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

Di Nezio, Francesco; Roman, Samuele; Buetti-Dinh, Antoine; Sepúlveda Steiner, Oscar; Bouffard, Damien; Sengupta, Anupam; Storelli, Nicola

doi:10.3389/fmicb.2023.1253009

Cited by 3 publications

References 81 publications

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Self‐organization of active plume lattice in bacterial bioconvection

Liu,

Hou,

Kearns

et al. 2024

Quant. Biol.

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Self‐organized pattern formation is common in biological systems. Microbial populations can generate spatiotemporal patterns through various mechanisms, such as chemotaxis, quorum sensing, and mechanical interactions. When their motile behavior is coupled to a gravitational potential field, swimming microorganisms display a phenomenon known as bioconvection, which is characterized by the pattern formation of active cellular plumes that enhance material mixing in the fluid. While bioconvection patterns have been characterized in various organisms, including eukaryotic and bacterial microswimmers, the dynamics of bioconvection pattern formation in bacteria is less explored. Here, we study this phenomenon using suspensions of a chemotactic bacterium Bacillus subtilis confined in closed three‐dimensional (3D) fluid chambers. We discovered an active plume lattice pattern that displays hexagonal order and emerges via a self‐organization process. By flow field measurement, we revealed a toroidal flow structure associated with individual plumes. We also uncovered a power‐law scaling relation between the lattice pattern’s wavelength and the dimensionless Rayleigh number that characterizes the ratio of buoyancy‐driven convection to diffusion. Taken together, this study highlights that coupling between chemotaxis and external potential fields can promote the self‐assembly of regular spatial structures in bacterial populations. The findings are also relevant to material transport in surface water environments populated by swimming microorganisms.

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Self‐organization of active plume lattice in bacterial bioconvection

Liu,

Hou,

Kearns

et al. 2024

Quant. Biol.

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Synergistic phenotypic adaptations of motile purple sulphur bacteria Chromatium okenii during lake-to-laboratory domestication

Di Nezio,

Ong,

Riedel

et al. 2024

PLoS ONE

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Isolating microorganisms from natural environments for cultivation under optimized laboratory settings has markedly improved our understanding of microbial ecology. Artificial growth conditions often diverge from those in natural ecosystems, forcing wild isolates into distinct selective pressures, resulting in diverse eco-physiological adaptations mediated by modification of key phenotypic traits. For motile microorganisms we still lack a biophysical understanding of the relevant traits emerging during domestication and their mechanistic interplay driving short-to-long-term microbial adaptation under laboratory conditions. Using microfluidics, atomic force microscopy, quantitative imaging, and mathematical modeling, we study phenotypic adaptation of Chromatium okenii, a motile phototrophic purple sulfur bacterium from meromictic Lake Cadagno, grown under laboratory conditions over multiple generations. Our results indicate that naturally planktonic C. okenii leverage shifts in cell-surface adhesive interactions, synergistically with changes in cell morphology, mass density, and distribution of intracellular sulfur globules, to suppress their swimming traits, ultimately switching to a sessile lifeform. A computational model of cell mechanics confirms the role of such phenotypic shifts in suppressing the planktonic lifeform. By investigating key phenotypic traits across different physiological stages of lab-grown C. okenii, we uncover a progressive loss of motility during the early stages of domestication, followed by concomitant deflagellation and enhanced surface attachment, ultimately driving the transition of motile sulfur bacteria to a sessile state. Our results establish a mechanistic link between suppression of motility and surface attachment via phenotypic changes, underscoring the emergence of adaptive fitness under laboratory conditions at the expense of traits tailored for natural environments.

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

Storelli,

Steiner,

Nezio

et al. 2024

Preprint

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Lake Cadagno differs from typical alpine lakes as it is stratified into two water layers that never vertically mix. This stratification creates a niche for the development of primordial anoxygenic phototrophs, which thrive in the chemocline of the lake, forming a characteristic bacterial layer (BL). Yet, the relationship between the temporal variation of meteorological factors that regulate stratification and the development of the BL remains unclear. Here, we explored the intra- and inter-seasonal stability of the water column stratification and ecological dynamics of the anoxygenic phototroph community of the BL over three years. Our continuous monitoring showed that the meromixis of the lake is highly stable, with density stratification seemingly unaffected by external meteorological factors. Further reanalysis of the lake’s recent history substantiated this remarkable stability. In contrast, the community of anoxygenic phototrophs showed significant intra- and inter-seasonal variability, modulated by weather events that primarily impacted light penetration. In fact, an exceptional intra-seasonal light increases in September 2020 led to an overgrowth of purple sulfur bacteria compared to commonly dominant, green ones. At the inter-seasonal level, there is a difference in BL development in July 2021, which was characterized by much precipitation and less light, compared with that in 2019/2020.

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

Cited by 3 publications

References 81 publications

Self‐organization of active plume lattice in bacterial bioconvection

Self‐organization of active plume lattice in bacterial bioconvection

Synergistic phenotypic adaptations of motile purple sulphur bacteria Chromatium okenii during lake-to-laboratory domestication

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

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