Autophosphorylation of the Bacterial Tyrosine-Kinase CpsD Connects Capsule Synthesis with the Cell Cycle in
Bacteria utilize a multi-protein membrane complex to synthesize and export the polysaccharide capsule that conceals and covers the cell. In bacterial pathogens, the capsule protects the cell form opsonophagocytosis and complement-mediated killing. The mechanisms allowing the bacterial cell to maintain this protective capsule during cell growth and division remain unknown. The capsule assembly machinery encompasses a particular type of tyrosine-kinases found only in bacteria, which are called BY-kinases. These kinases are involved in the regulation of several cellular functions including polysaccharide capsule production. Studying the role of BY-kinase represents thus an interesting approach to decipher the mechanisms of capsule synthesis and export. Here, we study the role of the BY-kinase CpsD in the human pathogen Streptococcus pneumoniae. We show that CpsD plays a dual function in the pneumococcus. Indeed, CpsD captures the capsule assembly machinery at the site of division, but we also show that CpsD coordinates capsule production with the cell cycle by interacting with the chromosome segregation system. These features provide a simple mechanism to cover the complete surface of the pneumococcal daughter cells. This finding further opens a new view of the function of BY-kinases in the bacterial cell notably in localizing protein complexes in subcellular regions over the cell cycle.
Vyšlo v časopise:
Autophosphorylation of the Bacterial Tyrosine-Kinase CpsD Connects Capsule Synthesis with the Cell Cycle in. PLoS Genet 11(9): e32767. doi:10.1371/journal.pgen.1005518
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1005518
Souhrn
Bacteria utilize a multi-protein membrane complex to synthesize and export the polysaccharide capsule that conceals and covers the cell. In bacterial pathogens, the capsule protects the cell form opsonophagocytosis and complement-mediated killing. The mechanisms allowing the bacterial cell to maintain this protective capsule during cell growth and division remain unknown. The capsule assembly machinery encompasses a particular type of tyrosine-kinases found only in bacteria, which are called BY-kinases. These kinases are involved in the regulation of several cellular functions including polysaccharide capsule production. Studying the role of BY-kinase represents thus an interesting approach to decipher the mechanisms of capsule synthesis and export. Here, we study the role of the BY-kinase CpsD in the human pathogen Streptococcus pneumoniae. We show that CpsD plays a dual function in the pneumococcus. Indeed, CpsD captures the capsule assembly machinery at the site of division, but we also show that CpsD coordinates capsule production with the cell cycle by interacting with the chromosome segregation system. These features provide a simple mechanism to cover the complete surface of the pneumococcal daughter cells. This finding further opens a new view of the function of BY-kinases in the bacterial cell notably in localizing protein complexes in subcellular regions over the cell cycle.
Zdroje
1. Henriques-Normark B, Normark S. Commensal pathogens, with a focus on Streptococcus pneumoniae, and interactions with the human host. Exp Cell Res. 2010;316:1408–14. doi: 10.1016/j.yexcr.2010.03.003 20227406
2. van der Poll T, Opal SM. Pathogenesis, treatment, and prevention of pneumococcal pneumonia. Lancet. 2009;374:1543–56. doi: 10.1016/S0140-6736(09)61114-4 19880020
3. Kadioglu A, Weiser JN, Paton JC, Andrew PW. The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat Rev Microbiol. 2008;6:288–301. doi: 10.1038/nrmicro1871 18340341
4. Magee AD, Yother J. Requirement for capsule in colonization by Streptococcus pneumoniae. Infect Immun. 2001;69:3755–61. 11349040
5. Winkelstein JA. The role of complement in the host's defense against Streptococcus pneumoniae. Rev Infect Dis. 1981;3:289–98. 7020046
