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

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Over the last decade, bacterial genomics have revealed the presence of eukaryotic-type serine/threonine protein kinases (STKPs) in many bacteria. However, their role and mode of action is still elusive. Recent studies have suggested that STKPs could play an important role in regulating cell division of some bacterial species but the underlying regulatory mechanisms are largely unknown. Considering that much remains to be discovered about the mechanisms by which the cell division machinery is assembled at the cell center and how the diversity of bacterial cell shapes is achieved and maintained, studying the role of STKPs represents a promising approach to decipher the inner workings of bacterial cell division. In this article, we show that the ser/thr-kinase StkP and the two cell division paralogs GpsB and DivIVA of Streptococcus pneumoniae (the pneumococcus) work together to finely tune peptidoglycan synthesis and achieve proper cell shape and division. We discuss the likelihood that similar mechanisms occur in other bacteria requiring protein-kinases for the cell division process. We propose that the interplay between protein-kinases and cell-division proteins like GpsB or DivIVA is of crucial importance to satisfy the modes of cell division and the cell shape displayed by streptococci and other bacteria.

Vyšlo v časopise: Interplay of the Serine/Threonine-Kinase StkP and the Paralogs DivIVA and GpsB in Pneumococcal Cell Elongation and Division. PLoS Genet 10(4): e32767. doi:10.1371/journal.pgen.1004275
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004275

Souhrn

Zdroje

1. YoungKD (2010) Bacterial shape: two-dimensional questions and possibilities. Annual review of microbiology 64: 223–240.

2. EganAJ, VollmerW (2012) The physiology of bacterial cell division. Annals of the New York Academy of Sciences 1277: 8–28.

3. TypasA, BanzhafM, GrossCA, VollmerW (2012) From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nature reviews Microbiology 10: 123–136.

4. CabeenMT, Jacobs-WagnerC (2010) The bacterial cytoskeleton. Annual review of genetics 44: 365–392.

5. FlardhK (2010) Cell polarity and the control of apical growth in Streptomyces. Current opinion in microbiology 13: 758–765.

6. FaddaD, SantonaA, D'UlisseV, GhelardiniP, EnnasMG, et al. (2007) Streptococcus pneumoniae DivIVA: localization and interactions in a MinCD-free context. Journal of bacteriology 189: 1288–1298.

7. LaraB, RicoAI, PetruzzelliS, SantonaA, DumasJ, et al. (2005) Cell division in cocci: localization and properties of the Streptococcus pneumoniae FtsA protein. Molecular microbiology 55: 699–711.

8. Le GouellecA, RouxL, FaddaD, MassiddaO, VernetT, et al. (2008) Roles of pneumococcal DivIB in cell division. Journal of bacteriology 190: 4501–4511.

9. LandAD, WinklerME (2011) The requirement for pneumococcal MreC and MreD is relieved by inactivation of the gene encoding PBP1a. Journal of bacteriology 193: 4166–4179.

10. PinhoMG, KjosM, VeeningJW (2013) How to get (a)round: mechanisms controlling growth and division of coccoid bacteria. Nature reviews Microbiology 11: 601–614.

11. HigginsML, ShockmanGD (1976) Study of cycle of cell wall assembly in Streptococcus faecalis by three-dimensional reconstructions of thin sections of cells. Journal of bacteriology 127: 1346–1358.

12. ShamLT, TsuiHC, LandAD, BarendtSM, WinklerME (2012) Recent advances in pneumococcal peptidoglycan biosynthesis suggest new vaccine and antimicrobial targets. Current opinion in microbiology 15: 194–203.

13. ClaessenD, EmminsR, HamoenLW, DanielRA, ErringtonJ, et al. (2008) Control of the cell elongation-division cycle by shuttling of PBP1 protein in Bacillus subtilis. Molecular microbiology 68: 1029–1046.

14. FleurieA, CluzelC, GuiralS, FretonC, GalissonF, et al. (2012) Mutational dissection of the S/T-kinase StkP reveals crucial roles in cell division of Streptococcus pneumoniae. Molecular microbiology 83: 746–758.

15. BeilharzK, NovakovaL, FaddaD, BrannyP, MassiddaO, et al. (2012) Control of cell division in Streptococcus pneumoniae by the conserved Ser/Thr protein kinase StkP. Proc Natl Acad Sci U S A 109: E905–913.

