Growth and Life Cycle of Actinobacteria

  • Javad HamediEmail author
  • Naghmeh Poorinmohammad
  • Reyhaneh Papiran


Since actinobacteria inhabit a vast range of ecological niches, their life cycle and growth dynamics have been evolved while acquiring different strategies for efficient survival. Of these differentiation strategies, spore (better to be called conidium due to their reproductive nature) formation in actinomycetes, the formation of resting cells discussed earlier in Chap.  5, or the complex cell envelope of Corynebacteriaceae and Mycobacteriaceae to produce more resistant forms of vegetative cells can be named. Accordingly, one of the most well-studied bacteria within the taxon is the filamentous actinobacteria (i.e., Streptomyces) for whom the exact true life cycle is presented and the dynamics are well elucidated. However, much more efforts regarding the growth dynamics of other members of actinobacteria are required to fulfill our interest of having a comprehensive insight of their physiology of growth and cell division. Herein, the available data together with recent studies on the growth and differentiation of these bacteria are discussed.


  1. Ainsa J, Ryding N, Hartley N, Findlay K, Bruton C, Chater K (2000) WhiA, a protein of unknown function conserved among gram-positive bacteria, is essential for sporulation in Streptomyces coelicolor A3 (2). J Bacteriol 182(19):5470–5478CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alonso A, Pomposiello P, Leschine S (2008) Biofilm formation in the life cycle of the cellulolytic actinomycete Thermobifida fusca. Biofilms 2008:1–11CrossRefGoogle Scholar
  3. Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Klenk H-P et al (2016) Taxonomy, physiology, and natural products of Actinobacteria. Microbiol Mol Biol Rev 80(1):1–43CrossRefPubMedGoogle Scholar
  4. Burger A, Sichler K, Kelemen G, Buttner M, Wohlleben W (2000) Identification and characterization of the mre gene region of Streptomyces coelicolor A3 (2). Mol Gen Genet MGG 263(6):1053–1060CrossRefPubMedGoogle Scholar
  5. Bush MJ, Bibb MJ, Chandra G, Findlay KC, Buttner MJ (2013) Genes required for aerial growth, cell division, and chromosome segregation are targets of WhiA before sporulation in Streptomyces venezuelae. MBio 4(5):e00684–e00613CrossRefPubMedPubMedCentralGoogle Scholar
  6. Capstick DS, Willey JM, Buttner MJ, Elliot MA (2007) SapB and the chaplins: connections between morphogenetic proteins in Streptomyces coelicolor. Mol Microbiol 64(3):602–613CrossRefPubMedGoogle Scholar
  7. Chater K (1975) Construction and phenotypes of double sporulation deficient mutants in Streptomyces coelicolor A3 (2). Microbiology 87(2):312–325Google Scholar
  8. Chater KF, Chandra G (2006) The evolution of development in Streptomyces analysed by genome comparisons. FEMS Microbiol Rev 30(5):651–672CrossRefPubMedGoogle Scholar
  9. Claessen D, Rink R, de Jong W, Siebring J, de Vreugd P, Boersma FH et al (2003) A novel class of secreted hydrophobic proteins is involved in aerial hyphae formation in Streptomyces coelicolor by forming amyloid-like fibrils. Genes Dev 17(14):1714–1726CrossRefPubMedPubMedCentralGoogle Scholar
  10. Claessen D, Stokroos I, Deelstra HJ, Penninga NA, Bormann C, Salas JA et al (2004) The formation of the rodlet layer of streptomycetes is the result of the interplay between rodlins and chaplins. Mol Microbiol 53(2):433–443CrossRefPubMedGoogle Scholar
  11. D'Alia D, Eggle D, Nieselt K, Hu WS, Breitling R, Takano E (2011) Deletion of the signalling molecule synthase ScbA has pleiotropic effects on secondary metabolite biosynthesis, morphological differentiation and primary metabolism in Streptomyces coelicolor A3 (2). Microb Biotechnol 4(2):239–251CrossRefPubMedPubMedCentralGoogle Scholar
  12. Dalton KA, Thibessard A, Hunter JI, Kelemen GH (2007) A novel compartment, the ‘subapical stem’ of the aerial hyphae, is the location of a sigN-dependent, developmentally distinct transcription in Streptomyces coelicolor. Mol Microbiol 64(3):719–737CrossRefPubMedGoogle Scholar
