Review

Authors: Kathrin S Fröhlich, Manuel Velasco Gomariz

In the past decades, Caulobacter crescentus has been extensively studied, mostly regarding its dimorphic, asymmetric life cycle. Its distinct mode of reproduction and the need to optimally adapt to ever-changing environmental conditions require tight coordination of gene regulation. Post-transcriptional regulation through non-coding RNAs and RNA-binding proteins constitutes an important layer of expression control in bacteria, but its principles and mechanisms in Caulobacter have only recently been explored. RNA-binding proteins including the RNA chaperone Hfq and ribonuclease RNase E contribute to the activity of regulatory RNAs. Riboswitches and RNA thermometers govern expression of downstream open reading frames, while the small regulatory RNAs CrfA, ChvR and GsrN instead control targets encoded in trans by direct base-pairing interactions.

Topics: Bacterial Proteins; Base Pairing; Caulobacter crescentus; Gene Expression Regulation, Bacterial; RNA, Bacterial; RNA, Messenger; RNA, Small Untranslated

PubMed: 33529919
DOI: 10.1016/j.mib.2021.01.002

Review

Authors: Gregory B Whitfield, Yves V Brun

Bacteria utilize type IV pili (T4P) to interact with their environment, where they facilitate processes including motility, adherence, and DNA uptake. T4P require multisubunit, membrane-spanning nanomachines for assembly. The tight adherence (Tad) pili are an Archaea-derived T4P subgroup whose machinery exhibits significant mechanistic and architectural differences from bacterial type IVa and IVb pili. Most Tad biosynthetic genes are encoded in a single locus that is widespread in bacteria due to facile acquisition via horizontal gene transfer. These loci experience extensive structural rearrangements, including the acquisition of novel regulatory or biosynthetic genes, which fine-tune their function. This has permitted their integration into many different bacterial lifestyles, including the Caulobacter crescentus cell cycle, Myxococcus xanthus predation, and numerous plant and mammalian pathogens and symbionts.

Topics: Fimbriae, Bacterial; Caulobacter crescentus; Bacteria; Bacterial Adhesion; Gene Transfer, Horizontal; Fimbriae Proteins; Bacterial Proteins; Myxococcus xanthus

PubMed: 38579360
DOI: 10.1016/j.mib.2024.102468

Review

Authors: Clare L Kirkpatrick, Patrick H Viollier

Caulobacter crescentus uses a multi-layered system of oscillating regulators to program different developmental fates into each daughter cell at division. This is achieved by superimposing gene expression, subcellular localization, phosphorylation, and regulated proteolysis to form a complex regulatory network that integrates chromosome replication, segregation, polar differentiation, and cytokinesis. In this review, we outline the current state of research in the field of Caulobacter development, emphasizing new findings that elaborate how the developmental program is modulated by factors such as the environment or the metabolic state of the cell.

Topics: Caulobacter crescentus; Cell Division; Gene Expression Regulation; Signal Transduction

PubMed: 22091823
DOI: 10.1111/j.1574-6976.2011.00309.x

Review

Authors: Justine Collier

Caulobacter crescentus is a free-living Alphaproteobacterium that thrives in oligotrophic environments. This review focuses on the regulatory network used by this bacterium to control the levels of cell division proteins, their organization inside the cell and their activity as a function of the cell cycle. Strikingly, C. crescentus makes frequent use of master transcriptional regulators and epigenetic signals, most likely to synchronize cell division with other events of the cell cycle. In addition, cellular metabolism and DNA damage sensors emerge as central players regulating cell division in response to changing environmental conditions.

Topics: Bacterial Proteins; Caulobacter crescentus; Cell Division; DNA Damage; Gene Expression Regulation, Bacterial; Gene Regulatory Networks; Stress, Physiological

PubMed: 29715525
DOI: 10.1016/j.bbagrm.2018.04.005

Review

Authors: Jordan M Barrows, Erin D Goley

First isolated and classified in the 1960s, Caulobacter crescentus has been instrumental in the study of bacterial cell biology and differentiation. C. crescentus is a Gram-negative alphaproteobacterium that exhibits a dimorphic life cycle composed of two distinct cell types: a motile swarmer cell and a nonmotile, division-competent stalked cell. Progression through the cell cycle is accentuated by tightly controlled biogenesis of appendages, morphological transitions, and distinct localization of developmental regulators. These features as well as the ability to synchronize populations of cells and follow their progression make C. crescentus an ideal model for answering questions relevant to how development and differentiation are achieved at the single-cell level. This review will explore the discovery and development of C. crescentus as a model organism before diving into several key features and discoveries that have made it such a powerful organism to study. Finally, we will summarize a few of the ongoing areas of research that are leveraging knowledge gained over the last century with C. crescentus to highlight its continuing role at the forefront of cell and developmental biology.

