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

Abstract

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.

Ecological dynamics of anoxygenic phototrophs in stably redox-stratified waters: Intra and inter-seasonal variability of Lake Cadagno

“…4C), contrary to what is usually observed (Fig. 4B) 22,34 . This situation also has an effect on the whole trophic network of Lake Cadagno, given the higher biovolume (Fig.…”

“…Previous studies, often conducted over one or a few days of sampling, have generally reported a certain regularity in the shift from a strong presence of large cells PSB C. okenii in early summer to an increase in the other phenotypic groups, namely small cells PSB and two GSB species in September 22,23,34,35 . While this pattern was evident in 2019, distinct ecological dynamics were observed in 2020 and 2021 (Fig.…”

“…Moreover, during July, PSB C. okenii produced an additional mixing process in the BLbioconvection 24,25,42 . The resulting (biogenic) turbulent mixing also displaces small PSB and GSB cells out of the APZ 34 , which are incapable of resisting the transport caused by the stirring as they move passively through gas vacuoles 8,43 . To summarize, weather conditions are essential for the ecological dynamics of BL anoxygenic phototroph organisms, as they determine the quantity and quality of light available to them in the APZ and, consequently, their growth rate.…”

“…3, fourth row, FTU). The increase in turbidity above 10 FTU is generated by the wide variety of anoxygenic phototrophs (7 PSB and 2 GSB) concentrated in the upper part of the anoxic zone where light penetrates, referred to as the anoxygenic photosynthetic zone (APZ) 34 . During the sampling season (June to October), the BL can be as thick as 1.5 meters (Fig.…”