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Self-propelling and rolling of a sessile-motile aggregate of the bacterium Caulobacter crescentus.

ABSTRACT: Active dispersal of microorganisms is often attributed to the cells' motile organelles. However, much less is known about whether sessile cells can access such motility through aggregation with motile counterparts. Here, we show that the rosette aggregates of the bacterium Caulobacter crescentus, although predominantly sessile, can actively disperse through the flagellar motors of motile members. Comparisons in kinematics between the motile rosettes and solitary swimming cells indicate that the rosettes can be powered by as few as a single motor. We further reconstructed the 3D movements of the rosettes to reveal that their proximity to a solid-liquid interface promotes a wheel-like rolling, as powered by the flagellar torque. This rolling movement also features a sequence of sharp turns, a reorientation mechanism distinct from that of swimming cells. Overall, our study elucidates an unexplored regime of aggregation-based motility that can be widely applied to sessile-motile composites.

SUBMITTER: Zeng Y

PROVIDER: S-EPMC7568532 | biostudies-literature | 2020 Oct

REPOSITORIES: biostudies-literature

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Self-propelling and rolling of a sessile-motile aggregate of the bacterium Caulobacter crescentus.

Zeng Yu Y Liu Bin B

Communications biology 20201016 1

Active dispersal of microorganisms is often attributed to the cells' motile organelles. However, much less is known about whether sessile cells can access such motility through aggregation with motile counterparts. Here, we show that the rosette aggregates of the bacterium Caulobacter crescentus, although predominantly sessile, can actively disperse through the flagellar motors of motile members. Comparisons in kinematics between the motile rosettes and solitary swimming cells indicate that the ...[more]

PMID: 33067555

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Project description:In this study, we characterize the response of the free-living oligotrophic alphaproteobacterium Caulobacter crescentus to low temperatures by global transcriptomic analysis. Our results showed that 656 genes were upregulated and 619 were downregulated at least 2-fold after a temperature downshift. The identified differentially expressed genes (DEG) belong to several functional categories, notably inorganic ion transport and metabolism, and a subset of these genes had their expression confirmed by reverse transcription quantitative real-time PCR (RT-qPCR). Several genes belonging to the ferric uptake regulator (Fur) regulon were downregulated, indicating that iron homeostasis is relevant for adaptation to cold. Several upregulated genes encode proteins that interact with nucleic acids, particularly RNA: cspA, cspB, and the DEAD box RNA helicases rhlE, dbpA, and rhlB. Moreover, 31 small regulatory RNAs (sRNAs), including the cell cycle-regulated noncoding RNA (ncRNA) CcnA, were upregulated, indicating that posttranscriptional regulation is important for the cold stress response. Interestingly, several genes related to transport were upregulated under cold stress, including three AcrB-like cation/multidrug efflux pumps, the nitrate/nitrite transport system, and the potassium transport genes kdpFABC. Further characterization showed that kdpA is upregulated in a potassium-limited medium and at a low temperature in a SigT-independent way. kdpA mRNA is less stable in rho and rhlE mutant strains, but while the expression is positively regulated by RhlE, it is negatively regulated by Rho. A kdpA-deleted strain was generated, and its viability in response to osmotic, acidic, or cold stresses was determined. The implications of such variation in the gene expression for cold adaptation are discussed. IMPORTANCE Low-temperature stress is an important factor for nucleic acid stability and must be circumvented in order to maintain the basic cell processes, such as transcription and translation. The oligotrophic lifestyle presents further challenges to ensure the proper nutrient uptake and osmotic balance in an environment of slow nutrient flow. Here, we show that in Caulobacter crescentus, the expression of the genes involved in cation transport and homeostasis is altered in response to cold, which could lead to a decrease in iron uptake and an increase in nitrogen and high-affinity potassium transport by the Kdp system. This previously uncharacterized regulation of the Kdp transporter has revealed a new mechanism for adaptation to low temperatures that may be relevant for oligotrophic bacteria.

Project description:Bacterial cells maintain sophisticated levels of intracellular organization that allow for signal amplification, response to stimuli, cell division, and many other critical processes. The mechanisms underlying localization and their contribution to fitness have been difficult to uncover, due to the often challenging task of creating mutants with systematically perturbed localization but normal enzymatic activity, and the lack of quantitative models through which to interpret subtle phenotypic changes. Focusing on the model bacterium Caulobacter crescentus, which generates two different types of daughter cells from an underlying asymmetric distribution of protein phosphorylation, we use mathematical modeling to investigate the contribution of the localization of histidine kinases to the establishment of cellular asymmetry and subsequent developmental outcomes. We use existing mutant phenotypes and fluorescence data to parameterize a reaction-diffusion model of the kinases PleC and DivJ and their cognate response regulator DivK. We then present a systematic computational analysis of the effects of changes in protein localization and abundance to determine whether PleC localization is required for correct developmental timing in Caulobacter. Our model predicts the developmental phenotypes of several localization mutants, and suggests that a novel strain with co-localization of PleC and DivJ could provide quantitative insight into the signaling threshold required for flagellar pole development. Our analysis indicates that normal development can be maintained through a wide range of localization phenotypes, and that developmental defects due to changes in PleC localization can be rescued by increased PleC expression. We also show that the system is remarkably robust to perturbation of the kinetic parameters, and while the localization of either PleC or DivJ is required for asymmetric development, the delocalization of one of these two components does not prevent flagellar pole development. We further find that allosteric regulation of PleC observed in vitro does not affect the predicted in vivo developmental phenotypes. Taken together, our model suggests that cells can tolerate perturbations to localization phenotypes, whose evolutionary origins may be connected with reducing protein expression or with decoupling pre- and post-division phenotypes.

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Self-propelling and rolling of a sessile-motile aggregate of the bacterium Caulobacter crescentus.

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Self-propelling and rolling of a sessile-motile aggregate of the bacterium Caulobacter crescentus.

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