Advertisement

Cell growth and cell division in the rod-shaped actinomycete Corynebacterium glutamicum

Abstract

Bacterial cell growth and cell division are highly complicated and diversified biological processes. In most rod-shaped bacteria, actin-like MreB homologues produce helicoidal structures along the cell that support elongation of the lateral cell wall. An exception to this rule is peptidoglycan synthesis in the rod-shaped actinomycete Corynebacterium glutamicum, which is MreB-independent. Instead, during cell elongation this bacterium synthesizes new cell-wall material at the cell poles whereas the lateral wall remains inert. Thus, the strategy employed by C. glutamicum to acquire a rod-shaped morphology is completely different from that of Escherichia coli or Bacillus subtilis. Cell division in C. glutamicum also differs profoundly by the apparent absence in its genome of homologues of spatial or temporal regulators of cell division, and its cell division apparatus seems to be simpler than those of other bacteria. Here we review recent advances in our knowledge of the C. glutamicum cell cycle in order to further understand this very different model of rod-shape acquisition.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 199

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Bendt AK, Burkovski A, Schaffer S, Bott M, Farwick M, HermannT (2003) Towards a phosphoproteome map of Corynebacterium glutamicum. Proteomics 3:1637–1646

  2. Bernard CS, Sadasivam M, Shiomi D, Margolin W (2007) An altered FtsA can compensate for the loss of essential cell division protein FtsN in Escherichia coli. Mol Microbiol 64:1289–1305

  3. Bernhardt TG, de Boer PA (2005) SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over chromosomes in E. coli. Mol Cell 18:555–564

  4. Cadenas RF, Fernandez-Gonzalez C, Martin JF, Gil JA (1996) Construction of new cloning vectors for Brevibacterium lactofermentum. FEMS Microbiol Lett 137:63–68

  5. Cadenas RF, Martin JF, Gil JA (1991) Construction and characterization of promoter-probe vectors for Corynebacteria using the kanamycin-resistance reporter gene. Gene 98:117–121

  6. Cerdeno-Tarraga AM, Efstratiou A, Dover LG, Holden MT, Pallen M, Bentley SD et al (2003) The complete genome sequence and analysis of Corynebacterium diphtheriae NCTC13129. Nucleic Acids Res 31:6516–6523

  7. Cha JH, Stewart GC (1997) The divIVA minicell locus of Bacillus subtilis. J Bacteriol 179:1671–1683

  8. Chami M, Bayan N, Peyret JL, Gulik-Krzywicki T, Leblon G, Shechter E (1997) The S-layer protein of Corynebacterium glutamicum is anchored to the cell wall by its C-terminal hydrophobic domain. Mol Microbiol 23:483–492

  9. Collins MD, Cummins CS (1986) Genus Corynebacterium Lehmann and Neumann 1896, 350AL. In: Sneath PHA, Mair NS, Sharpe ME, Holt JG (eds) Bergey’s manual of systematic bacteriology. Williams & Wilkins, Baltimore, pp 1266–1276

  10. Collins MD, Goodfellow M, Minnikin DE (1982) Fatty acid composition of some mycolic acid-containing coryneform bacteria. J Gen Microbiol 128:2503–2509

  11. Courvalin P, Davies J (2003) Antimicrobials. Curr Opin Microbiol 6:425–529

  12. Cure GL, Keddie RM (1973) Methods for the morphological examination of aerobic coryneform bacteria. In: Board RG, Lovelock DW (eds) Sampling—microbiological monitoring of environments. Academic Press, London, pp 123–135

  13. Daniel RA, Errington J (2003) Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 113:767–776

  14. Dasgupta A, Datta P, Kundu M, Basu J (2006) The serine/threonine kinase PknB of Mycobacterium tuberculosis phosphorylates PBPA, a penicillin-binding protein required for cell division. Microbiology 152:493–504

  15. Datta P, Dasgupta A, Singh AK, Mukherjee P, Kundu M, Basu J (2006) Interaction between FtsW and penicillin-binding protein 3 (PBP3) directs PBP3 to mid-cell, controls cell septation and mediates the formation of a trimeric complex involving FtsZ, FtsW and PBP3 in mycobacteria. Mol Microbiol 62:1655–1673

  16. de Boer PA, Crossley RE, Rothfield LI (1989) A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli. Cell 56:641–649