16. MorlotC, BayleL, JacqM, FleurieA, TourcierG, et al. (2013) Interaction of Penicillin-Binding Protein 2x and Ser/Thr protein kinase StkP, two key players in Streptococcus pneumoniae R6 morphogenesis. Molecular microbiology 90: 88–102.

17. NovakovaL, BezouskovaS, PompachP, SpidlovaP, SaskovaL, et al. (2010) Identification of multiple substrates of the StkP Ser/Thr protein kinase in Streptococcus pneumoniae. Journal of bacteriology 192: 3629–3638.

18. FalkSP, WeisblumB (2012) Phosphorylation of the Streptococcus pneumoniae Cell Wall Biosynthesis Enzyme MurC by a Eukaryotic-like Ser/Thr Kinase. FEMS microbiology letters 340 ((1)) 19–23.

19. TavaresJR, de SouzaRF, MeiraGL, Gueiros-FilhoFJ (2008) Cytological characterization of YpsB, a novel component of the Bacillus subtilis divisome. Journal of bacteriology 190: 7096–7107.

20. MacekB, MijakovicI, OlsenJV, GnadF, KumarC, et al. (2007) The serine/threonine/tyrosine phosphoproteome of the model bacterium Bacillus subtilis. Mol Cell Proteomics 4: 697–707.

21. BurnsideK, LemboA, HarrellMI, GurneyM, XueL, et al. (2011) Serine/threonine phosphatase Stp1 mediates post-transcriptional regulation of hemolysin, autolysis, and virulence of group B Streptococcus. The Journal of biological chemistry 286: 44197–44210.

22. FaddaD, PischeddaC, CaldaraF, WhalenMB, AnderluzziD, et al. (2003) Characterization of divIVA and other genes located in the chromosomal region downstream of the dcw cluster in Streptococcus pneumoniae. Journal of bacteriology 185: 6209–6214.

23. KuruE, HughesHV, BrownPJ, HallE, TekkamS, et al. (2012) In Situ probing of newly synthesized peptidoglycan in live bacteria with fluorescent D-amino acids. Angewandte Chemie 51: 12519–12523.

24. PilhoferM, AistleitnerK, BiboyJ, GrayJ, KuruE, et al. (2013) Discovery of chlamydial peptidoglycan reveals bacteria with murein sacculi but without FtsZ. Nature communications 4: 2856.

25. LandAD, TsuiHC, KocaogluO, VellaSA, ShawSL, et al. (2013) Requirement of essential Pbp2x and GpsB for septal ring closure in Streptococcus pneumoniae D39. Molecular microbiology 90: 939–955.

26. KarimovaG, PidouxJ, UllmannA, LadantD (1998) A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci U S A 95: 5752–5756.

27. KavalKG, HalbedelS (2012) Architecturally the same, but playing a different game: the diverse species-specific roles of DivIVA proteins. Virulence 3: 406–407.

28. HempelAM, WangSB, LetekM, GilJA, FlardhK (2008) Assemblies of DivIVA mark sites for hyphal branching and can establish new zones of cell wall growth in Streptomyces coelicolor. Journal of bacteriology 190: 7579–7583.

29. KangCM, NyayapathyS, LeeJY, SuhJW, HussonRN (2008) Wag31, a homologue of the cell division protein DivIVA, regulates growth, morphology and polar cell wall synthesis in mycobacteria. Microbiology 154: 725–735.

30. LetekM, OrdonezE, VaqueraJ, MargolinW, FlardhK, et al. (2008) DivIVA is required for polar growth in the MreB-lacking rod-shaped actinomycete Corynebacterium glutamicum. Journal of bacteriology 190: 3283–3292.

31. VicenteM, Garcia-OvalleM (2007) Making a point: the role of DivIVA in streptococcal polar anatomy. Journal of bacteriology 189: 1185–1188.

32. Giefing-KrollC, JelencsicsKE, ReipertS, NagyE (2011) Absence of pneumococcal PcsB is associated with overexpression of LysM domain-containing proteins. Microbiology 157: 1897–1909.

33. HalbedelS, HahnB, DanielRA, FliegerA (2012) DivIVA affects secretion of virulence-related autolysins in Listeria monocytogenes. Molecular microbiology 83: 821–839.

34. van OpijnenT, BodiKL, CamilliA (2009) Tn-seq: high-throughput parallel sequencing for fitness and genetic interaction studies in microorganisms. Nature methods 6: 767–772.

35. ThanassiJA, Hartman-NeumannSL, DoughertyTJ, DoughertyBA, PucciMJ (2002) Identification of 113 conserved essential genes using a high-throughput gene disruption system in Streptococcus pneumoniae. Nucleic acids research 30: 3152–3162.

