Single-cell trait diversity explains niche and fitness differences in aquatic microbial communities

Two fundamental questions in ecology are how biodiversity is maintained and how it affects ecosystem functioning. Until now, it has been difficult to study the above mechanisms in natural microbial communities, yet they are important drivers of biogeochemical ecosystem functions. Here, we use a new approach to define and measure biodiversity in complex lake microbial communities (Lake Cadagno, Switzerland) based on the cell-to-cell variation in multiple functionally relevant phenotypic traits. We use stable isotope probing coupled to correlative imaging using confocal laser scanning microscopy (CLSM) and nanometer-scale secondary ion mass spectrometry (NanoSIMS) to obtain morphological (size), physiological (pigments) and metabolic (carbon and nitrogen isotope uptake and sulfur content) traits for a large number of individual cells along the environmental gradient found across lake depth. We show that cell-to-cell trait variation is significantly correlated with cell densities as a proxy for ecosystem functioning, whereas genetic diversity measured at the level of 16S and 18S is not. Our single-cell analysis provides evidence for a simultaneous increase in niche partitioning (measured as increased evenness in pigment composition) and decrease in fitness differences (measured as decreased variability in sulfur content) due to light limitation and competition for nutrients in deep layers of the lake. This leads to a negative relationship between niche and fitness differences. Our results suggest that niche and fitness differences in natural microbial communities can be understood at the level of single-cell traits, providing a mechanistic understanding of the relationship between microbial diversity and ecosystem functioning.