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

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.
Competing Interests: The authors have declared that no competing interests exist.
(Copyright: © 2024 Di Nezio et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)