6. Kjos M, Aprianto R, Fernandes VE, Andrew PW, van Strijp JA, Nijland R, et al. Bright Fluorescent Streptococcus pneumoniae for Live-Cell Imaging of Host-Pathogen Interactions. J Bacteriol. 2015;197:807–18. doi: 10.1128/JB.02221-14 25512311
7. Bentley SD, Aanensen DM, Mavroidi A, Saunders D, Rabbinowitsch E, Collins M, et al. Genetic analysis of the capsular biosynthetic locus from all 90 pneumococcal serotypes. PLoS genetics. 2006;2:e31. 16532061
8. Whitfield C. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem. 2006;75:39–68. 16756484
9. Yother J. Capsules of Streptococcus pneumoniae and other bacteria: paradigms for polysaccharide biosynthesis and regulation. Annu Rev Microbiol. 2011;65:563–81. doi: 10.1146/annurev.micro.62.081307.162944 21721938
10. Kawai Y, Marles-Wright J, Cleverley RM, Emmins R, Ishikawa S, Kuwano M, et al. A widespread family of bacterial cell wall assembly proteins. Embo J. 2011;30:4931–41. doi: 10.1038/emboj.2011.358 21964069
11. Morona JK, Morona R, Miller DC, Paton JC. Streptococcus pneumoniae capsule biosynthesis protein CpsB is a novel manganese-dependent phosphotyrosine-protein phosphatase. J Bacteriol. 2002;184:577–83. 11751838
12. Morona JK, Morona R, Paton JC. Attachment of capsular polysaccharide to the cell wall of Streptococcus pneumoniae type 2 is required for invasive disease. Proc Natl Acad Sci U S A. 2006;103:8505–10. 16707578
13. Henriques MX, Rodrigues T, Carido M, Ferreira L, Filipe SR. Synthesis of capsular polysaccharide at the division septum of Streptococcus pneumoniae is dependent on a bacterial tyrosine kinase. Mol Microbiol. 2011;82:515–34. doi: 10.1111/j.1365-2958.2011.07828.x 21929561
14. Grangeasse C, Nessler S, Mijakovic I. Bacterial tyrosine kinases: evolution, biological function and structural insights. Philos Trans R Soc Lond B Biol Sci. 2012;367:2640–55. doi: 10.1098/rstb.2011.0424 22889913
15. Grangeasse C, Cozzone AJ, Deutscher J, Mijakovic I. Tyrosine phosphorylation: an emerging regulatory device of bacterial physiology. Trends Biochem Sci. 2007;32:86–94. 17208443
16. Soulat D, Jault JM, Duclos B, Geourjon C, Cozzone AJ, Grangeasse C. Staphylococcus aureus operates protein-tyrosine phosphorylation through a specific mechanism. J Biol Chem. 2006;281:14048–56. 16565080
17. Olivares-Illana V, Meyer P, Bechet E, Gueguen-Chaignon V, Soulat D, Lazereg-Riquier S, et al. Structural basis for the regulation mechanism of the tyrosine kinase CapB from Staphylococcus aureus. PLoS Biol. 2008;6:e143. doi: 10.1371/journal.pbio.0060143 18547145
18. Morona JK, Morona R, Miller DC, Paton JC. Mutational Analysis of the Carboxy-Terminal (YGX)(4) Repeat Domain of CpsD, an Autophosphorylating Tyrosine Kinase Required for Capsule Biosynthesis in Streptococcus pneumoniae. J Bacteriol. 2003;185:3009–19. 12730159
19. Grangeasse C, Doublet P, Cozzone AJ. Tyrosine phosphorylation of protein kinase Wzc from Escherichia coli K12 occurs through a two-step process. J Biol Chem. 2002;277:7127–35. 11751920
20. Obadia B, Lacour S, Doublet P, Baubichon-Cortay H, Cozzone AJ, Grangeasse C. Influence of Tyrosine-Kinase Wzc Activity on Colanic Acid Production in Escherichia coli K12 Cells. J Mol Biol. 2007;367:42–53. 17254603
21. Bechet E, Gruszczyk J, Terreux R, Gueguen-Chaignon V, Vigouroux A, Obadia B, et al. Identification of structural and molecular determinants of the tyrosine-kinase Wzc and implications in capsular polysaccharide export. Mol Microbiol. 2010;77:1315–25. doi: 10.1111/j.1365-2958.2010.07291.x 20633230
22. Wugeditsch T, Paiment A, Hocking J, Drummelsmith J, Forrester C, Whitfield C. Phosphorylation of Wzc, a tyrosine autokinase, is essential for assembly of group 1 capsular polysaccharides in Escherichia coli. J Biol Chem. 2001;276:2361–71. 11053445
23. Paiment A, Hocking J, Whitfield C. Impact of phosphorylation of specific residues in the tyrosine autokinase, Wzc, on its activity in assembly of group 1 capsules in Escherichia coli. J Bacteriol. 2002;184:6437–47. 12426330
