1887

Abstract

In this study, we analysed the gene from , which encodes a homologue of , a gene required for the sporulation of aerial hyphae. Deletion of the gene (Δ) severely affected cell growth in . The Δ strain exhibited a large filamentous, branched and bud-shaped morphology with multiple septa. The transcription levels of the cell division genes involved in Z-ring assembly and septal peptidoglycan synthesis, including , , and , were markedly decreased in the Δ strain. The gene, which is responsible for apical growth, also showed decreased transcription in the Δ strain. However, genes involved in the later stages of cell division, such as cell separation and chromosome segregation, did not show notable changes in their transcription levels. Moreover, the mutant strain was susceptible to inhibitors of transpeptidation, including penicillin and vancomycin. In addition, the transcription of genes , and , which participate in the synthesis of fatty acid and cell envelope component mycolic acid, was altered in the Δ strain. This increased the cell surface hydrophobicity in the mutant strain, apparently leading to cell aggregation in liquid media. These findings indicate that is a -like gene with roles in the early stages of cell division and fatty acid synthesis, and the pleiotropic phenotypes of the Δ strain suggest that may be a global regulatory gene.

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2017-02-01
2024-03-28
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References

  1. Stackebrandt E, Rainey FA, Ward-Rainey NL. Proposal for a new hierarchic classification system, Actinobacteria classis nov. Int J Syst Bacteriol 1997; 47:479–491 [View Article]
    [Google Scholar]
  2. Eggeling L, Bott M. A giant market and a powerful metabolism: l-lysine provided by Corynebacterium glutamicum. Appl Microbiol Biotechnol 2015; 99:3387–3394 [View Article][PubMed]
    [Google Scholar]
  3. Lee JY, Na YA, Kim E, Lee HS, Kim P. The actinobacterium Corynebacterium glutamicum, an industrialindustrial workhorse. J Microbiol Biotechnol 2016; 26:807–822 [View Article][PubMed]
    [Google Scholar]
  4. Soliveri JA, Gomez J, Bishai WR, Chater KF. Multiple paralogous genes related to the Streptomyces coelicolor developmental regulatory gene whiB are present in Streptomyces and other actinomycetes. Microbiology 2000; 146:333–343 [View Article][PubMed]
    [Google Scholar]
  5. Chater KF, Chandra G. The evolution of development in Streptomyces analysed by genome comparisons. FEMS Microbiol Rev 2006; 30:651–672 [View Article][PubMed]
    [Google Scholar]
  6. Zheng F, Long Q, Xie J. The function and regulatory network of WhiB and WhiB-like protein from comparative genomics and systems biology perspectives. Cell Biochem Biophys 2012; 63:103–108 [View Article][PubMed]
    [Google Scholar]
  7. Gomez JE, Bishai WR. whmD is an essential mycobacterial gene required for proper septation and cell division. Proc Natl Acad Sci USA 2000; 97:8554–8559 [View Article][PubMed]
    [Google Scholar]
  8. Fowler-Goldsworthy K, Gust B, Mouz S, Chandra G, Findlay KC et al. The actinobacteria-specific gene wblA controls major developmental transitions in Streptomyces coelicolor A3(2). Microbiology 2011; 157:1312–1328 [View Article][PubMed]
    [Google Scholar]
  9. Lee JY, Kim HJ, Kim ES, Kim P, Kim Y et al. Regulatory interaction of the Corynebacterium glutamicum whc genes in oxidative stress responses. J Biotechnol 2013; 168:149–154 [View Article][PubMed]
    [Google Scholar]
  10. Choi WW, Park SD, Lee SM, Kim HB, Kim Y et al. The whcA gene plays a negative role in oxidative stress response of Corynebacterium glutamicum. FEMS Microbiol Lett 2009; 290:32–38 [View Article][PubMed]
    [Google Scholar]
  11. Kim TH, Park JS, Kim HJ, Kim Y, Kim P et al. The whcE gene of Corynebacterium glutamicum is important for survival following heat and oxidative stress. Biochem Biophys Res Commun 2005; 337:757–764 [View Article][PubMed]
    [Google Scholar]
  12. Lee JY, Park JS, Kim HJ, Kim Y, Lee HS. Corynebacterium glutamicum whcB, a stationary phase-specific regulatory gene. FEMS Microbiol Lett 2012; 327:103–109 [View Article][PubMed]