  17. Dover LG, Cerdeno-Tarraga AM, Pallen MJ, Parkhill J, Besra GS (2004) Comparative cell wall core biosynthesis in the mycolated pathogens, Mycobacterium tuberculosis and Corynebacterium diphtheriae. FEMS Microbiol Rev 28:225–250

  18. Errington J, Daniel RA, Scheffers DJ (2003) Cytokinesis in bacteria. Microbiol Mol Biol Rev 67:52–65, table

  19. Fadda D, Santona A, D’Ulisse V, Ghelardini P, Ennas MG, Whalen MB, Massidda O (2007) Streptococcus pneumoniae DivIVA: localization and interactions in a MinCD free context. J Bacteriol 189:1288–1298

  20. Fernandez-Natal I, Guerra J, Alcoba M, Cachon F, Soriano F (2001) Bacteremia caused by multiply resistant Corynebacterium urealyticum: six case reports and review. Eur J Clin Microbiol Infect Dis 20:514–517

  21. Figge RM, Divakaruni AV, Gober JW (2004) MreB, the cell shape-determining bacterial actin homologue, co-ordinates cell wall morphogenesis in Caulobacter crescentus. Mol Microbiol 51:1321–1332

  22. Flardh K (2003a) Essential role of DivIVA in polar growth and morphogenesis in Streptomyces coelicolor A3(2). Mol Microbiol 49:1523–1536

  23. Flardh K (2003b) Growth polarity and cell division in Streptomyces. Curr Opin Microbiol 6:564–571

  24. Geissler B, Margolin W (2005) Evidence for functional overlap among multiple bacterial cell division proteins: compensating for the loss of FtsK. Mol Microbiol 58:596–612

  25. Goehring NW, Beckwith J (2005) Diverse paths to midcell: assembly of the bacterial cell division machinery. Curr Biol 15:514–526

  26. Goffin C, Ghuysen JM (1998) Multimodular penicillin-binding proteins: an enigmatic family of orthologs and paralogs. Microbiol Mol Biol Rev 62:1079–1093

  27. Hamoen LW, Meile JC, de Jong JW, Noirot P, Errington J (2006) SepF, a novel FtsZ-interacting protein required for a late step in cell division. Mol Microbiol 59:989–999

  28. Hansmeier N, Albersmeier A, Tauch A, Damberg T, Ros R, Anselmetti D et al (2006) The surface (S)-layer gene cspB of Corynebacterium glutamicum is transcriptionally activated by a LuxR-type regulator and located on a 6 kb genomic island absent from the type strain ATCC 13032. Microbiology 152:923–935

  29. Henriques AO, Glaser P, Piggot PJ, Moran CP Jr (1998) Control of cell shape and elongation by the rodA gene in Bacillus subtilis. Mol Microbiol 28:235–247

  30. Hermann T (2003) Industrial production of amino acids by coryneform bacteria. J Biotechnol 104:155–172

  31. Hermann T, Pfefferle W, Baumann C, Busker E, Schaffer S, Bott M et al (2001) Proteome analysis of Corynebacterium glutamicum. Electrophoresis 22:1712–1723

  32. Hirasawa T, Wachi M, Nagai K (2000) A mutation in the Corynebacterium glutamicum ltsA gene causes susceptibility to lysozyme, temperature-sensitive growth, and L-glutamate production. J Bacteriol 182:2696–2701

  33. Honrubia MP, Fernandez FJ, Gil JA (1998) Identification, characterization, and chromosomal organization of the ftsZ gene from Brevibacterium lactofermentum. Mol Gen Genet 259:97–104

  34. Honrubia MP, Ramos A, Gil JA (2001) The cell division genes ftsQ and ftsZ, but not the three downstream open reading frames YFIH, ORF5 and ORF6, are essential for growth and viability in Brevibacterium lactofermentum ATCC 13869. Mol Genet Genomics 265:1022–1030

  35. Ikeda M, Nakagawa S (2003) The Corynebacterium glutamicum genome: features and impacts on biotechnological processes. Appl Microbiol Biotechnol 62:99–109

  36. Jones LJ, Carballido-Lopez R, Errington J (2001) Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104:913–922

  37. Kalinowski J, Bathe B, Bartels D, Bischoff N, Bott M, Burkovski A et al (2003) The complete Corynebacterium glutamicum ATCC 13032 genome sequence and its impact on the production of L-aspartate-derived amino acids and vitamins. J Biotechnol 104:5–25