  13. Daza A, Martin JF, Dominguez A, Gil JA (1989) Sporulation of several species of Streptomyces in submerged cultures after nutritional downshift. Microbiology 135(9):2483–2491CrossRefGoogle Scholar
  14. Dedrick RM, Wildschutte H, McCormick JR (2009) Genetic interactions of smc, ftsK, and parB genes in Streptomyces coelicolor and their developmental genome segregation phenotypes. J Bacteriol 191(1):320–332CrossRefPubMedGoogle Scholar
  15. Di Berardo C, Capstick DS, Bibb MJ, Findlay KC, Buttner MJ, Elliot MA (2008) Function and redundancy of the chaplin cell surface proteins in aerial hypha formation, rodlet assembly, and viability in Streptomyces coelicolor. J Bacteriol 190(17):5879–5889CrossRefPubMedPubMedCentralGoogle Scholar
  16. Ditkowski B, Holmes N, Rydzak J, Donczew M, Bezulska M, Ginda K et al (2013) Dynamic interplay of ParA with the polarity protein, Scy, coordinates the growth with chromosome segregation in Streptomyces coelicolor. Open biology 3(3):130006CrossRefPubMedPubMedCentralGoogle Scholar
  17. Donczew M, Mackiewicz P, Wróbel A, Flärdh K, Zakrzewska-Czerwińska J, Jakimowicz D (2016) ParA and ParB coordinate chromosome segregation with cell elongation and division during Streptomyces sporulation. Open biology 6(4):150263CrossRefPubMedPubMedCentralGoogle Scholar
  18. Donovan C, Bramkamp M (2014) Cell division in Corynebacterineae. Front Microbiol 5:132CrossRefPubMedPubMedCentralGoogle Scholar
  19. Ekkers DM, Claessen D, Galli F, Stamhuis E (2014) Surface modification using interfacial assembly of the Streptomyces chaplin proteins. Appl Microbiol Biotechnol 98(10):4491–4501CrossRefPubMedGoogle Scholar
  20. Elliot MA, Karoonuthaisiri N, Huang J, Bibb MJ, Cohen SN, Kao CM, Buttner MJ (2003) The chaplins: a family of hydrophobic cell-surface proteins involved in aerial mycelium formation in Streptomyces coelicolor. Genes Dev 17(14):1727–1740CrossRefPubMedPubMedCentralGoogle Scholar
  21. Errington J, Daniel RA, Scheffers D-J (2003) Cytokinesis in bacteria. Microbiol Mol Biol Rev 67(1):52–65CrossRefPubMedPubMedCentralGoogle Scholar
  22. Flärdh K, Buttner MJ (2009) Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat Rev Microbiol 7(1):36–49CrossRefPubMedGoogle Scholar
  23. Flärdh K, Findlay KC, Chater KF (1999) Association of early sporulation genes with suggested developmental decision points in Streptomyces coelicolor A3 (2). Microbiology 145(9):2229–2243CrossRefPubMedGoogle Scholar
  24. Flärdh K, Richards DM, Hempel AM, Howard M, Buttner MJ (2012) Regulation of apical growth and hyphal branching in Streptomyces. Curr Opin Microbiol 15(6):737–743CrossRefPubMedGoogle Scholar
  25. Fuhrmann C, Soedarmanto I, Lämmler C (1997) Studies on the Rod-Coccus life cycle of Rhodococcus equi. J Veterinary Med Ser B 44(1–10):287–294CrossRefGoogle Scholar
  26. Glazebrook MA, Doull JL, Stuttard C, Vining LC (1990) Sporulation of Streptomyces venezuelae in submerged cultures. Microbiology 136(3):581–588Google Scholar
  27. Goodfellow M, Alderson G, Chun J (1998) Rhodococcal systematics: problems and developments. Antonie Van Leeuwenhoek 74(1–3):3–20CrossRefPubMedGoogle Scholar
  28. Gray D, Gooday G, Prosser J (1990) Apical hyphal extension in Streptomyces coelicolor A3 (2). Microbiology 136(6):1077–1084Google Scholar
  29. Haiser HJ, Yousef MR, Elliot MA (2009) Cell wall hydrolases affect germination, vegetative growth, and sporulation in Streptomyces coelicolor. J Bacteriol 191(21):6501–6512CrossRefPubMedPubMedCentralGoogle Scholar
  30. Halbedel S, Visser L, Shaw M, Wu LJ, Errington J, Marenduzzo D, Hamoen LW (2009) Localisation of DivIVA by targeting to negatively curved membranes. EMBO J 28(15):2272–2282CrossRefPubMedPubMedCentralGoogle Scholar
  31. Heichlinger A, Ammelburg M, Kleinschnitz E-M, Latus A, Maldener I, Flärdh K et al (2011) The MreB-like protein Mbl of Streptomyces coelicolor A3 (2) depends on MreB for proper localization and contributes to spore wall synthesis. J Bacteriol 193(7):1533–1542CrossRefPubMedPubMedCentralGoogle Scholar
