Analysis of the CtrA Pathway in Magnetospirillum Reveals an Ancestral Role in Motility in Alphaproteobacteria

Greene, Shannon E.; Brilli, Matteo; Biondi, Emanuele G.; Komeili, Arash

doi:10.1128/jb.00170-12

Cited by 50 publications

(57 citation statements)

References 58 publications

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“…About 50% of cells that tethered . Deletion of cheOp1 reduced swim ring size to the level of a non-motile DctrA mutant, which lacks any flagella filaments similar as described previously 56 . Cis-complementation of the DcheOp1 mutant strain (DcheOp1 þ ) restored WT-like behaviour.…”

Section: Resultsmentioning

confidence: 92%

Polarity of bacterial magnetotaxis is controlled by aerotaxis through a common sensory pathway

2014

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Section: Resultsmentioning

confidence: 92%

Polarity of bacterial magnetotaxis is controlled by aerotaxis through a common sensory pathway

2014

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“…The regulation of motility and flagellum biosynthesis by CtrA is posited to be an ancestral trait (21); thus, our observation of CtrA-binding sites upstream of genes involved in motility and chemotaxis is to be expected. Remarkably, in P. hirschii, the putative mechanism of CtrA regulation of motility is more similar to that of C. crescentus than to that of S. meliloti.…”

Section: Discussionmentioning

confidence: 97%

“…Furthermore, genes shown to be essential for cell cycle progression in C. crescentus have also been shown to have important functions in cell cycle regulation of Agrobacterium tumefaciens (9)(10)(11)(12), Sinorhizobium meliloti (3,(13)(14)(15)(16), and Brucella abortus (14,(17)(18)(19)(20). Notably, the essentiality and regulons of cell cycle regulators are varied in Alphaproteobacteria, suggesting that mechanisms of cell cycle regulation are plastic and may provide a means of adapting to a particular environment (12,15,21).…”

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confidence: 99%

Short-Stalked Prosthecomicrobium hirschii Cells Have a Caulobacter-Like Cell Cycle

et al. 2016

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The dimorphic alphaproteobacterium Prosthecomicrobium hirschii has both short-stalked and long-stalked morphotypes. Notably, these morphologies do not arise from transitions in a cell cycle. Instead, the maternal cell morphology is typically reproduced in daughter cells, which results in microcolonies of a single cell type. In this work, we further characterized the shortstalked cells and found that these cells have a Caulobacter-like life cycle in which cell division leads to the generation of two morphologically distinct daughter cells. Using a microfluidic device and total internal reflection fluorescence (TIRF) microscopy, we observed that motile short-stalked cells attach to a surface by means of a polar adhesin. Cells attached at their poles elongate and ultimately release motile daughter cells. Robust biofilm growth occurs in the microfluidic device, enabling the collection of synchronous motile cells and downstream analysis of cell growth and attachment. Analysis of a draft P. hirschii genome sequence indicates the presence of CtrA-dependent cell cycle regulation. This characterization of P. hirschii will enable future studies on the mechanisms underlying complex morphologies and polymorphic cell cycles. IMPORTANCEBacterial cell shape plays a critical role in regulating important behaviors, such as attachment to surfaces, motility, predation, and cellular differentiation; however, most studies on these behaviors focus on bacteria with relatively simple morphologies, such as rods and spheres. Notably, complex morphologies abound throughout the bacteria, with striking examples, such as P. hirschii, found within the stalked Alphaproteobacteria. P. hirschii is an outstanding candidate for studies of complex morphology generation and polymorphic cell cycles. Here, the cell cycle and genome of P. hirschii are characterized. This work sets the stage for future studies of the impact of complex cell shapes on bacterial behaviors. The Alphaproteobacteria comprise a diverse group of bacteria, including important pathogens of animals (Brucella spp. and Rickettsia spp.) and plants (Agrobacterium spp.), plant symbionts (Rhizobium spp., Sinorhizobium spp., and Mesorhizobium spp.), photosynthetic bacteria (Rhodobacter spp.), freshwater bacteria (Caulobacter spp.), and marine bacteria (Hyphomonas spp.). Despite the diverse habitats and lifestyles of these bacteria, many alphaproteobacterial species have a characteristic life cycle that culminates in asymmetric cell division (1-4). Caulobacter crescentus has served as a model bacterial system for the study of cell cycle regulation, and decades of research have provided insights into the mechanism underlying the precise cell cycle control that allows