    [Google Scholar]
  13. Park JC, Park JS, Kim Y, Kim P, Kim ES et al. SpiE interacts with Corynebacterium glutamicum WhcE and is involved in heat and oxidative stress responses. Appl Microbiol Biotechnol 2016; 100:4063–4072 [View Article][PubMed]
    [Google Scholar]
  14. Raghunand TR, Bishai WR. Mycobacterium smegmatis whmD and its homologue Mycobacterium tuberculosis whiB2 are functionally equivalent. Microbiology 2006; 152:2735–2747 [View Article][PubMed]
    [Google Scholar]
  15. Schwedock J, Mccormick JR, Angert ER, Nodwell JR, Losick R. Assembly of the cell division protein FtsZ into ladder-like structures in the aerial hyphae of Streptomyces coelicolor. Mol Microbiol 1997; 25:847–858 [View Article][PubMed]
    [Google Scholar]
  16. Raghunand TR, Bishai WR. Mapping essential domains of Mycobacterium smegmatis WhmD: insights into WhiB structure and function. J Bacteriol 2006; 188:6966–6976 [View Article][PubMed]
    [Google Scholar]
  17. Letek M, Fiuza M, Ordóñez E, Villadangos AF, Ramos A et al. Cell growth and cell division in the rod-shaped actinomycete Corynebacterium glutamicum. Antonie van Leeuwenhoek 2008; 94:99–109 [View Article][PubMed]
    [Google Scholar]
  18. Letek M, Ordóñez E, Vaquera J, Margolin W, Flärdh K et al. DivIVA is required for polar growth in the MreB-lacking rod-shaped actinomycete Corynebacterium glutamicum. J Bacteriol 2008; 190:3283–3292 [View Article][PubMed]
    [Google Scholar]
  19. Sieger B, Schubert K, Donovan C, Bramkamp M. The lipid II flippase RodA determines morphology and growth in Corynebacterium glutamicum. Mol Microbiol 2013; 90:966–982 [View Article][PubMed]
    [Google Scholar]
  20. Sieger B, Bramkamp M. Interaction sites of DivIVA and RodA from Corynebacterium glutamicum. Front Microbiol 2014; 5:738 [View Article][PubMed]
    [Google Scholar]
  21. Meeske AJ, Riley EP, Robins WP, Uehara T, Mekalanos JJ et al. SEDS proteins are a widespread family of bacterial cell wall polymerases. Nature 2016; 537:634–638 [View Article][PubMed]
    [Google Scholar]
  22. Letek M, Ordóñez E, Fiuza M, Honrubia-Marcos P, Vaquera J et al. Characterization of the promoter region of ftsZ from Corynebacterium glutamicum and controlled overexpression of FtsZ. Int Microbiol 2007; 10:271–282[PubMed]
    [Google Scholar]
  23. Ramos A, Letek M, Campelo AB, Vaquera J, Mateos LM et al. Altered morphology produced by ftsZ expression in Corynebacterium glutamicum ATCC 13869. Microbiology 2005; 151:2563–2572 [View Article][PubMed]
    [Google Scholar]
  24. Donovan C, Bramkamp M. Cell division in Corynebacterineae. Front Microbiol 2014; 5:132 [View Article][PubMed]
    [Google Scholar]
  25. Plocinski P, Ziolkiewicz M, Kiran M, Vadrevu SI, Nguyen HB et al. Characterization of CrgA, a new partner of the Mycobacterium tuberculosis peptidoglycan polymerization complexes. J Bacteriol 2011; 193:3246–3256 [View Article][PubMed]
    [Google Scholar]
  26. Ramos A, Honrubia MP, Vega D, Ayala JA, Bouhss A et al. Characterization and chromosomal organization of the murD-murC-ftsQ region of Corynebacterium glutamicum ATCC 13869. Res Microbiol 2004; 151:2563–2572
    [Google Scholar]
  27. Valbuena N, Letek M, Ramos A, Ayala J, Nakunst D et al. Morphological changes and proteome response of Corynebacterium glutamicum to a partial depletion of FtsI. Microbiology 2006; 152:2491–2503 [View Article][PubMed]
    [Google Scholar]
  28. Valbuena N, Letek M, Ordóñez E, Ayala J, Daniel RA et al. Characterization of HMW-PBPs from the rod-shaped actinomycete Corynebacterium glutamicum: peptidoglycan synthesis in cells lacking actin-like cytoskeletal structures. Mol Microbiol 2007; 66:643–657 [View Article][PubMed]
    [Google Scholar]
  29. Deng LL, Humphries DE, Arbeit RD, Carlton LE, Smole SC et al. Identification of a novel peptidoglycan hydrolase CwlM in Mycobacterium tuberculosis. Biochim Biophys Acta 2005; 1747:57–66 [View Article][PubMed]
    [Google Scholar]