  32. Hett EC, Rubin EJ (2008) Bacterial growth and cell division: a mycobacterial perspective. Microbiol Mol Biol Rev 72(1):126–156CrossRefPubMedPubMedCentralGoogle Scholar
  33. Hopwood DA, Wildermuth H, Palmer HM (1970) Mutants of Streptomyces coelicolor defective in sporulation. Microbiology 61(3):397–408Google Scholar
  34. Jakimowicz D, van Wezel GP (2012) Cell division and DNA segregation in Streptomyces: how to build a septum in the middle of nowhere? Mol Microbiol 85(3):393–404CrossRefPubMedGoogle Scholar
  35. Joyce G, Williams KJ, Robb M, Noens E, Tizzano B, Shahrezaei V, Robertson BD (2012) Cell division site placement and asymmetric growth in mycobacteria. PLoS One 7(9):e44582CrossRefPubMedPubMedCentralGoogle Scholar
  36. Jyothikumar V, Tilley EJ, Wali R, Herron PR (2008) Time-lapse microscopy of Streptomyces coelicolor growth and sporulation. Appl Environ Microbiol 74(21):6774–6781CrossRefPubMedPubMedCentralGoogle Scholar
  37. Kalakoutskii L, Agre NS (1976) Comparative aspects of development and differentiation in actinomycetes. Bacteriol Rev 40(2):469PubMedPubMedCentralGoogle Scholar
  38. Kang C-M, 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(14):1692–1704CrossRefPubMedPubMedCentralGoogle Scholar
  39. Kang C-M, Nyayapathy S, Lee J-Y, Suh J-W, Husson RN (2008) Wag31, a homologue of the cell division protein DivIVA, regulates growth, morphology and polar cell wall synthesis in mycobacteria. Microbiology 154(3):725–735CrossRefPubMedGoogle Scholar
  40. Kaval KG, Halbedel S (2012) Architecturally the same, but playing a different game: the diverse species-specific roles of DivIVA proteins. Virulence 3(4):406–407CrossRefPubMedPubMedCentralGoogle Scholar
  41. Kieser KJ, Rubin EJ (2014) How sisters grow apart: mycobacterial growth and division. Nat Rev Microbiol 12(8):550–562CrossRefPubMedGoogle Scholar
  42. Kim SH, Traag BA, Hasan AH, McDowall KJ, Kim B-G, van Wezel GP (2015) Transcriptional analysis of the cell division-related ssg genes in Streptomyces coelicolor reveals direct control of ssgR by AtrA. Antonie Van Leeuwenhoek 108(1):201–213CrossRefPubMedPubMedCentralGoogle Scholar
  43. Kleinschnitz EM, Heichlinger A, Schirner K, Winkler J, Latus A, Maldener I et al (2011) Proteins encoded by the MRE gene cluster in Streptomyces coelicolor A3 (2) cooperate in spore wall synthesis. Mol Microbiol 79(5):1367–1379CrossRefPubMedGoogle Scholar
  44. Kontro M, Lignell U, Hirvonen MR, Nevalainen A (2005) pH effects on 10 Streptomyces spp. growth and sporulation depend on nutrients. Lett Appl Microbiol 41(1):32–38CrossRefPubMedGoogle Scholar
  45. Kontroab M, Lignella U, Hyvärinena A, Vahteristoa M, Hirvonena M, Nevalainena A (2007) Nutrient effects on ten Streptomyces spp. sporulation, in Communicating Current Research nd Educational Topics and Trends in Applied Microbiology. Formatex 137–142Google Scholar
  46. Kwak J, Dharmatilake AJ, Jiang H, Kendrick KE (2001) Differential regulation of ftsZ Transcription during septation of streptomyces griseus. J Bacteriol 183(17):5092–5101CrossRefPubMedPubMedCentralGoogle Scholar
  47. Manteca A, Sanchez J (2010) Streptomyces developmental cycle and secondary metabolite production. Curr Res Technol Educ Top Appl Microbiol Microb Biotechnol 1:560–566Google Scholar
  48. Mazza P, Noens EE, Schirner K, Grantcharova N, Mommaas AM, Koerten HK et al (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(4):838–852CrossRefPubMedGoogle Scholar
  49. McCormick JR (2009) Cell division is dispensable but not irrelevant in Streptomyces. Curr Opin Microbiol 12(6):689–698CrossRefPubMedGoogle Scholar
  50. McCormick JR, Flärdh K (2012) Signals and regulators that govern Streptomyces development. FEMS Microbiol Rev 36(1):206–231CrossRefPubMedGoogle Scholar
  51. Mendez C, Chater KF (1987) Cloning of whiG, a gene critical for sporulation of Streptomyces coelicolor A3 (2). J Bacteriol 169(12):5715–5720CrossRefPubMedPubMedCentralGoogle Scholar
  52. Miguélez EM, Martín C, Manzanal MB, Hardisson C (1992) Growth and morphogenesis in Streptomyces. FEMS Microbiol Lett 100(1–3):351–359CrossRefPubMedGoogle Scholar
