Motile bacteria leverage bioconvection for eco-physiological benefits in a natural aquatic environment

Abstract

AbstractBioconvection, the active self-sustaining transport phenomenon triggered by the accumulation of motile microbes under competing physico-chemical cues, has been long studied, with recent reports suggesting its role in driving ecologically-relevant fluid flows. Yet, how this collective behaviour impacts the ecophysiology of swimming microbes remains unexplored. Here, through physicochemical profiles and physiological characterizations analysis of the permanently stratified meromictic Lake Cadagno, we characterize the community structure of a dense layer of anaerobic phototrophic sulfur bacteria, and report that the associated physico-chemical conditions engender bioconvection when bulk of the motile purple sulfur bacteriumChromatium okeniisynchronize their movement against the gravity direction. The combination of flow cytometry and fluorescentin situhybridization (FISH) techniques uncover the eco-physiological effects resulting from bioconvection, and simultaneous measurements using dialysis bags and14C radioisotope, allowed us to quantifyin situthe diurnal and nocturnal CO2fixation activity of the three co-existing species in the bacterial layer. The results provide a direct measure of the cellular fitness, with comparative transcriptomics data – ofC. okeniipopulations present in regions of bioconvection vis-à-vis populations in bioconvection-free regions – indicating the transcripts potentially involved in the bioconvection process. This work provides direct evidence of the impact of bioconvection onC. okeniimetabolism, and highlights the functional role of bioconvection in enhancing the metabolic advantage ofC. okeniirelative to other microbial species inhabiting the microbial layer.