The Brucella pathogens are polarized bacteria

Henst, Charles Van der; Barsy, Marie de; Zorreguieta, Ángeles; Letesson, Jean‐Jacques; Bolle, Xavier De

doi:10.1016/j.micinf.2013.10.008

Cited by 32 publications

(12 citation statements)

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“…4a–f and Supplementary Note 1)21. Each bacterial cell is characterized by a new pole and an old pole22, the new poles are generated by cell division, and the new pole becomes an old pole when the next cell division is completed. In a few larger bacteria, two close mCherry-ParB foci were observed at the old pole, while in the rest of the larger cells, these foci were strictly found at opposite poles.…”

Section: Resultsmentioning

confidence: 99%

G1-arrested newborn cells are the predominant infectious form of the pathogen Brucella abortus

et al. 2014

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Several intracellular pathogens, such as Brucella abortus, display a biphasic infection process starting with a non-proliferative stage of unclear nature. Here, we study the cell cycle of B. abortus at the single-cell level, in culture and during infection of HeLa cells and macrophages. The localization of segregation and replication loci of the two bacterial chromosomes indicates that, immediately after being engulfed by host-cell endocytic vacuoles, most bacterial cells are newborn. These bacterial cells do not initiate DNA replication for the next 4 to 6 h, indicating a G1 arrest. Moreover, growth is completely stopped during that time, reflecting a global cell cycle block. Growth and DNA replication resume later, although bacteria still reside within endosomal-like compartments. We hypothesize that the predominance of G1-arrested bacteria in the infectious population, and the bacterial cell cycle arrest following internalization, may constitute a widespread strategy among intracellular pathogens to colonize new proliferation niches.

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Section: Resultsmentioning

confidence: 99%

G1-arrested newborn cells are the predominant infectious form of the pathogen Brucella abortus

et al. 2014

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“…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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“…This growing characteristic generates two different cells after cell division: a mother cell inheriting the old envelope material and a daughter cell having a newly synthesized envelope (30). Recent reports suggest that the polar distribution of certain proteins and the asymmetry of Brucella growth have a functional role.…”

Section: Discussionmentioning

confidence: 99%

Interaction Network and Localization of Brucella abortus Membrane Proteins Involved in the Synthesis, Transport, and Succinylation of Cyclic β-1,2-Glucans

Guidolin¹,

Seijo²,

Guaimas³

et al. 2015

J. Bacteriol.

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Cyclic ␤-1,2-glucans (C␤G) are periplasmic homopolysaccharides that play an important role in the virulence and interaction of Brucella with the host. Once synthesized in the cytoplasm by the C␤G synthase (Cgs), C␤G are transported to the periplasm by the C␤G transporter (Cgt) and succinylated by the C␤G modifier enzyme (Cgm). Here, we used a bacterial two-hybrid system and coimmunoprecipitation techniques to study the interaction network between these three integral inner membrane proteins. Our results indicate that Cgs, Cgt, and Cgm can form both homotypic and heterotypic interactions. Analyses carried out with Cgs mutants revealed that the N-terminal region of the protein (Cgs region 1 to 418) is required to sustain the interactions with Cgt and Cgm as well as with itself. We demonstrated by single-cell fluorescence analysis that in Brucella, Cgs and Cgt are focally distributed in the membrane, particularly at the cell poles, whereas Cgm is mostly distributed throughout the membrane with a slight accumulation at the poles colocalizing with the other partners. In summary, our results demonstrate that Cgs, Cgt, and Cgm form a membrane-associated biosynthetic complex. We propose that the formation of a membrane complex could serve as a mechanism to ensure the fidelity of C␤G biosynthesis by coordinating their synthesis with the transport and modification. IMPORTANCEIn this study, we analyzed the interaction and localization of the proteins involved in the synthesis, transport, and modification of Brucella abortus cyclic ␤-1,2-glucans (C␤G), which play an important role in the virulence and interaction of Brucella with the host. We demonstrate that these proteins interact, forming a complex located mainly at the cell poles; this is the first experimental evidence of the existence of a multienzymatic complex involved in the metabolism of osmoregulated periplasmic glucans in bacteria and argues for another example of pole differentiation in Brucella. We propose that the formation of this membrane complex could serve as a mechanism to ensure the fidelity of C␤G biosynthesis by coordinating synthesis with the transport and modification.O smoregulated periplasmic glucans (OPGs) are cyclic, branched cyclic, or branched linear oligosaccharides present in the periplasm of certain Gram-negative bacteria. Common features of these oligosaccharides are the presence of glucose as the sole sugar constituent and the regulation of their synthesis by the osmolarity of the growth milieu. Agrobacterium, Rhizobium, Sinorhizobium, and Brucella species synthesize cyclic OPGs consisting of a cyclic chain of 17 to 25 glucose residues linked in ␤-1,2 glycosidic bonds and substituted with sn-1-phosphoglycerol, succinic acid, methylmalonic acid, or a combination of them (1-3).Cyclic ␤-1,2-glucan synthase (Cgs), the enzyme responsible for the synthesis of cyclic ␤-1,2-glucans (C␤G), is present in a restricted number of symbiotic or pathogenic bacteria, most of them belonging to the Alphaproteobacteria group, in which C␤G are a symbi...

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The Brucella pathogens are polarized bacteria

Cited by 32 publications

References 60 publications

G1-arrested newborn cells are the predominant infectious form of the pathogen Brucella abortus

G1-arrested newborn cells are the predominant infectious form of the pathogen Brucella abortus

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

Interaction Network and Localization of Brucella abortus Membrane Proteins Involved in the Synthesis, Transport, and Succinylation of Cyclic β-1,2-Glucans

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