24. Morona JK, Paton JC, Miller DC, Morona R. Tyrosine phosphorylation of CpsD negatively regulates capsular polysaccharide biosynthesis in streptococcus pneumoniae. Mol Microbiol. 2000;35:1431–42. 10760144
25. Morona JK, Miller DC, Morona R, Paton JC. The effect that mutations in the conserved capsular polysaccharide biosynthesis genes cpsA, cpsB, and cpsD have on virulence of Streptococcus pneumoniae. J Infect Dis. 2004;189:1905–13. 15122528
26. Avery OT, Macleod CM, McCarty M. Studies on the Chemical Nature of the Substance Inducing Transformation of Pneumococcal Types: Induction of Transformation by a Desoxyribonucleic Acid Fraction Isolated from Pneumococcus Type Iii. J Exp Med. 1944;79:137–58. 19871359
27. Leipe DD, Wolf YI, Koonin EV, Aravind L. Classification and evolution of P-loop GTPases and related ATPases. J Mol Biol. 2002;317:41–72. 11916378
28. Gerdes K, Howard M, Szardenings F. Pushing and pulling in prokaryotic DNA segregation. Cell. 2010;141:927–42. doi: 10.1016/j.cell.2010.05.033 20550930
29. Mijakovic I, Poncet S, Boel G, Maze A, Gillet S, Jamet E, et al. Transmembrane modulator-dependent bacterial tyrosine kinase activates UDP-glucose dehydrogenases. Embo J. 2003;22:4709–18. 12970183
30. Toniolo C, Balducci E, Romano MR, Proietti D, Ferlenghi I, Grandi G, et al. Streptococcus agalactiae capsule polymer length and attachment is determined by the proteins CpsABCD. J Biol Chem. 2015.
31. Guiral S, Henard V, Laaberki MH, Granadel C, Prudhomme M, Martin B, et al. Construction and evaluation of a chromosomal expression platform (CEP) for ectopic, maltose-driven gene expression in Streptococcus pneumoniae. Microbiology. 2006;152:343–9. 16436422
32. Fleurie A, Cluzel C, Guiral S, Freton C, Galisson F, Zanella-Cleon I, et al. Mutational dissection of the S/T-kinase StkP reveals crucial roles in cell division of Streptococcus pneumoniae. Mol Microbiol. 2012;83:746–58. doi: 10.1111/j.1365-2958.2011.07962.x 22211696
33. Dinh T, Bernhardt TG. Using superfolder green fluorescent protein for periplasmic protein localization studies. J Bacteriol. 2011;193:4984–7. doi: 10.1128/JB.00315-11 21764912
34. Bi EF, Lutkenhaus J. FtsZ ring structure associated with division in Escherichia coli. Nature. 1991;354:161–4. 1944597
35. Fleurie A, Manuse S, Zhao C, Campo N, Cluzel C, Lavergne JP, et al. Interplay of the serine/threonine-kinase StkP and the paralogs DivIVA and GpsB in pneumococcal cell elongation and division. PLoS genetics. 2014;10:e1004275. doi: 10.1371/journal.pgen.1004275 24722178
36. Kjos M, Veening JW. Tracking of chromosome dynamics in live Streptococcus pneumoniae reveals that transcription promotes chromosome segregation. Mol Microbiol. 2014;91:1088–105. doi: 10.1111/mmi.12517 24417389
37. Land AD, Tsui HC, Kocaoglu O, Vella SA, Shaw SL, Keen SK, et al. Requirement of essential Pbp2x and GpsB for septal ring closure in Streptococcus pneumoniae D39. Mol Microbiol. 2013;90:939–55. doi: 10.1111/mmi.12408 24118410
38. Slager J, Kjos M, Attaiech L, Veening JW. Antibiotic-induced replication stress triggers bacterial competence by increasing gene dosage near the origin. Cell. 2014;157:395–406. doi: 10.1016/j.cell.2014.01.068 24725406
39. Livny J, Yamaichi Y, Waldor MK. Distribution of centromere-like parS sites in bacteria: insights from comparative genomics. J Bacteriol. 2007;189:8693–703. 17905987
40. Minnen A, Attaiech L, Thon M, Gruber S, Veening JW. SMC is recruited to oriC by ParB and promotes chromosome segregation in Streptococcus pneumoniae. Mol Microbiol. 2011;81:676–88. doi: 10.1111/j.1365-2958.2011.07722.x 21651626
41. Vincent C, Duclos B, Grangeasse C, Vaganay E, Riberty M, Cozzone AJ, et al. Relationship between exopolysaccharide production and protein-tyrosine phosphorylation in gram-negative bacteria. J Mol Biol. 2000;304:311–21. 11090276