Topics: Caulobacter crescentus; Cell Cycle; Cell Division; Bacterial Proteins

PubMed: 36715542
DOI: 10.1128/jb.00384-22

Authors: Yoann G Santin, Adrià Sogues, Yvann Bourigault...

Predatory bacteria feed upon other bacteria in various environments. Bdellovibrio exovorus is an obligate epibiotic predator that attaches on the prey cell surface, where it grows and proliferates. Although the mechanisms allowing feeding through the prey cell envelope are unknown, it has been proposed that the prey's proteinaceous S-layer may act as a defensive structure against predation. Here, we use time-lapse and cryo-electron microscopy to image the lifecycle of B. exovorus feeding on Caulobacter crescentus. We show that B. exovorus proliferates by non-binary division, primarily generating three daughter cells. Moreover, the predator feeds on C. crescentus regardless of the presence of an S-layer, challenging its assumed protective role against predators. Finally, we show that apparently secure junctions are established between prey and predator outer membranes.

Topics: Caulobacter crescentus; Cryoelectron Microscopy; Bdellovibrio; Cell Membrane; Bacterial Proteins; Membrane Glycoproteins; Time-Lapse Imaging

PubMed: 38678033
DOI: 10.1038/s41467-024-48042-5

Authors: Maeve McLaughlin, Aretha Fiebig, Sean Crosson...

The xenobiotic response element (XRE) family of transcription factors (TFs), which are commonly encoded by bacteria and bacteriophage, regulate diverse features of bacterial cell physiology and impact phage infection dynamics. Through a pangenome analysis of Caulobacter species isolated from soil and aquatic ecosystems, we uncovered an apparent radiation of a paralogous XRE TF gene cluster, several of which have established functions in the regulation of holdfast adhesin development and biofilm formation in C. crescentus. We further discovered related XRE TFs throughout the class Alphaproteobacteria and its phages, including the φCbK Caulophage, suggesting that members of this cluster impact host-phage interactions. Here we show that a closely related group of XRE transcription factors encoded by both C. crescentus and φCbK can physically interact and function to control the transcription of a common gene set, influencing processes including holdfast development and the production of φCbK virions. The φCbK-encoded XRE paralog, tgrL, is highly expressed at the earliest stages of infection and can directly inhibit transcription of host genes including hfiA, a potent holdfast inhibitor, and gafYZ, an activator of prophage-like gene transfer agents (GTAs). XRE proteins encoded from the C. crescentus chromosome also directly repress gafYZ transcription, revealing a functionally redundant set of host regulators that may protect against spurious production of GTA particles and inadvertent cell lysis. Deleting the C. crescentus XRE transcription factors reduced φCbK burst size, while overexpressing these host genes or φCbK tgrL rescued this burst defect. We conclude that this XRE TF gene cluster, shared by C. crescentus and φCbK, plays an important role in adhesion regulation under phage-free conditions, and influences host-phage dynamics during infection.

Topics: Transcription Factors; Bacteriophages; Caulobacter; Ecosystem; Xenobiotics; Caulobacter crescentus; Adhesins, Bacterial; Response Elements

PubMed: 37972151
DOI: 10.1371/journal.pgen.1011048

Authors: Hunter North, Maeve McLaughlin, Aretha Fiebig...