  30. Fiuza M, Canova MJ, Zanella-Cléon I, Becchi M, Cozzone AJ et al. From the characterization of the four serine/threonine protein kinases (PknA/B/G/L) of Corynebacterium glutamicum toward the role of PknA and PknB in cell division. J Biol Chem 2008; 283:18099–18112 [View Article][PubMed]
    [Google Scholar]
  31. Schultz C, Niebisch A, Schwaiger A, Viets U, Metzger S et al. Genetic and biochemical analysis of the serine/threonine protein kinases PknA, PknB, PknG and PknL of Corynebacterium glutamicum: evidence for non-essentiality and for phosphorylation of OdhI and FtsZ by multiple kinases. Mol Microbiol 2009; 74:724–741 [View Article][PubMed]
    [Google Scholar]
  32. Donovan C, Schwaiger A, Krämer R, Bramkamp M. Subcellular localization and characterization of the ParAB system from Corynebacterium glutamicum. J Bacteriol 2010; 192:3441–3451 [View Article][PubMed]
    [Google Scholar]
  33. Grant SG, Jessee J, Bloom FR, Hanahan D. Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc Natl Acad Sci USA 1990; 87:4645–4649 [View Article][PubMed]
    [Google Scholar]
  34. Sambrook J, Russell DW. Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 2001
    [Google Scholar]
  35. Follettie MT, Peoples OP, Agoropoulou C, Sinskey AJ. Gene structure and expression of the Corynebacterium flavum N13 ask-asd operon. J Bacteriol 1993; 175:4096–4103 [View Article][PubMed]
    [Google Scholar]
  36. Park SD, Youn JW, Kim YJ, Lee SM, Kim Y et al. Corynebacterium glutamicum σE is involved in responses to cell surface stresses and its activity is controlled by the anti-σ factor CseE. Microbiology 2008; 154:915–923 [View Article][PubMed]
    [Google Scholar]
  37. Schäfer A, Tauch A, Jäger W, Kalinowski J, Thierbach G et al. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 1994; 145:69–73 [View Article][PubMed]
    [Google Scholar]
  38. Macneil DJ, Occi JL, Gewain KM, Macneil T, Gibbons PH et al. Complex organization of the Streptomyces avermitilis genes encoding the avermectin polyketide synthase. Gene 1992; 115:119–125 [View Article][PubMed]
    [Google Scholar]
  39. Hwang BJ, Yeom HJ, Kim Y, Lee HS. Corynebacterium glutamicum utilizes both transsulfuration and direct sulfhydrylation pathways for methionine biosynthesis. J Bacteriol 2002; 184:1277–1286 [View Article][PubMed]
    [Google Scholar]
  40. Park SD, Lee SN, Park IH, Choi JS, Jeong WK et al. Isolation and characterization of transcriptional elements from Corynebacterium glutamicum. J Microbiol Biotechnol 2004; 14:789–795
    [Google Scholar]
  41. Park JS, Shin S, Kim ES, Kim P, Kim Y et al. Identification of SpiA that interacts with Corynebacterium glutamicum WhcA using a two-hybrid system. FEMS Microbiol Lett 2011; 322:8–14 [View Article][PubMed]
    [Google Scholar]
  42. Rosenberg M, Gutnick D, Rosenberg E. Adherence of bacteria to hydrocarbons: a simple method for measuring cell-surface hydrophobicity. FEMS Microbiol Lett 1980; 9:29–33 [View Article]
    [Google Scholar]
  43. Nešvera J, Pátek M. Plasmids and promoters in corynebacteria and their applications. In Burkovski A. (editor) Corynebacteria: Genomics and Molecular Biology Poole, UK: Caister Academic Press; 2008 pp. 113–154
    [Google Scholar]
  44. Pfeifer-Sancar K, Mentz A, Rückert C, Kalinowski J. Comprehensive analysis of the Corynebacterium glutamicum transcriptome using an improved RNAseq technique. BMC Genomics 2013; 14:888 [View Article][PubMed]
    [Google Scholar]
  45. Guerrero R, Berlanga M. The hidden side of the prokaryotic cell: rediscovering the microbial world. Int Microbiol 2007; 10:157–168[PubMed]
    [Google Scholar]
  46. Honrubia MP, Ramos A, Gil JA. 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 2001; 265:1022–1030[PubMed] [CrossRef]
    [Google Scholar]
  47. Hubbard BK, Walsh CT. Vancomycin assembly: nature's way. Angew Chem Int Ed Engl 2003; 42:730–765 [View Article][PubMed]
    [Google Scholar]
  48. Gande R, Gibson KJ, Brown AK, Krumbach K, Dover LG et al. Acyl-CoA carboxylases (accD2 and accD3), together with a unique polyketide synthase (Cg-pks), are key to mycolic acid biosynthesis in Corynebacterianeae such as Corynebacterium glutamicum and Mycobacterium tuberculosis. J Biol Chem 2004; 279:44847–44857 [View Article][PubMed]