42. Elsholz AK, Wacker SA, Losick R. Self-regulation of exopolysaccharide production in Bacillus subtilis by a tyrosine kinase. Genes Dev. 2014;28:1710–20. doi: 10.1101/gad.246397.114 25085422
43. Nakar D, Gutnick DL. Involvement of a protein tyrosine kinase in production of the polymeric bioemulsifier emulsan from the oil-degrading strain Acinetobacter lwoffii RAG-1. J Bacteriol. 2003;185:1001–9. 12533476
44. Niemeyer D, Becker A. The molecular weight distribution of succinoglycan produced by Sinorhizobium meliloti is influenced by specific tyrosine phosphorylation and ATPase activity of the cytoplasmic domain of the ExoP protein. J Bacteriol. 2001;183:5163–70. 11489870
45. Xayarath B, Yother J. Mutations blocking side chain assembly, polymerization, or transport of a Wzy-dependent Streptococcus pneumoniae capsule are lethal in the absence of suppressor mutations and can affect polymer transfer to the cell wall. J Bacteriol. 2007;189:3369–81. 17322316
46. Wheeler R, Mesnage S, Boneca IG, Hobbs JK, Foster SJ. Super-resolution microscopy reveals cell wall dynamics and peptidoglycan architecture in ovococcal bacteria. Mol Microbiol. 2011;82:1096–109. doi: 10.1111/j.1365-2958.2011.07871.x 22059678
47. Fleurie A, Lesterlin C, Manuse S, Zhao C, Cluzel C, Lavergne JP, et al. MapZ marks the division sites and positions FtsZ rings in Streptococcus pneumoniae. Nature. 2014;516:259–62. doi: 10.1038/nature13966 25470041
48. Morona R. Encapsulating bacteria. Structure. 2013;21:692–3. doi: 10.1016/j.str.2013.04.011 23664360
49. Eberhardt A, Hoyland CN, Vollmer D, Bisle S, Cleverley RM, Johnsborg O, et al. Attachment of capsular polysaccharide to the cell wall in Streptococcus pneumoniae. Microb Drug Resist. 2012;18:240–55. doi: 10.1089/mdr.2011.0232 22432711
50. Kuru E, Hughes HV, Brown PJ, Hall E, Tekkam S, Cava F, et al. In Situ probing of newly synthesized peptidoglycan in live bacteria with fluorescent D-amino acids. Angew Chem Int Ed Engl. 2012;51:12519–23. doi: 10.1002/anie.201206749 23055266
51. Pinho MG, Kjos M, Veening JW. How to get (a)round: mechanisms controlling growth and division of coccoid bacteria. Nat Rev Microbiol. 2013;11:601–14. doi: 10.1038/nrmicro3088 23949602
52. Holeckova N, Doubravova L, Massidda O, Molle V, Buriankova K, Benada O, et al. LocZ is a new cell division protein involved in proper septum placement in Streptococcus pneumoniae. mBio. 2015;6:e01700–14.
53. Lutkenhaus J. The ParA/MinD family puts things in their place. Trends Microbiol. 2012;20:411–8. doi: 10.1016/j.tim.2012.05.002 22672910
54. Ringgaard S, Schirner K, Davis BM, Waldor MK. A family of ParA-like ATPases promotes cell pole maturation by facilitating polar localization of chemotaxis proteins. Genes Dev. 2011;25:1544–55. doi: 10.1101/gad.2061811 21764856
55. Roberts MA, Wadhams GH, Hadfield KA, Tickner S, Armitage JP. ParA-like protein uses nonspecific chromosomal DNA binding to partition protein complexes. Proceedings of the National Academy of Sciences of the United States of America. 2012;109:6698–703. doi: 10.1073/pnas.1114000109 22496588
56. Correa NE, Peng F, Klose KE. Roles of the regulatory proteins FlhF and FlhG in the Vibrio cholerae flagellar transcription hierarchy. J Bacteriol. 2005;187:6324–32. 16159765
57. Weiser JN, Austrian R, Sreenivasan PK, Masure HR. Phase variation in pneumococcal opacity: relationship between colonial morphology and nasopharyngeal colonization. Infect Immun. 1994;62:2582–9. 8188381
58. Hyams C, Camberlein E, Cohen JM, Bax K, Brown JS. The Streptococcus pneumoniae capsule inhibits complement activity and neutrophil phagocytosis by multiple mechanisms. Infect Immun. 2010;78:704–15. doi: 10.1128/IAI.00881-09 19948837
59. Martin B, Garcia P, Castanie MP, Claverys JP. The recA gene of Streptococcus pneumoniae is part of a competence-induced operon and controls lysogenic induction. Mol Microbiol. 1995;15:367–79. 7538190
