Making a Point: the Role of DivIVA in Streptococcal Polar Anatomy
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Vicente, Miguel; García-Ovalle, Marta

doi:10.1128/jb.01710-06

Cited by 10 publications

(7 citation statements)

References 36 publications

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“…DivIVA has been previously found to interact or to contribute to the positioning of some PG hydrolases in the pneumococcus [31], [32] or in autolysin secretion in other bacteria as Listeria monocytogenes [33]. The chain phenotype displayed by the Δ divIVA mutant is consistent with impairment of PG hydrolysis and remodeling required for final separation of daughter cells.…”

Section: Discussionmentioning

confidence: 82%

Interplay of the Serine/Threonine-Kinase StkP and the Paralogs DivIVA and GpsB in Pneumococcal Cell Elongation and Division

et al. 2014

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Despite years of intensive research, much remains to be discovered to understand the regulatory networks coordinating bacterial cell growth and division. The mechanisms by which Streptococcus pneumoniae achieves its characteristic ellipsoid-cell shape remain largely unknown. In this study, we analyzed the interplay of the cell division paralogs DivIVA and GpsB with the ser/thr kinase StkP. We observed that the deletion of divIVA hindered cell elongation and resulted in cell shortening and rounding. By contrast, the absence of GpsB resulted in hampered cell division and triggered cell elongation. Remarkably, ΔgpsB elongated cells exhibited a helical FtsZ pattern instead of a Z-ring, accompanied by helical patterns for DivIVA and peptidoglycan synthesis. Strikingly, divIVA deletion suppressed the elongated phenotype of ΔgpsB cells. These data suggest that DivIVA promotes cell elongation and that GpsB counteracts it. Analysis of protein-protein interactions revealed that GpsB and DivIVA do not interact with FtsZ but with the cell division protein EzrA, which itself interacts with FtsZ. In addition, GpsB interacts directly with DivIVA. These results are consistent with DivIVA and GpsB acting as a molecular switch to orchestrate peripheral and septal PG synthesis and connecting them with the Z-ring via EzrA. The cellular co-localization of the transpeptidases PBP2x and PBP2b as well as the lipid-flippases FtsW and RodA in ΔgpsB cells further suggest the existence of a single large PG assembly complex. Finally, we show that GpsB is required for septal localization and kinase activity of StkP, and therefore for StkP-dependent phosphorylation of DivIVA. Altogether, we propose that the StkP/DivIVA/GpsB triad finely tunes the two modes of peptidoglycan (peripheral and septal) synthesis responsible for the pneumococcal ellipsoid cell shape.

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Section: Discussionmentioning

confidence: 82%

Interplay of the Serine/Threonine-Kinase StkP and the Paralogs DivIVA and GpsB in Pneumococcal Cell Elongation and Division

et al. 2014

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“…Our data show that StkP kinase activity but also its extracellular and cytoplasmic domains have a crucial role in pneumococcus cell division. Many proteins are involved in the division process and a function has been attributed to only a few of them (Goehring and Beckwith, 2005; Vicente and Garcia‐Ovalle, 2007; Maggi et al ., 2008). Cell shape, spatial localization of nascent peptidoglycan and septum defects displayed by stkP mutants are reminiscent of some abnormal phenotypes of pneumococcus cells deficient for the expression of proteins involved in cell division (Fadda et al ., 2007; Barendt et al ., 2009; 2011).…”

Section: Resultsmentioning

confidence: 99%

Mutational dissection of the S/T‐kinase StkP reveals crucial roles in cell division of Streptococcus pneumoniae

Fleurie¹,

Cluzel²,

Guiral³

et al. 2012

Molecular Microbiology

101

170

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SummaryEukaryotic-like serine/threonine-kinases are involved in the regulation of a variety of physiological processes in bacteria. In Streptococcus pneumoniae, deletion of the single serine/threonine-kinase gene stkP results in an aberrant cell morphology suggesting that StkP participates in pneumococcus cell division. To understand the function of StkP, we have engineered various pneumococcus strains expressing truncated or kinase-dead forms of StkP. We show that StkP kinase activity, but also its extracellular and cytoplasmic domains per se, are required for pneumococcus cell division. Indeed, we observe that mutant cells show round or elongated shapes with nonfunctional septa and a chain phenotype, delocalized sites of peptidoglycan synthesis and diffused membrane StkP localization. To gain understanding of the underlying StkP-mediated regulatory mechanism, we show that StkP specifically phosphorylates in vivo the cell division protein DivIVA on threonine 201. Pneumococcus cells expressing non-phosphorylatable DivIVA-T201A possess an elongated shape with a polar bulge and aberrant spatial organization of nascent peptidoglycan. This brings the first evidence of the importance of StkP in relationship to the phosphorylation of one of its substrates in cell division. It is concluded that StkP is a multifunctional protein that plays crucial functions in pneumococcus cell shape and division.