  53. Molle V, Palframan WJ, Findlay KC, Buttner MJ (2000) WhiD and WhiB, homologous proteins required for different stages of sporulation in Streptomyces coelicolor A3 (2). J Bacteriol 182(5):1286–1295CrossRefPubMedPubMedCentralGoogle Scholar
  54. Noens EE, Mersinias V, Traag BA, Smith CP, Koerten HK, van Wezel GP (2005) SsgA-like proteins determine the fate of peptidoglycan during sporulation of Streptomyces coelicolor. Mol Microbiol 58(4):929–944CrossRefPubMedGoogle Scholar
  55. Palazzotto E, Renzone G, Fontana P, Botta L, Scaloni A, Puglia AM, Gallo G (2015) Tryptophan promotes morphological and physiological differentiation in Streptomyces coelicolor. Appl Microbiol Biotechnol 99(23):10177–10189CrossRefPubMedGoogle Scholar
  56. Pérez J, Muñoz-Dorado J, Braña AF, Shimkets LJ, Sevillano L, Santamaría RI (2011) Myxococcus xanthus induces actinorhodin overproduction and aerial mycelium formation by Streptomyces coelicolor. Microb Biotechnol 4(2):175–183CrossRefPubMedPubMedCentralGoogle Scholar
  57. Santi I, Dhar N, Bousbaine D, Wakamoto Y, McKinney JD (2013) Single-cell dynamics of the chromosome replication and cell division cycles in mycobacteria. Nat Commun 4:2470PubMedGoogle Scholar
  58. Scherr N, Nguyen L (2009) Mycobacterium versus Streptomyces—we are different, we are the same. Curr Opin Microbiol 12(6):699–707CrossRefPubMedGoogle Scholar
  59. Schwedock J, McCormick J, Angert E, Nodwell J, Losick R (1997) Assembly of the cell division protein FtsZ into ladder-like structures in the aerial hyphae of Streptomyces coelicolor. Mol Microbiol 25(5):847–858CrossRefPubMedGoogle Scholar
  60. Singh B, Nitharwal RG, Ramesh M, Pettersson B, Kirsebom LA, Dasgupta S (2013) Asymmetric growth and division in Mycobacterium spp.: compensatory mechanisms for non-medial septa. Mol Microbiol 88(1):64–76CrossRefPubMedGoogle Scholar
  61. Tan H, Tian Y, Yang H, Liu G, Nie L (2002) A novel Streptomyces gene, samR, with different effects on differentiation of Streptomyces ansochromogenes and Streptomyces coelicolor. Arch Microbiol 177(3):274–278CrossRefPubMedGoogle Scholar
  62. Traag BA, van Wezel GP (2008) The SsgA-like proteins in actinomycetes: small proteins up to a big task. Antonie Van Leeuwenhoek 94(1):85–97CrossRefPubMedPubMedCentralGoogle Scholar
  63. Wang S-B, Cantlay S, Nordberg N, Letek M, Gil JA, Flärdh K (2009) Domains involved in the in vivo function and oligomerization of apical growth determinant DivIVA in Streptomyces coelicolor. FEMS Microbiol Lett 297(1):101–109CrossRefPubMedGoogle Scholar
  64. White EL, Ross LJ, Reynolds RC, Seitz LE, Moore GD, Borhani DW (2000) Slow polymerization of Mycobacterium tuberculosis FtsZ. J Bacteriol 182(14):4028–4034CrossRefPubMedPubMedCentralGoogle Scholar
  65. Wildermuth H, Hopwood D (1970) Septation during sporulation in Streptomyces coelicolor. Microbiology 60(1):51–59Google Scholar
  66. Willemse J, Borst JW, de Waal E, Bisseling T, van Wezel GP (2011) Positive control of cell division: FtsZ is recruited by SsgB during sporulation of Streptomyces. Genes Dev 25(1):89–99CrossRefPubMedPubMedCentralGoogle Scholar
  67. Yagüe P, López-García MT, Rioseras B, Sánchez J, Manteca Á (2013) Pre-sporulation stages of Streptomyces differentiation: state-of-the-art and future perspectives. FEMS Microbiol Lett 342(2):79–88CrossRefPubMedPubMedCentralGoogle Scholar
  68. Zhang L, Willemse J, Claessen D, van Wezel GP (2016) SepG coordinates sporulation-specific cell division and nucleoid organization in Streptomyces coelicolor. Open biology 6(4):150164CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Javad Hamedi
    • 1
    • 2
    Email author
  • Naghmeh Poorinmohammad
    • 1
    • 2
  • Reyhaneh Papiran
    • 1
    • 2
  1. 1.Department of Microbial Biotechnology, School of Biology and Center of Excellence in Phylogeny of Living OrganismsCollege of Science, University of TehranTehranIran
  2. 2.Microbial Technology and Products Research CenterUniversity of TehranTehranIran

Personalised recommendations