Abstract
All living cells are characterized by certain cell shapes and sizes. Many bacteria can change these properties depending on the growth conditions. The underlying mechanisms and the ecological relevance of changing cell shape and size remain unclear in most cases. One bacterium that undergoes extensive shape-shifting in response to changing growth conditions is the freshwater bacterium Caulobacter crescentus When incubated for an extended time in stationary phase, a subpopulation of C. crescentus forms viable filamentous cells with a helical shape. Here, we demonstrated that this stationary-phase-induced filamentation results from downregulation of most critical cell cycle regulators and a consequent block of DNA replication and cell division while cell growth and metabolism continue. Our data indicate that this response is triggered by a combination of three stresses caused by prolonged growth in complex medium, namely, the depletion of phosphate, alkaline pH, and an excess of ammonium. We found that these conditions are experienced in the summer months during algal blooms near the surface in freshwater lakes, a natural habitat of C. crescentus, suggesting that filamentous growth is a common response of C. crescentus to its environment. Finally, we demonstrate that when grown in a biofilm, the filamentous cells can reach beyond the surface of the biofilm and potentially access nutrients or release progeny. Altogether, our work highlights the ability of bacteria to alter their morphology and suggests how this behavior might enable adaptation to changing environments.IMPORTANCE Many bacteria drastically change their cell size and morphology in response to changing environmental conditions. Here, we demonstrate that the freshwater bacterium Caulobacter crescentus and related species transform into filamentous cells in response to conditions that commonly occur in their natural habitat as a result of algal blooms during the warm summer months. These filamentous cells may be better able to scavenge nutrients when they grow in biofilms and to escape from protist predation during planktonic growth. Our findings suggest that seasonal changes and variations in the microbial composition of the natural habitat can have profound impact on the cell biology of individual organisms. Furthermore, our work highlights that bacteria exist in morphological and physiological states in nature that can strongly differ from those commonly studied in the laboratory.
Highlights
All living cells are characterized by certain cell shapes and sizes
We found that the combination of low levels of phosphate, alkaline pH, and high levels of ammonium leads to this phenotype and that such conditions occur in the native environment of Caulobacter as a consequence of algal bloom
We studied the morphological transition of the alphaproteobacterium C. crescentus when incubated for several days in stationary phase, during which cells lose their characteristic swarmer and stalked-cell morphologies and instead gain helical filamentous morphologies
Summary
Prolonged growth in complex medium leads to formation of a subpopulation of filamentous cells that can be purified by density gradient centrifugation. We measured the levels of selected proteins by Western blotting (Fig. 3C) These data confirmed that the master cell cycle regulators DnaA, CtrA, GcrA, CcrM, and SciP were eliminated and that the levels of the division protein FtsZ and the translation factor EF-Tu were downregulated in the filamentous cells. The major cell cycle regulators, including CtrA and DnaA, as well as proteins involved in chemotaxis and motility were strongly downregulated during growth in spent medium (Fig. 3A and B; see Fig. 4C). FtsZ, ribosomal proteins, and proteins involved in amino acid metabolism were less strongly downregulated, with levels that resembled those seen in earlystationary-phase cells (Fig. 3A and B; see Fig. 4C) This might be explained by the fact that we supplemented the spent medium with glucose, which was not required for filament formation but which accelerated their emergence and increased the proportion of filamentous cells (Fig. S2).
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