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“…This phenotype has not been described in the literature of functional research on Rgg-like regulators in other streptococci. Subsequent microarray-based results provided a possible explanation for this phenotype: the transcript of the divIVA gene, which is required for correct cell division and chromosome segregation in most Gram-positive bacteria (46), was half as abundant in ⌬rgg. In some other streptococcus species, e.g., S. pneumoniae, and in Synechococcus elongatus, disruption of divIVA resulted in cells having a reduced separation frequency and undergoing aberrant polar division, leading to the formation of anucleate minicells and chains of unseparated cells two or three times longer than those of the WT cells (6,28).…”

Section: Discussionmentioning

confidence: 99%

Contribution of the Rgg Transcription Regulator to Metabolism and Virulence of Streptococcus suis Serotype 2

Feng

Cao

et al. 2011

Infect Immun

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The Rgg-like regulators, a family of transcription factors commonly found in many Gram-positive bacteria, play multiple roles, especially in the control of pathogen virulence. Here, we report an rgg homologue from a Chinese isolate, 05ZYH33, of Streptococcus suis serotype 2 (SS2). Deletion of the rgg gene in SS2 increased its adhesion to Hep-2 cells and hemolytic activity in vitro. Significantly, inactivation of the rgg gene attenuated SS2 virulence in an experimental piglet infection model. Using DNA microarrays and quantitative reverse transcription-PCR, we found that the Rgg regulator affects the transcriptional profile of 15.87% (n ‫؍‬ 345) of all of the annotated chromosomal genes, including those involved in nonglucose carbohydrate metabolism, DNA recombination, protein biosynthesis, bacterial defense mechanisms, and others. It was experimentally verified that the deletion of rgg in SS2 reduced the utilization of nonglucose carbohydrates, such as lactose and maltose. In addition, the rgg gene was found to be associated with changes in the bacterial microscopic phenotype and growth curve. These data suggested that Rgg in SS2 is a global transcriptional regulator that plays an important role in promoting SS2 bacterial survival during pathogen-host interaction.Streptococcus suis serotype 2 (SS2) is a leading swine pathogen that occasionally infects humans who engage in close contact with swine and pork-derived products (7,14,35,38). Before our report of two epidemic outbreaks of human SS2 in China, it was thought that SS2 could only cause sporadic human cases (7,38,43,49). In view of this epidemiological history of human SS2 infection, both outbreaks (37, 43, 49) and sporadic cases (9, 27) are now believed to take place in China. Comparative genomics analyses from three different groups (4, 15, 48) have suggested that virulent Chinese strains of SS2 feature a specific, 89-kb-long DNA fragment (dubbed 89K by our group [4]). Further genetic studies showed preliminary evidence that 89K may function as a pathogenicity island (22). Besides well-known virulence-associated factors, such as capsular polysaccharide (36) and suilysin (18), 17 additional virulence-associated components have been identified (9), including a two-component signal transduction system (TCSTS), SalK-SalR (22); an orphan regulator, CovR (31); lipoteichoic acid (11); and others.Like many other pathogenic bacteria, SS2 is transmitted via the respiratory route and remains localized in the palatine tonsils but subsequently escapes from the immune system and disseminates via the blood circulation system, finally invading various host organs (1). In order to colonize and infect different regions within the host, SS2 requires a regulatory network that senses changing surroundings and responds to environmental signals. Such responses typically involve genome-wide changes in transcriptional activation or repression of specific genes through interactions among multiple regulators. In recent years, thorough research and analyses of global regulatory netw...

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Making a Point: the Role of DivIVA in Streptococcal Polar Anatomy ^▿

Cited by 10 publications

References 36 publications

Interplay of the Serine/Threonine-Kinase StkP and the Paralogs DivIVA and GpsB in Pneumococcal Cell Elongation and Division

Interplay of the Serine/Threonine-Kinase StkP and the Paralogs DivIVA and GpsB in Pneumococcal Cell Elongation and Division

Mutational dissection of the S/T‐kinase StkP reveals crucial roles in cell division of Streptococcus pneumoniae

Contribution of the Rgg Transcription Regulator to Metabolism and Virulence of Streptococcus suis Serotype 2

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Making a Point: the Role of DivIVA in Streptococcal Polar Anatomy ▿

Cited by 10 publications

References 36 publications

Interplay of the Serine/Threonine-Kinase StkP and the Paralogs DivIVA and GpsB in Pneumococcal Cell Elongation and Division

Interplay of the Serine/Threonine-Kinase StkP and the Paralogs DivIVA and GpsB in Pneumococcal Cell Elongation and Division

Mutational dissection of the S/T‐kinase StkP reveals crucial roles in cell division of Streptococcus pneumoniae

Contribution of the Rgg Transcription Regulator to Metabolism and Virulence of Streptococcus suis Serotype 2

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Making a Point: the Role of DivIVA in Streptococcal Polar Anatomy ^▿