidence suggests that bacteria can be credited with social behavior and decision-making abilities. Despite the increasing acceptance of the idea of social behavior and communication in bacteria, it is not yet known how these small scale behaviors influence microbial community interactions in nature. This study will provide the first test of whether microbial social interactions lead to impacts in function at the ecosystem level using microbial communities from both natural grassland and agricultural soil. Communication in the form of chemical signals that can be detected by bacteria will influence whether cells will make various extracellular enzymes that degrade plant matter. The social organization of these bacterial communities could allow for a division of labor, with some species contributing one set of enzymes and other species contributing different ones, thereby increasing the efficiency of organic matter decomposition. In this way, social interactions among bacteria could influence how well the entire ecosystem works. The research will also provide training opportunities for graduate and undergraduate students at a Hispanic-Serving Institution. Students will gain experience in field, lab, and computational techniques, including bioinformatics and mathematical modeling approaches that link game theory to ecological processes, and will participate in outreach to high school science students and their teacher. In soil, bacteria are most likely to interact with other bacteria within clumps of soil particles known as aggregates. Aggregates give soil a structure, which helps water and oxygen flow, protects carbon in soil, and supports diverse communities of microorganisms. These microbes decompose dead plants and animals, recycle nutrients, and help new plants to thrive. Soil that is mechanically disturbed, for example by plowing, loses many of its aggregates and overall structure. This team of researchers hypothesize that soil aggregates, like those found in prairie soils that have not been farmed for many years, will provide the necessary stability and spatial organization to develop bacterial communities that rely more on communication and cooperation among different species when compared to more recently disturbed soils. Experiments will combine molecular and bioinformatic approaches to study bacteria at fine scales using a low-disturbance method for isolating soil aggregates and a coupled game theory-ecosystem model to connect microbial behavior in soil aggregates to changes in biogeochemical cycling. The researchers will use a well-characterized restoration gradient in a prairie ecosystem, including cultivated sites, restored sites of varying age, and relic prairie with no cultivation history. The overarching goal of this study is to investigate microbial social interactions within soil aggregate communities and their impacts on carbon, nitrogen, and phosphorus cycling at the ecosystem level. Specifically, the study will address two questions: (1) Do stable, biologically active microaggregates foster microbial communities with a higher potential for signaling and communication, with increased metabolic interdependence and division of labor? (2) How does the division of labor within an aggregate community affect ecosystem-level carbon, nitrogen, and phosphorus cycling? Metagenomic and transcriptomic data will be used to parameterize a coupled microbial dynamics-ecosystem model for investigating the roles of microbial social interactions in community assembly and carbon, nitrogen, and phosphorus cycling in soils. The researchers will also train 3 graduate students and 12 undergraduates. This project will also strengthen a research collaboration between their university and The Nature Conservancy, where a graduate student will be trained in field sampling and aggregate sieving techniques through an immersive experience in conservation work. An artist will work with the researchers to develop a virtual reality program to disseminate results of this project to high school students and public visitors to the field site.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.