  38. Kang CM, Abbott DW, Park ST, Dascher CC, Cantley LC, Husson RN (2005) The Mycobacterium tuberculosis serine/threonine kinases PknA and PknB: substrate identification and regulation of cell shape. Genes Dev 19:1692–1704

  39. Kinoshita S, Udaka S, Shimono S (1957) Studies on the amino acid fermentation. Part I. Production of L-glutamic acid by various microorganisms. J Gen Appl Microbiol 3:193–205

  40. Kobayashi M, Asai Y, Hatakeyama K, Kijima N, Wachi M, Nagai K, Yukawa H (1997) Cloning, sequencing, and characterization of the ftsZ gene from coryneform bacteria. Biochem Biophys Res Commun 236:383–388

  41. Kruse T, Bork-Jensen J, Gerdes K (2005) The morphogenetic MreBCD proteins of Escherichia coli form an essential membrane-bound complex. Mol Microbiol 55:78–89

  42. Letek M, Ordonez E, Fernadez-Natal I, Gil JA, Mateos LM (2006a) Identification of the emerging skin pathogen Corynebacterium amycolatum, using the essential divIVA gene as a target by PCR-amplification. FEMS Microbiol Lett 265:256–263

  43. Letek M, Ordonez E, Fiuza M, Honrubia-Marcos MP, Vaquera J, Gil JA, Mateos LM (2007) Characterization of the promoter region of ftsZ from Corynebacterium glutamicum and controlled overexpression of FtsZ. Int Microbiol 10:271–282

  44. Letek M, Ordonez E, Vaquera J, Margolin W, Flardh K, Mateos LM, Gil JA (2008) DivIVA is required for polar growth in the MreB-lacking rod-shaped actinomycete Corynebacterium glutamicum. J Bacteriol (submitted)

  45. Letek M, Valbuena N, Ramos A, Ordonez E, Gil JA, Mateos LM (2006b) Characterization and use of catabolite-repressed promoters from gluconate genes in Corynebacterium glutamicum. J Bacteriol 188:409–423

  46. Martin JF, Santamaria RI, Sandoval H, del Real G, Mateos LM, Gil JA, Aguilar A (1987) Cloning systems in amino acid-producing corynebacteria. Bio/Technology 5:137–146

  47. Massidda O, Anderluzzi D, Friedli L, Feger G (1998) Unconventional organization of the division and cell wall gene cluster of Streptococcus pneumoniae. Microbiology 144:3069–3078

  48. Mateos LM, del Real G, Aguilar A, Martin JF (1987a) Cloning and expression in Escherichia coli of the homoserine kinase (thrB) gene from Brevibacterium lactofermentum. Mol Gen Genet 206:361–367

  49. Mateos LM, del Real G, Aguilar A, Martin JF (1987b) Nucleotide sequence of the homoserine dehydrogenase (thrA) gene of Brevibacterium lactofermentum. Nucleic Acids Res 15:10598

  50. Matsuzawa H, Asoh S, Kunai K, Muraiso K, Takasuga A, Ohta T (1989) Nucleotide sequence of the rodA gene, responsible for the rod shape of Escherichia coli: rodA and the pbpA gene, encoding penicillin-binding protein 2, constitute the rodA operon. J Bacteriol 171:558–560

  51. Mazza P, Noens EE, Schirner K, Grantcharova N, Mommaas AM, Koerten HK, Muth G, Flärdh K, van Wezel GP, Wohlleben W (2006) MreB of Streptomyces coelicolor is not essential for vegetative growth but is required for the integrity of aerial hyphae and spores. Mol Microbiol 60:838–852

  52. Minnikin DE (1982) Lipids: complex lipids, their chemistry, biosynthesis and roles. In: Ratledge C, Stanforf J (eds) The Biology of the Mycobacteria. Academic Press, London, pp 95–184

  53. Mir MA, Rajeswari HS, Veeraraghavan U, Ajitkumar P (2006) Molecular characterisation of ABC transporter type FtsE and FtsX proteins of Mycobacterium tuberculosis. Arch Microbiol 185:147–158

  54. Nguyen L, Scherr N, Gatfield J, Walburger A, Pieters J, Thompson CJ (2007) Antigen 84, an effector of pleiomorphism in Mycobacterium smegmatis. J Bacteriol 189:7896–7910

