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

IntroductionBioconvection, a phenomenon characterized by the collective upward swimming of motile microorganisms, has mainly been investigated within controlled laboratory settings, leaving a knowledge gap regarding its ecological implications in natural aquatic environments. This study aims to address this question by investigating the influence of bioconvection on the eco-physiology of the anoxygenic phototrophic sulfur bacteria community of meromictic Lake Cadagno.MethodsHere we comprehensively explore its effects by comparing the physicochemical profiles of the water column and the physiological traits of the main populations of the bacterial layer (BL). The search for eco-physiological effects of bioconvection involved a comparative analysis between two time points during the warm season, one featuring bioconvection (July) and the other without it (September).ResultsA prominent distinction in the physicochemical profiles of the water column centers on light availability, which is significantly higher in July. This minimum threshold of light intensity is essential for sustaining the physiological CO2 fixation activity of Chromatium okenii, the microorganism responsible for bioconvection. Furthermore, the turbulence generated by bioconvection redistributes sulfides to the upper region of the BL and displaces other microorganisms from their optimal ecological niches.ConclusionThe findings underscore the influence of bioconvection on the physiology of C. okenii and demonstrate its functional role in improving its metabolic advantage over coexisting phototrophic sulfur bacteria. However, additional research is necessary to confirm these results and to unravel the multiscale processes activated by C. okenii’s motility mechanisms

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

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

Synergistic phenotypic shifts during domestication promote plankton-to-biofilm transition in purple sulfur bacterium Chromatium okenii

The ability to isolate microorganisms from natural environments to pure cultures under optimized laboratory settings has markedly improved our understanding of microbial ecology. Laboratory-induced artificial growth conditions often diverge from those in natural ecosystems, forcing wild isolates into selective pressures which are distinct compared to those in nature. Consequently, fresh isolates undergo diverse eco-physiological adaptations mediated by modification of key phenotypic traits. For motile microorganisms, we still lack a biophysical understanding of the relevant traits which emerge during domestication, and possible mechanistic interrelations between them which could ultimately drive short-to-long term microbial adaptation under laboratory conditions. Here, using microfluidics, atomic force microscopy (AFM), quantitative imaging, and mathematical modelling, we study phenotypic adaptation of natural isolates of Chromatium okenii, a motile phototrophic purple sulfur bacterium (PSB) common to meromictic settings, grown under ecologically-relevant laboratory conditions over multiple generations. Our results indicate that the naturally planktonic C. okenii populations leverage synergistic shifts in cell-surface adhesive interactions, together with changes in their cell morphology, mass density, and distribution of intracellular sulfur globules, to suppress their swimming traits, ultimately switching to a sessile lifeform under laboratory conditions. A computational model of cell mechanics confirms the role of the synergistic phenotypic shifts in suppressing the planktonic lifeform. Over longer domestication periods (~10 generations), the switch from planktonic to sessile lifeform is driven by loss of flagella and enhanced adhesion. By investigating key phenotypic traits across different physiological stages of lab-grown C. okenii, we uncover a progressive loss of motility via synergistic phenotypic shifts during the early stages of domestication, which is followed by concomitant deflagellation and enhanced surface attachment that ultimately drive the transition of motile sulphur bacteria to a sessile biofilm state. Our results establish a mechanistic link between suppression of motility and surface attachment via synergistic phenotypic changes, underscoring the emergence of adaptive fitness under felicitous laboratory conditions that comes at a cost of lost ecophysiological traits tailored for natural environments

Bioconvection-Mediated Microbial Ecophysiology in the Chemocline of Meromictic Lake Cadagno

Meromictic Lake Cadagno is a permanently redox-stratified lake in the Swiss Alps. This environment supports the growth of a dense community of anoxygenic phototrophic sulfur bacteria that form a distinct bacterial layer (BL) between the two layers, in the chemocline. The study aimed to investigate the eco-physiological consequences of bioconvection, a phenomenon of self-sustaining transport driven by motile microorganisms in response to light and oxygen. Our research included laboratory and field experiments that revealed phenotypic cell changes and metabolic activity in response to fluctuations in various physicochemical parameters between the wild and lab-grown bacterial populations. The seasonal dynamics of bioconvection and its impact on microbial ecophysiology were also investigated. The results highlight how bioconvection affects fitness and ecological niches within the bacterial community. Overall, the results indicate that bioconvection provides a competitive advantage to the responsible species, the motile bacterium Chromatium okenii, over the other anoxygenic phototrophs in the BL.</p

Anoxygenic photo- and chemo-synthesis of phototrophic sulfur bacteria from an alpine meromictic lake

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