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.
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References
Bendt AK, Burkovski A, Schaffer S, Bott M, Farwick M, HermannT (2003) Towards a phosphoproteome map of Corynebacterium glutamicum. Proteomics 3:1637–1646
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
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
Cadenas RF, Fernandez-Gonzalez C, Martin JF, Gil JA (1996) Construction of new cloning vectors for Brevibacterium lactofermentum. FEMS Microbiol Lett 137:63–68
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
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
Cha JH, Stewart GC (1997) The divIVA minicell locus of Bacillus subtilis. J Bacteriol 179:1671–1683
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
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
Collins MD, Goodfellow M, Minnikin DE (1982) Fatty acid composition of some mycolic acid-containing coryneform bacteria. J Gen Microbiol 128:2503–2509
Courvalin P, Davies J (2003) Antimicrobials. Curr Opin Microbiol 6:425–529
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
Daniel RA, Errington J (2003) Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 113:767–776
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
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
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
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
Errington J, Daniel RA, Scheffers DJ (2003) Cytokinesis in bacteria. Microbiol Mol Biol Rev 67:52–65, table
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
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
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
Flardh K (2003a) Essential role of DivIVA in polar growth and morphogenesis in Streptomyces coelicolor A3(2). Mol Microbiol 49:1523–1536
Flardh K (2003b) Growth polarity and cell division in Streptomyces. Curr Opin Microbiol 6:564–571
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
Goehring NW, Beckwith J (2005) Diverse paths to midcell: assembly of the bacterial cell division machinery. Curr Biol 15:514–526
Goffin C, Ghuysen JM (1998) Multimodular penicillin-binding proteins: an enigmatic family of orthologs and paralogs. Microbiol Mol Biol Rev 62:1079–1093
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
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
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
Hermann T (2003) Industrial production of amino acids by coryneform bacteria. J Biotechnol 104:155–172
Hermann T, Pfefferle W, Baumann C, Busker E, Schaffer S, Bott M et al (2001) Proteome analysis of Corynebacterium glutamicum. Electrophoresis 22:1712–1723
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
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
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
Ikeda M, Nakagawa S (2003) The Corynebacterium glutamicum genome: features and impacts on biotechnological processes. Appl Microbiol Biotechnol 62:99–109
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
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
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
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
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
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
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
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
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)
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Pinho MG, Errington J (2004) A divIVA null mutant of Staphylococcus aureus undergoes normal cell division. FEMS Microbiol Lett 240:145–149
Polen T, Wendisch VF (2004) Genomewide expression analysis in amino acid-producing bacteria using DNA microarrays. Appl Biochem Biotechnol 118:215–232
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
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
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
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
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
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
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
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
Santamaria RI, Gil JA, Martin JF (1985) High-frequency transformation of Brevibacterium lactofermentum protoplasts by plasmid DNA. J Bacteriol 162:463–467
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
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
Scheffers DJ, Jones LJ, Errington J (2004) Several distinct localization patterns for penicillin-binding proteins in Bacillus subtilis. Mol Microbiol 51:749–764
Scheffers DJ, Pinho MG (2005) Bacterial cell wall synthesis: new insights from localization studies. Microbiol Mol Biol Rev 69:585–607
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
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
Tamames J, Gonzalez-Moreno M, Mingorance J, Valencia A, Vicente M (2001) Bringing gene order into bacterial shape. Trends Genet 17:124–126
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
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
Umeda A, Amako K (1983) Growth of the surface of Corynebacterium diphtheriae. Microbiol Immunol 27:663–671
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
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
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
Wachi M, Wijayarathna CD, Teraoka H, Nagai K (1999) A murC gene from coryneform bacteria. Appl Microbiol Biotechnol 51:223–228
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
Wu LJ, Errington J (2004) Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell 117:915–925
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
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.
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Timelapse of C. glutamicum growing on complex medium at room temperature. The pictures were taken every 20 minutes during 12 hours (DOC 19 kb)
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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
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DOI: https://doi.org/10.1007/s10482-008-9224-4