    [Google Scholar]
  49. Lanéelle MA, Tropis M, Daffé M. Current knowledge on mycolic acids in Corynebacterium glutamicum and their relevance for biotechnological processes. Appl Microbiol Biotechnol 2013; 97:9923–9930 [View Article][PubMed]
    [Google Scholar]
  50. Varela C, Rittmann D, Singh A, Krumbach K, Bhatt K et al. MmpL genes are associated with mycolic acid metabolism in mycobacteria and corynebacteria. Chem Biol 2012; 19:498–506 [View Article][PubMed]
    [Google Scholar]
  51. Radmacher E, Alderwick LJ, Besra GS, Brown AK, Gibson KJ et al. Two functional FAS-I type fatty acid synthases in Corynebacterium glutamicum. Microbiology 2005; 151:2421–2427 [View Article][PubMed]
    [Google Scholar]
  52. Gola S, Munder T, Casonato S, Manganelli R, Vicente M. The essential role of SepF in mycobacterial division. Mol Microbiol 2015; 97:560–576 [View Article][PubMed]
    [Google Scholar]
  53. Gupta S, Banerjee SK, Chatterjee A, Sharma AK, Kundu M et al. Essential protein SepF of mycobacteria interacts with FtsZ and MurG to regulate cell growth and division. Microbiology 2015; 161:1627–1638 [View Article][PubMed]
    [Google Scholar]
  54. Hamoen LW, Meile JC, De Jong W, Noirot P, Errington J. SepF, a novel FtsZ-interacting protein required for a late step in cell division. Mol Microbiol 2006; 59:989–999 [View Article][PubMed]
    [Google Scholar]
  55. Yi QM, Rockenbach S, Ward JE, Lutkenhaus J. Structure and expression of the cell division genes ftsQ, ftsA and ftsZ. J Mol Biol 1985; 184:399–412[PubMed] [CrossRef]
    [Google Scholar]
  56. Hett EC, Rubin EJ. Bacterial growth and cell division: a mycobacterial perspective. Microbiol Mol Biol Rev 2008; 72:126–156 [View Article][PubMed]
    [Google Scholar]
  57. Pichoff S, Lutkenhaus J. Tethering the Z ring to the membrane through a conserved membrane targeting sequence in FtsA. Mol Microbiol 2005; 55:1722–1734 [View Article][PubMed]
    [Google Scholar]
  58. Kimura E, Abe C, Kawahara Y, Nakamatsu T, Tokuda H. A dtsR gene-disrupted mutant of Brevibacterium lactofermentum requires fatty acids for growth and efficiently produces l-glutamate in the presence of an excess of biotin. Biochem Biophys Res Commun 1997; 234:157–161 [View Article][PubMed]
    [Google Scholar]
  59. Lea-Smith DE, Pyke JS, Tull D, Mcconville MJ, Coppel RL et al. The reductase that catalyzes mycolic motif synthesis is required for efficient attachment of mycolic acids to arabinogalactan. J Biol Chem 2007; 282:11000–11008 [View Article][PubMed]
    [Google Scholar]
  60. Portevin D, De Sousa-D'Auria C, Houssin C, Grimaldi C, Chami M et al. A polyketide synthase catalyzes the last condensation step of mycolic acid biosynthesis in mycobacteria and related organisms. Proc Natl Acad Sci USA 2004; 101:314–319 [View Article][PubMed]
    [Google Scholar]
  61. Portevin D, De Sousa-D'Auria C, Montrozier H, Houssin C, Stella A et al. The acyl-AMP ligase FadD32 and AccD4-containing acyl-CoA carboxylase are required for the synthesis of mycolic acids and essential for mycobacterial growth: identification of the carboxylation product and determination of the acyl-CoA carboxylase components. J Biol Chem 2005; 280:8862–8874 [View Article][PubMed]
    [Google Scholar]
  62. Kacem R, De Sousa-D'Auria C, Tropis M, Chami M, Gounon P et al. Importance of mycoloyltransferases on the physiology of Corynebacterium glutamicum. Microbiology 2004; 150:73–84 [View Article][PubMed]
    [Google Scholar]
  63. Lee SM, Lee JY, Park KJ, Park JS, Ha UH et al. The regulator RamA influences cmytA transcription and cell morphology of Corynebacterium ammoniagenes. Curr Microbiol 2010; 61:92–100 [View Article][PubMed]
    [Google Scholar]
  64. Follettie MT, Sinskey AJ. Recombinant DNA technology for Corynebacterium glutamicum. Food Technol 1986; 40:88–94
    [Google Scholar]
  65. Yoshihama M, Higashiro K, Rao EA, Akedo M, Shanabruch WG et al. Cloning vector system for Corynebacterium glutamicum. J Bacteriol 1985; 162:591–597[PubMed]
    [Google Scholar]
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