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“…For some species of this bacterial group, it has been reported that CtrA does not control the cell cycle, but it controls directly or indirectly the expression of the flagellar genes (14)(15)(16)(17)(18)(19). In this group of bacteria, there is no evidence regarding the control of the activity of CckA, but it has been reported that the expression of cckA, chpT, and/or ctrA is reduced in quorum sensing mutants in Ruegeria sp.…”

mentioning

confidence: 93%

The Flagellar Set Fla2 in Rhodobacter sphaeroides Is Controlled by the CckA Pathway and Is Repressed by Organic Acids and the Expression of Fla1

et al. 2015

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Rhodobacter sphaeroides has two different sets of flagellar genes. Under the growth conditions commonly used in the laboratory, the expression of the fla1 set is constitutive, whereas the fla2 genes are not expressed. Phylogenetic analyses have previously shown that the fla1 genes were acquired by horizontal transfer from a gammaproteobacterium and that the fla2 genes are endogenous genes of this alphaproteobacterium. In this work, we characterized a set of mutants that were selected for swimming using the Fla2 flagella in the absence of the Fla1 flagellum (Fla2 ؉ strains). We determined that these strains have a single missense mutation in the histidine kinase domain of CckA. The expression of these mutant alleles in a Fla1؊ strain allowed fla2-dependent motility without selection. Motility of the Fla2 ؉ strains is also dependent on ChpT and CtrA. The mutant versions of CckA showed an increased autophosphorylation activity in vitro. Interestingly, we found that cckA is transcriptionally repressed by the presence of organic acids, suggesting that the availability of carbon sources could be a part of the signal that turns on this flagellar set. Evidence is presented showing that reactivation of fla1 gene expression in the Fla2؉ background strongly reduces the number of cells with Fla2 flagella. More than 40 genes are involved in the biogenesis and functioning of the bacterial flagellum. This structure has three major subcomponents, the basal body, the hook, and the filament. The basal body contains the export apparatus, an inner membrane ring (MS ring), a periplasmic ring (P ring), and, depending on the species, an outer membrane ring (L ring). The basal body also includes the flagellar motor and a rod that expands from the MS ring and crosses the L and P rings. The hook is the first extracellular structure that is assembled; it connects the basal body with the flagellar filament that is formed by thousands of flagellin subunits (reviewed in references 1-3).In most bacterial species, the expression of the flagellar genes is highly regulated and frequently follows a hierarchical order in which the late genes are expressed until the early genes, that are higher in the hierarchy, are expressed. At the top of the hierarchy, a transcriptional regulator is responsible for the expression of the genes required to assemble the early flagellar structures that are located in the cytoplasm (i.e., export apparatus), in the cytoplasmic membrane (i.e., MS ring), and, depending on the hierarchy, in the periplasm (i.e., P ring), the outer membrane (i.e., L ring), and the extracellular milieu (i.e., hook). Within this class, additional transcription factors are expressed. These proteins are required to transcribe the late genes, such as fliC (flagellin), fliD (filament cap), and fliS

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Analysis of the CtrA Pathway in Magnetospirillum Reveals an Ancestral Role in Motility in Alphaproteobacteria

Cited by 50 publications

References 58 publications

Polarity of bacterial magnetotaxis is controlled by aerotaxis through a common sensory pathway

Polarity of bacterial magnetotaxis is controlled by aerotaxis through a common sensory pathway

Short-Stalked Prosthecomicrobium hirschii Cells Have a Caulobacter-Like Cell Cycle

The Flagellar Set Fla2 in Rhodobacter sphaeroides Is Controlled by the CckA Pathway and Is Repressed by Organic Acids and the Expression of Fla1

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