<i>Plesiomonas shigelloides</i>, an Atypical Enterobacterales with a<i>Vibrio</i>-Related Secondary Chromosome

Adam, Yazid; Brézellec, Pierre; Espinosa, Elena; Besombes, Amelie; Naquin, Delphine; Paly, Evelyne; Possoz, Christophe; Dijk, Erwin van; Barre, François‐Xavier; Ferat, Jean-Luc

doi:10.1093/gbe/evac011

Cited by 9 publications

(7 citation statements)

References 34 publications

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“…We previously noticed that a conserved amino acid motif differentiated the Vibrionales and Enterobacterales MatP proteins (22). This raised the possibility that V. cholerae MatP bound to a different DNA motif than E. coli MatP, which would be over- and under-represented in ter1 and ter2 , respectively (9).…”

Section: Resultsmentioning

confidence: 99%

MatP local enrichment delays segregation independently of tetramer formation and septal anchoring inVibrio cholerae

Espinosa,

Challita,

Desfontaines

et al. 2024

Preprint

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The cellular arrangement and segregation choreography of the genetic material is involved in the timing of assembly and cellular positioning of the cell division apparatus in bacteria. Key to this mode of regulation is the positioning of sister copies of the replication terminus zone (ter) of the chromosomes at the end of the replication cycle. The Vibrio cholerae genome is distributed on two chromosomes, ChrI and ChrII. ChrI is derived from the ancestor of the Vibrionales and Enterobacterales. ChrII is derived from a megaplasmid. ChrI encodes for a homologue of MatP, a protein that tethers sister copies of the ter of the Escherichia coli chromosome together at mid-cell at the time of cell division. MatP structures the ter by binding to a ter-specific DNA motif, matS. It forms tetramers that can bridge DNA segments together and it connects sister ter copies to the divisome via an interaction with a cell division protein, ZapB. We find that MatP structures the ter of ChrI and ChrII, ter1 and ter2, and ensures the cohesion and mid-cell position of sister ter1 and ter2 copies at the time of cell division, demonstrating that ChrII is organised and behaves as a bona fide chromosome. We show that cohesion and positioning are independent of cell division and tetramer formation, but are linked to the local density of matS sites, with sister ter2 separating earlier than sister ter1 because of a lower number of matS sites. Overall, our results suggest that the primary mechanism of action of MatP is to slow down the decatenation of newly replicated molecules.

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Section: Resultsmentioning

confidence: 99%

MatP local enrichment delays segregation independently of tetramer formation and septal anchoring inVibrio cholerae

Espinosa,

Challita,

Desfontaines

et al. 2024

Preprint

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“…Notably, in addition to multipartite genomes in Vibrionaceae and Pseudoalteromonas, there are reports of single strains with chromids in Alteromonas mediterranea [45] and in Plesiomonas shigella [46].…”

Section: Enterobacterales Reference Treementioning

confidence: 99%

Bipartite Genomes in Enterobacterales: Independent Origins of Chromids, Elevated Openness and Donors of Horizontally Transferred Genes

Sonnenberg¹,

Haugen²

2023

Preprint

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Multipartite bacteria have one chromosome and one or more chromid. Chromids are believed to have properties that enhance genomic flexibility, making them a favored integration site for new genes. However, the mechanism by which chromosomes and chromids jointly contribute to this flexibility is not clear. To shed light on this, we analyzed the openness of chromosomes and chromids of the two bacteria, Vibrio and Pseudoalteromonas, both in the Enterobacterales order of gamma-proteobacteria, and compared it with monopartite genomes in the same order. We applied pangenome analysis, codon usage analysis and the HGTector software to detect horizontally transferred genes. Our findings suggest that the chromids of Vibrio and Pseudoalteromonas likely originated from two separate plasmid acquisition events. Bipartite genomes were found to be more open compared to monopartite. We found that the shell and cloud pangene categories drive the openness of bipartite genomes in Vibrio and Pseudoalteromonas. Based on this and our two recent studies, we propose a hypothesis that explains how chromids and the chromosome terminus region contribute to the genomic plasticity of bipartite genomes.

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“…V. cholerae belongs to the Vibrionales, whose genome is divided into a primary chromosome, Chr1, and a secondary chromosome, Chr2. The Vibrionales are closely related to the Enterobacterales, such as E. coli, which are known to be mono-chromosomal bacteria [29]. The primary chromosome of the Vibrionales is derived from the chromosome of the ancestor of the Vibrionales and the Enterobacterales.…”

Section: Introductionmentioning

confidence: 99%

“…The Vibrionales are closely related to the Enterobacterales, such as E . coli , which are known to be mono-chromosomal bacteria [ 29 ]. The primary chromosome of the Vibrionales is derived from the chromosome of the ancestor of the Vibrionales and the Enterobacterales.…”

Section: Introductionmentioning

confidence: 99%

Recovery of Vibrio cholerae polarized cellular organization after exit from a non-proliferating spheroplast state

Goudin,

Ferat,

Possoz

et al. 2023

PLoS ONE

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Vibrio cholerae, the causative agent of cholera epidemics, is a rod-shaped bacterium with a highly polarized cellular organization. It can survive harmful growth conditions by entering a non-proliferating spheroplast state, which involves loss of the cell envelope and polarity. How polarized rod organization cells are formed when the spheroplasts exit the non-proliferating state remains largely uncharacterized. To address this question, we investigated how L-arabinose-induced V. cholerae spheroplasts return to growth. We found that de novo morphogenesis started with the elimination of an excess of periplasm, which was immediately followed by cell elongation and the formation of cell branches with a diameter similar to that of normal V. cholerae cells. Periplasm elimination was driven by bifunctional peptidoglycan synthases involved in cell-wall maintenance, the aPBPs. Elongation and branching relied on the MreB-associated monofunctional peptidoglycan synthase PBP2. The cell division monofunctional peptidoglycan synthase FtsI was not involved in any of these processes. However, the FtsK cell division protein specifically targeted the sites of vesicle extrusion. Genetic material was amplified by synchronous waves of DNA replication as periplasmic elimination began. The HubP polarity factor targeted the tip of the branches as they began to form. However, HubP-mediated polarization was not involved in the efficiency of the recovery process. Finally, our results suggest that the positioning of HubP and the activities of the replication terminus organizer of the two V. cholerae chromosomes, MatP, are independent of cell division. Taken together, these results confirm the interest of L-arabinose-induced V. cholerae spheroplasts to study how cell shape is generated and shed light on the de novo establishment of the intracellular organization and cell polarization in V. cholerae.

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Plesiomonas shigelloides, an Atypical Enterobacterales with aVibrio-Related Secondary Chromosome

Cited by 9 publications

References 34 publications

MatP local enrichment delays segregation independently of tetramer formation and septal anchoring inVibrio cholerae

MatP local enrichment delays segregation independently of tetramer formation and septal anchoring inVibrio cholerae

Bipartite Genomes in Enterobacterales: Independent Origins of Chromids, Elevated Openness and Donors of Horizontally Transferred Genes

Recovery of Vibrio cholerae polarized cellular organization after exit from a non-proliferating spheroplast state

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