A suite of molecular sensory systems enables to control growth, development, and reproduction in response to levels of essential elements. The bacterial enhancer-binding protein (bEBP) NtrC and its cognate sensor histidine kinase, NtrB, are key regulators of nitrogen assimilation in many bacteria, but their roles in metabolism and development are not well defined. Notably, NtrC is an unconventional bEBP that lacks the σ-interacting loop commonly known as the GAFTGA motif. Here we show that deletion of slows cell growth in complex medium and that and are essential when ammonium is the sole nitrogen source due to their requirement for glutamine synthetase expression. Random transposition of a conserved IS3-family mobile genetic element frequently rescued the growth defect of mutant strains by restoring transcription of the operon, revealing a possible role for IS3 transposition in shaping the evolution of populations during nutrient limitation. We further identified dozens of direct NtrC-binding sites on the chromosome, with a large fraction located near genes involved in polysaccharide biosynthesis. The majority of binding sites align with those of the essential nucleoid-associated protein, GapR, or the cell cycle regulator, MucR1. NtrC is therefore predicted to directly impact the regulation of cell cycle and cell development. Indeed, loss of NtrC function led to elongated polar stalks and elevated synthesis of cell envelope polysaccharides. This study establishes regulatory connections between NtrC, nitrogen metabolism, polar morphogenesis, and envelope polysaccharide synthesis in . IMPORTANCE Bacteria balance cellular processes with the availability of nutrients in their environment. The NtrB-NtrC two-component signaling system is responsible for controlling nitrogen assimilation in many bacteria. We have characterized the effect of and deletion on growth and development and uncovered a role for spontaneous IS element transposition in the rescue of transcriptional and nutritional deficiencies caused by mutation. We further defined the regulon of NtrC, a bacterial enhancer-binding protein, and demonstrate that it shares specific binding sites with essential proteins involved in cell cycle regulation and chromosome organization. Our work provides a comprehensive view of transcriptional regulation mediated by a distinctive NtrC protein, establishing its connection to nitrogen assimilation and developmental processes in .

Topics: Base Sequence; Caulobacter; Nitrogen; Bacterial Proteins; DNA-Binding Proteins; Polysaccharides; Gene Expression Regulation, Bacterial; PII Nitrogen Regulatory Proteins

PubMed: 37791753
DOI: 10.1128/jb.00181-23

Review

Authors: Selamawit Abi Woldemeskel, Erin D Goley

Bacterial cell shape is a genetically encoded and inherited feature that is optimized for efficient growth, survival, and propagation of bacteria. In addition, bacterial cell morphology is adaptable to changes in environmental conditions. Work in recent years has demonstrated that individual features of cell shape, such as length or curvature, arise through the spatial regulation of cell wall synthesis by cytoskeletal proteins. However, the mechanisms by which these different morphogenetic factors are coordinated and how they may be globally regulated in response to cell cycle and environmental cues are only beginning to emerge. Here, we have summarized recent advances that have been made to understand morphology in the dimorphic Gram-negative bacterium Caulobacter crescentus.

Topics: Bacterial Proteins; Caulobacter crescentus; Cell Cycle; Cell Division; Cell Wall; Cytoskeletal Proteins; Cytoskeleton; Microbial Viability; Peptidoglycan; Stress, Physiological

PubMed: 28359631
DOI: 10.1016/j.tim.2017.03.006

Authors: Christopher R Mahone, Isaac P Payne, Zhixin Lyu...

To divide, bacteria must synthesize their peptidoglycan (PG) cell wall, a protective meshwork that maintains cell shape. FtsZ, a tubulin homolog, dynamically assembles into a midcell band, recruiting division proteins, including the PG synthases FtsW and FtsI. FtsWI are activated to synthesize PG and drive constriction at the appropriate time and place. However, their activation pathway remains unresolved. In Caulobacter crescentus, FtsWI activity requires FzlA, an essential FtsZ-binding protein. Through time-lapse imaging and single-molecule tracking of Caulobacter FtsW and FzlA, we demonstrate that FzlA is a limiting constriction activation factor that signals to promote conversion of inactive FtsW to an active, slow-moving state. We find that FzlA interacts with the DNA translocase FtsK and place FtsK genetically in a pathway with FzlA and FtsWI. Misregulation of the FzlA-FtsK-FtsWI pathway leads to heightened DNA damage and cell death. We propose that FzlA integrates the FtsZ ring, chromosome segregation, and PG synthesis to ensure robust and timely constriction during Caulobacter division.

Topics: Caulobacter; Cell Death; Cell Division; Cell Wall; Chromosome Segregation; Bacterial Proteins; Peptidoglycan

PubMed: 38015166
DOI: 10.1083/jcb.202211026