A conceptual framework to dissect emergent functions in microbial communities

Microbial communities play vital roles in diverse ecosystems and are key drivers of numerous industrial or health-related applications. In many cases, the functional properties microorganisms contribute to these processes cannot be explained by simply adding up the activities of individual strains, but they result from complex interactions among several community members. While it is clear that these so-called emergent functions (EFs) are important for determining collective behaviors of microbial communities, thus far, a systematic framework to identify, classify, and experimentally dissect them has been lacking. Here, we aim at filling this gap by proposing a conceptual framework that defines EFs as community-level traits, which deviate from additive expectations. Depending on the direction of deviation, we distinguish positive from negative emergence. In addition, we define cases of a de novo emergence as those where the focal function is absent in monocultures and only arises upon cocultivation, while modulated functions are already detectable in monocultures, yet shift quantitatively through interaction. We then classify the underlying ecological mechanisms along the two main axes, contact-dependence and regulation, and propose diagnostic experiments to assign microbial systems to these categories. Finally, we address the evolutionary origin of EFs by distinguishing cases that arise spontaneously as by-products from those that have been favored by natural selection and discuss experimental procedures to tell them apart. Together, this new framework will help to identify and characterize emergent functions, thus advancing our mechanistic understanding of microbial community function.