60. Martin B, Prudhomme M, Alloing G, Granadel C, Claverys JP. Cross-regulation of competence pheromone production and export in the early control of transformation in Streptococcus pneumoniae. Mol Microbiol. 2000;38:867–78. 11115120
61. Sung CK, Li H, Claverys JP, Morrison DA. An rpsL cassette, janus, for gene replacement through negative selection in Streptococcus pneumoniae. Appl Environ Microbiol. 2001;67:5190–6. 11679344
62. Martin B, Granadel C, Campo N, Henard V, Prudhomme M, Claverys JP. Expression and maintenance of ComD-ComE, the two-component signal-transduction system that controls competence of Streptococcus pneumoniae. Mol Microbiol. 2010;75:1513–28. doi: 10.1111/j.1365-2958.2010.07071.x 20180906
63. Beilharz K, Novakova L, Fadda D, Branny P, Massidda O, Veening JW. Control of cell division in Streptococcus pneumoniae by the conserved Ser/Thr protein kinase StkP. Proceedings of the National Academy of Sciences of the United States of America. 2012;109:E905–13. doi: 10.1073/pnas.1119172109 22431591
64. Cortay JC, Negre D, Scarabel M, Ramseier TM, Vartak NB, Reizer J, et al. In vitro asymmetric binding of the pleiotropic regulatory protein, FruR, to the ace operator controlling glyoxylate shunt enzyme synthesis. J Biol Chem. 1994;269:14885–91. 8195118
65. James P, Halladay J, Craig EA. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics. 1996;144:1425–36. 8978031
66. Noirot-Gros MF, Dervyn E, Wu LJ, Mervelet P, Errington J, Ehrlich SD, et al. An expanded view of bacterial DNA replication. Proceedings of the National Academy of Sciences of the United States of America. 2002;99:8342–7. 12060778
67. Yother J, White JM. Novel surface attachment mechanism of the Streptococcus pneumoniae protein PspA. J Bacteriol. 1994;176:2976–85. 7910604
68. Bender MH, Cartee RT, Yother J. Positive correlation between tyrosine phosphorylation of CpsD and capsular polysaccharide production in Streptococcus pneumoniae. J Bacteriol. 2003;185:6057–66. 14526017
69. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22:4673–80. 7984417
70. Robert X, Gouet P. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res. 2014;42:W320–4. doi: 10.1093/nar/gku316 24753421
71. Cole C, Barber JD, Barton GJ. The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 2008;36(Web Server issue):W197–201. doi: 10.1093/nar/gkn238 18463136
72. Zhang Y. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics. 2008;9:40. doi: 10.1186/1471-2105-9-40 18215316
73. Jerabek-Willemsen M, Wienken CJ, Braun D, Baaske P, Duhr S. Molecular interaction studies using microscale thermophoresis. Assay Drug Dev Technol. 2011;9:342–53. doi: 10.1089/adt.2011.0380 21812660
74. Sliusarenko O, Heinritz J, Emonet T, Jacobs-Wagner C. High-throughput, subpixel precision analysis of bacterial morphogenesis and intracellular spatio-temporal dynamics. Mol Microbiol. 2011;80:612–27. doi: 10.1111/j.1365-2958.2011.07579.x 21414037
75. de Jong IG, Beilharz K, Kuipers OP, Veening JW. Live Cell Imaging of Bacillus subtilis and Streptococcus pneumoniae using Automated Time-lapse Microscopy. J Vis Exp. 2011;(53).
76. Leonard TA, Butler PJ, Lowe J. Bacterial chromosome segregation: structure and DNA binding of the Soj dimer—a conserved biological switch. Embo J. 2005;24:270–82. 15635448
77. Hester CM, Lutkenhaus J. Soj (ParA) DNA binding is mediated by conserved arginines and is essential for plasmid segregation. Proc Natl Acad Sci U S A. 2007;104:20326–31. 18077387
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2015 Číslo 9
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Arabidopsis AtPLC2 Is a Primary Phosphoinositide-Specific Phospholipase C in Phosphoinositide Metabolism and the Endoplasmic Reticulum Stress Response
- Bridges Meristem and Organ Primordia Boundaries through , , and during Flower Development in
- KLK5 Inactivation Reverses Cutaneous Hallmarks of Netherton Syndrome
- The Chromatin Protein DUET/MMD1 Controls Expression of the Meiotic Gene during Male Meiosis in