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.