Leveraging DNA and RNA oscillatory dynamics to investigate the ecology and physiology of a freshwater microbial community

Abstract

The dynamics of microbial communities in temporally varying environments are often mediated by the physiological responses of their members. However, physiological measurements remain difficult to obtain \textit{in situ} from diverse communities in nature, limiting our understanding of microbial community dynamics in changing environments. Here, we investigate the physiological dynamics of a microbial community by applying a macroecological approach to a multi-year timeseries of paired ribosomal RNA (rRNA) and DNA (rDNA) measurements from a freshwater community, interpreting their relationship by developing a model of microbial physiology. Leveraging the existence of seasonal oscillations, we developed a data-driven minimal model that provided macroecological predictions and interpretations of rDNA, rRNA, and their relationship. Using this model, we examined two macroecological patterns with physiological interpretations: 1) time averaged rRNA:rDNA as a measure of a community member's steady-state and 2) the temporal ordering of rRNA fluctuations relative to rDNA. We found that rRNA:rDNA increased with the number of 16S rRNA operon copies, which in the context of our model suggests a superlinear effect of copy number. Temporal fluctuations of rRNA tended to \textit{precede} those of rDNA, consistent with the view that increases in ribosomal content can lead to future biomass. We then identified environmental variables where rRNA and rRNA:rDNA displayed greater sensitivity than rDNA, reasoning that rRNA:rDNA, as a reflection of the growth rate, may respond more strongly to environmental change. The ratio rRNA:rDNA provided greater sensitivity than rDNA for the majority of the aquatic environmental variables tested, particularly those reflecting the degree of eutrophy vs. oligotrophy. The results of this work indicate that the ratio rRNA:rDNA may be underutilized as a measure of the physiological state of natural communities.