Molecular Basis and Ecological Relevance of Caulobacter Cell Filamentation in Freshwater Habitats

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.

Environmental pH impacts division assembly and cell size inEscherichia coli

“…We observed similar effects of pH on cell area in E. coli strain W3110 and in the evolutionary distant Gram-positive coccus Staphylococcus aureus (SI Appendix, Figure S3). Likewise, during this work two separate studies noted the size of Streptococcus pneumoniae and C. crescentus also increases during growth in alkaline media [23]. Altogether, these findings establish environmental pH as mediator of size across evolutionary distant bacterial species.…”

pH-dependent activation of cytokinesis modulates Escherichia coli cell size

“…The average volume of S. aureus cells was reduced by~48% during growth in acidic (pH 5.5) medium compared to alkaline (pH 8.0) medium (average volume of 1.02 ± 0.03 compared to 2.10 ± 0.17 μm 3 ). Likewise, during this work two separate studies noted the size of Streptococcus pneumoniae and C. crescentus also increases during growth in alkaline medium [25,26]. Altogether, these findings establish environmental pH as a mediator of size across evolutionarily distant bacterial species.…”

Cyanobacterial growth and morphology are influenced by carboxysome positioning and temperature

“…That is, S. elongatus may use temperature as a cue to elongate so as to avoid planktivorous protists. Consistent with this possibility, previous studies have demonstrated that several freshwater bacteria, including Caulobacter crescentus (58), exhibit high phenotypic plasticity and can transition to a filamentous morphology -a transition that may be specifically triggered in the presence of a size-selective protistan predator (63,65,66). It is possible that some aquatic bacteria have evolved to undergo filamentation at temperatures that coincide with grazing season.…”

“…We propose colder temperatures trigger filamentation indirectly as a carbon-limitation response due to the reduced carbon-fixing activity of RuBisCO. Alternatively, transition into a filamentous morphology has been proposed to confer advantages, such as avoiding phagocytosis via the host immune response (54,55,57,61) or to protect against predation in aquatic environments (58,(62)(63)(64). It is attractive to speculate that the growth temperature of 20 o C coincides with the seasonal temperature during which predation occurs (63).…”