Principles for engineering microbial composition and ecosystem functioning

Abstract

Microbial probiotics are designed to improve functions in diverse ecosystems, yet probiotics often fail to have the desired beneficial effects. The introduction of probiotics to an environment with a preexisting microbiome is analogous to an invasion event, but is rarely considered in this light. Here, we tested the relative importance of propagule pressure (inoculation dose and frequency) compared to biotic interactions (composition of introduced and resident communities) in driving microbial composition and functional outcomes following microbial community invasions in experimental microcosms. Ecosystem functioning was assessed through measurements of CO2 production and DOC (dissolved organic carbon) accumulation, an activity and an environmental modification metric, respectively. Further, to test the dependence of propagule pressures versus biotic interactions was dependent on environmental context, experiments were performed on two different substrates, R2A agar and plant litter. In both environments, we found that biotic interactions were more important than propagule pressure in driving microbial composition. Moreover, bacteria were more successful invaders than fungi. While successful invasion is a first step, ultimately the success of microbial invasions in microbiome engineering applications is measured by the impact on ecosystem functioning. As with shaping the microbiome composition, biotic interactions were key to functional outcomes, but the magnitude of the functional impact varied by environment. Identifying general principles that determine the community composition and functioning following microbial invasions is key to efficient community engineering.\n\nSignificanceWith increasing frequency humans are introducing new microbes into pre-existing microbiomes to alter functioning. Examples include, modification of microflora in human guts for better health, and soil for food security and/or climate management. Probiotic applications are often approached as trial-and-error endeavors and have mixed outcomes. We propose that increased success in microbiome engineering may be achieved by better understanding of microbial invasions. We conducted a microbial community invasion experiment, to test the relative importance of propagule pressure and biotic interactions in driving microbial community composition and ecosystem functioning in microcosms. We found that biotic interactions were more important than propagule pressure in determining the impact of microbial invasions. Furthermore, the principles for community engineering vary among organismal groups (bacteria versus fungi).