  55. Nishio Y, Nakamura Y, Kawarabayasi Y, Usuda Y, Kimura E, Sugimoto S et al (2003) Comparative complete genome sequence analysis of the amino acid replacements responsible for the thermostability of Corynebacterium efficiens. Genome Res 13:1572–1579

  56. Ohnishi J, Hayashi M, Mitsuhashi S, Ikeda M (2003) Efficient 40 degrees C fermentation of L-lysine by a new Corynebacterium glutamicum mutant developed by genome breeding. Appl Microbiol Biotechnol 62:69–75

  57. Ohnishi J, Mitsuhashi S, Hayashi M, Ando S, Yokoi H, Ochiai K, Ikeda M (2002) A novel methodology employing Corynebacterium glutamicum genome information to generate a new L-lysine-producing mutant. Appl Microbiol Biotechnol 58:217–223

  58. Peyret JL, Bayan N, Joliff G, Gulik-Krzywicki T, Mathieu L, Schechter E, Leblon G (1993) Characterization of the cspB gene encoding PS2, an ordered surface-layer protein in Corynebacterium glutamicum. Mol Microbiol 9:97–109

  59. Pinho MG, Errington J (2004) A divIVA null mutant of Staphylococcus aureus undergoes normal cell division. FEMS Microbiol Lett 240:145–149

  60. Polen T, Wendisch VF (2004) Genomewide expression analysis in amino acid-producing bacteria using DNA microarrays. Appl Biochem Biotechnol 118:215–232

  61. Puech V, Chami M, Lemassu A, Laneelle MA, Schiffler B, Gounon P et al (2001) Structure of the cell envelope of corynebacteria: importance of the non-covalently bound lipids in the formation of the cell wall permeability barrier and fracture plane. Microbiology 147:1365–1382

  62. Radmacher E, Alderwick LJ, Besra GS, Brown AK, Gibson KJ, Sahm H, Eggeling L (2005) Two functional FAS-I type fatty acid synthases in Corynebacterium glutamicum. Microbiology 151:2421–2427

  63. Ramirez-Arcos S, Liao M, Marthaler S, Rigden M, Dillon JA (2005) Enterococcus faecalis divIVA: an essential gene involved in cell division, cell growth and chromosome segregation. Microbiology 151:1381–1393

  64. Ramos A, Honrubia MP, Valbuena N, Vaquera J, Mateos LM, Gil JA (2003) Involvement of DivIVA in the morphology of the rod-shaped actinomycete Brevibacterium lactofermentum. Microbiology 149:3531–3542

  65. Ramos A, Honrubia MP, Vega D, Ayala JA, Bouhss A, Mengin-Lecreulx D, Gil JA (2004) Characterization and chromosomal organization of the murD-murC-ftsQ region of Corynebacterium glutamicum ATCC 13869. Res Microbiol 155:174–184

  66. Ramos A, Letek M, Campelo AB, Vaquera J, Mateos LM, Gil JA (2005) Altered morphology produced by ftsZ expression in Corynebacterium glutamicum ATCC 13869. Microbiology 151:2563–2572

  67. Reddy M (2007) Role of FtsEX in cell division of Escherichia coli: viability of ftsEX mutants is dependent on functional SufI or high osmotic strength. J Bacteriol 189:98–108

  68. Sall T, Mudd S, Takagi A (1958) Polyphosphate accumulation and utilization as related to synchronized cell division of Corynebacterium diphtheriae. J Bacteriol 76:640–645

  69. Santamaria RI, Gil JA, Martin JF (1985) High-frequency transformation of Brevibacterium lactofermentum protoplasts by plasmid DNA. J Bacteriol 162:463–467

  70. Santamaria RI, Gil JA, Mesas JM, Martin JF (1984) Characterization of an endogenous plasmid and development of cloning vectors and a transformation system in Brevibacterium lactofermentum. J Gen Microbiol 130:2237–2246

  71. Santamaria RI, Martin JF, Gil JA (1987) Identification of a promoter sequence in the plasmid pUL340 of Brevibacterium lactofermentum and construction of new cloning vectors for corynebacteria containing two selectable markers. Gene 56:199–208

  72. Scheffers DJ, Jones LJ, Errington J (2004) Several distinct localization patterns for penicillin-binding proteins in Bacillus subtilis. Mol Microbiol 51:749–764

