Meromictic lakes are interesting ecosystems to study anaerobic microorganisms due their permanent stratification allowing the formation of a stable anoxic environment. The crenogenic meromictic Lake Cadagno harbors an important community of anoxygenic phototrophic sulfur bacteria responsible for almost half of its total productivity. Besides their ability to fix CO2 through photosynthesis, these microorganisms also showed high rates of dark carbon fixation via chemosyntesis. Here, we grew in pure cultures three populations of anoxygenic phototrophic sulfur bacteria previously isolated from the lake, accounting for 72.8% of the total microbial community, and exibiting different phenotypes: 1) the motile, large-celled purple sulfur bacterium (PSB) Chromatium okenii, 2) the small-celled PSB Thiodictyon syntrophicum, and 3) the green sulfur bacterium (GSB) Chlorobium phaeobacteroides. We measured their ability to fix CO2 through photo- and chemo-synthesis, both in situ in the lake and in laboratory under different incubation conditions. We also evaluated the efficiency and velocity of H2S photo-oxidation, an important reaction in the anoxygenic photosynthesis process. Our results confirm that phototrophic sulfur bacteria strongly fix CO2 in the presence of light and that oxygen increases chemosynthesis at night, in laboratory conditions. Moreover, substancial differences were displayed between the three selected populations in terms of activity and abundance.

Bioconvection, 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 bacterium Chromatium okenii synchronize their movement against the gravity direction. The combination of flow cytometry and fluorescent in situ hybridization (FISH) techniques uncover the eco-physiological effects resulting from bioconvection, and simultaneous measurements using dialysis bags and 14C radioisotope, allowed us to quantify in situ the diurnal and nocturnal CO2 fixation 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 - of C. okenii populations present in regions of bioconvection vis-a-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 on C. okenii metabolism, and highlights the functional role of bioconvection in enhancing the metabolic advantage of C. okenii relative to other microbial species inhabiting the microbial layer.