36. SongJH, KoKS, LeeJY, BaekJY, OhWS, et al. (2005) Identification of essential genes in Streptococcus pneumoniae by allelic replacement mutagenesis. Molecules and cells 19: 365–374.

37. HoskinsJ, MatsushimaP, MullenDL, TangJ, ZhaoG, et al. (1999) Gene disruption studies of penicillin-binding proteins 1a, 1b, and 2a in Streptococcus pneumoniae. Journal of bacteriology 181: 6552–6555.

38. PaikJ, KernI, LurzR, HakenbeckR (1999) Mutational analysis of the Streptococcus pneumoniae bimodular class A penicillin-binding proteins. Journal of bacteriology 181: 3852–3856.

39. WheelerR, MesnageS, BonecaIG, HobbsJK, FosterSJ (2011) Super-resolution microscopy reveals cell wall dynamics and peptidoglycan architecture in ovococcal bacteria. Molecular microbiology 82: 1096–1109.

40. BergKH, StamsasGA, StraumeD, HavarsteinLS (2013) Effects of Low PBP2b Levels on Cell Morphology and Peptidoglycan Composition in Streptococcus pneumoniae R6. Journal of bacteriology 195: 4342–4354.

41. KangCM, AbbottDW, ParkST, DascherCC, CantleyLC, et al. (2005) The Mycobacterium tuberculosis serine/threonine kinases PknA and PknB: substrate identification and regulation of cell shape. Genes & development 19: 1692–1704.

42. HempelAM, CantlayS, MolleV, WangSB, NaldrettMJ, et al. (2012) The Ser/Thr protein kinase AfsK regulates polar growth and hyphal branching in the filamentous bacteria Streptomyces. Proc Natl Acad Sci U S A 109: E2371–2379.

43. PearlmanSM, SerberZ, FerrellJEJr (2011) A mechanism for the evolution of phosphorylation sites. Cell 147: 934–946.

44. MartinB, PrudhommeM, AlloingG, GranadelC, ClaverysJP (2000) Cross-regulation of competence pheromone production and export in the early control of transformation in Streptococcus pneumoniae. Molecular microbiology 38: 867–878.

45. CanovaMJ, KremerL, MolleV (2008) pETPhos: a customized expression vector designed for further characterization of Ser/Thr/Tyr protein kinases and their substrates. Plasmid 60: 149–153.

46. MartinB, GranadelC, CampoN, HenardV, PrudhommeM, et al. (2010) Expression and maintenance of ComD-ComE, the two-component signal-transduction system that controls competence of Streptococcus pneumoniae. Molecular microbiology 75: 1513–1528.

47. EberhardtA, WuLJ, ErringtonJ, VollmerW, VeeningJW (2009) Cellular localization of choline-utilization proteins in Streptococcus pneumoniae using novel fluorescent reporter systems. Molecular microbiology 74: 395–408.

48. SungCK, LiH, ClaverysJP, MorrisonDA (2001) An rpsL cassette, janus, for gene replacement through negative selection in Streptococcus pneumoniae. Applied and environmental microbiology 67: 5190–5196.

49. MorlotC, ZapunA, DidebergO, VernetT (2003) Growth and division of Streptococcus pneumoniae: localization of the high molecular weight penicillin-binding proteins during the cell cycle. Molecular microbiology 50: 845–855.

50. de JongIG, BeilharzK, KuipersOP, VeeningJW (2011) Live Cell Imaging of Bacillus subtilis and Streptococcus pneumoniae using Automated Time-lapse Microscopy. Journal of visualized experiments : JoVE ((53)) 3145.

51. MacekB, GnadF, SoufiB, KumarC, OlsenJV, et al. (2008) Phosphoproteome analysis of E. coli reveals evolutionary conservation of bacterial Ser/Thr/Tyr phosphorylation. Mol Cell Proteomics 7: 299–307.

52. OlsenJV, de GodoyLM, LiG, MacekB, MortensenP, et al. (2005) Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Molecular & cellular proteomics : Mol Cell Proteomics 4: 2010–2021.

53. CoxJ, MaticI, HilgerM, NagarajN, SelbachM, et al. (2009) A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nature protocols 4: 698–705.

54. GouetP, RobertX, CourcelleE (2003) ESPript/ENDscript: Extracting and rendering sequence and 3D information from atomic structures of proteins. Nucleic acids research 31: 3320–3323.