  73. Scheffers DJ, Pinho MG (2005) Bacterial cell wall synthesis: new insights from localization studies. Microbiol Mol Biol Rev 69:585–607

  74. Schmidt KL, Peterson ND, Kustusch RJ, Wissel MC, Graham B, Phillips GJ, Weiss DS (2004) A predicted ABC transporter, FtsEX, is needed for cell division in Escherichia coli. J Bacteriol 186:785–793

  75. Stahlberg H, Kutejova E, Muchova K, Gregorini M, Lustig A, Muller SA et al (2004) Oligomeric structure of the Bacillus subtilis cell division protein DivIVA determined by transmission electron microscopy. Mol Microbiol 52:1281–1290

  76. Tamames J, Gonzalez-Moreno M, Mingorance J, Valencia A, Vicente M (2001) Bringing gene order into bacterial shape. Trends Genet 17:124–126

  77. Tauch A, Kaiser O, Hain T, Goesmann A, Weisshaar B, Albersmeier A et al (2005) Complete genome sequence and analysis of the multiresistant nosocomial pathogen Corynebacterium jeikeium K411, a lipid-requiring bacterium of the human skin flora. J Bacteriol 187:4671–4682

  78. Thomaides HB, Freeman M, El Karoui M, Errington J (2001) Division site selection protein DivIVA of Bacillus subtilis has a second distinct function in chromosome segregation during sporulation. Genes Dev 15:1662–1673

  79. Umeda A, Amako K (1983) Growth of the surface of Corynebacterium diphtheriae. Microbiol Immunol 27:663–671

  80. Valbuena N, Letek M, Ordonez E, Ayala JA, Daniel RA, Gil JA, Mateos LM (2007) Characterization of HMW-PBPs from the rod-shaped actinomycete Corynebacterium glutamicum: peptidoglycan synthesis in cells lacking actin-like cytoskeletal structures. Mol Microbiol 66:643–657

  81. Valbuena N, Letek M, Ramos A, Ayala J, Nakunst D, Kalinowski J et al (2006) Morphological changes and proteome response of Corynebacterium glutamicum to a partial depletion of FtsI. Microbiology 152:2491–2503

  82. Vicente M, Hodgson J, Massidda O, Tonjum T, Henriques-Normark B, Ron EZ (2006) The fallacies of hope: will we discover new antibiotics to combat pathogenic bacteria in time? FEMS Microbiol Rev 30:841–852

  83. Wachi M, Wijayarathna CD, Teraoka H, Nagai K (1999) A murC gene from coryneform bacteria. Appl Microbiol Biotechnol 51:223–228

  84. Wijayarathna CD, Wachi M, Nagai K (2001) Isolation of ftsI and murE genes involved in peptidoglycan synthesis from Corynebacterium glutamicum. Appl Microbiol Biotechnol 55:466–470

  85. Wu LJ, Errington J (2004) Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell 117:915–925

  86. Yukawa H, Omumasaba CA, Nonaka H, Kos P, Okai N, Suzuki N et al (2007) Comparative analysis of the Corynebacterium glutamicum group and complete genome sequence of strain R. Microbiology 153:1042–1058

Download references

Acknowledgments

M. Letek and M. Fiuza were beneficiaries of fellowships from the Ministerio de Educación y Ciencia (Spain); E. Ordóñez and A. Villadangos from the Junta de Castilla y León, and A. Ramos from the ALFA project II-0313-FA-FCB. This work was funded by grants from the Junta de Castilla y León (Ref. LE040A07), University of León (ULE 2001-08B), and Ministerio de Ciencia y Tecnología (BIO2002-03223 and BIO2005-02723). We thank Dr. Ramon Santamaría (Universidad de Salamanca, Spain) for the TEM image of C. glutamicum.

Author information

Correspondence to José A. Gil.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Letek, M., Fiuza, M., Ordóñez, E. et al. Cell growth and cell division in the rod-shaped actinomycete Corynebacterium glutamicum . Antonie van Leeuwenhoek 94, 99–109 (2008). https://doi.org/10.1007/s10482-008-9224-4

Download citation

Keywords

  • Corynebacterium
  • Cell division
  • Cell growth
  • FtsZ
  • DivIVA
  • FtsI
  • HMW-PBP
  • Cell wall