Skip to main content
Log in

Pivotal roles for Streptomyces cell surface polymers in morphological differentiation, attachment and mycelial architecture

  • Invited Review
  • Antonie van Leeuwenhoek 80th Anniversary Issue
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

Cells that are part of a multicellular structure are typically embedded in an extracellular matrix, which is produced by the community members. These matrices, the composition of which is highly diverse between different species, are typically composed of large amounts of extracellular polymeric substances, including polysaccharides, proteins, and nucleic acids. The functions of all these matrices are diverse: they provide protection, mechanical stability, mediate adhesion to surfaces, regulate motility, and form a cohesive network in which cells are transiently immobilized. In this review we discuss the role of matrix components produced by streptomycetes during growth, development and attachment. Compared to other bacteria it appears that streptomycetes can form morphologically and functionally distinct matrices using a core set of building blocks.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alteri CJ, Xicohténcatl-Cortes J, Hess S, Caballero-Olin G, Girón JA, Friedman RL (2007) Mycobacterium tuberculosis produces pili during human infection. Proc Natl Acad Sci USA 104:5145–5150

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Barnes AM, Ballering KS, Leibman RS, Wells CL, Dunny GM (2012) Enterococcus faecalis produces abundant extracellular structures containing DNA in the absence of cell lysis during early biofilm formation. MBio 3:e00112–e00193

    Article  Google Scholar 

  • Bibb MJ, Domonkos A, Chandra G, Buttner MJ (2012) Expression of the chaplin and rodlin hydrophobic sheath proteins in Streptomyces venezuelae is controlled by σ(BldN) and a cognate anti-sigma factor, RsbN. Mol Microbiol 84:1033–1049

    Article  CAS  PubMed  Google Scholar 

  • Blake CC, Serpell LC (1996) Synchrotron X-ray studies suggest that the core of the transthyretin amyloid fibril is a continuous β-sheet helix. Structure 4:989–998

    Article  CAS  PubMed  Google Scholar 

  • Blanco LP, Evans ML, Smith DR, Badtke MP, Chapman MR (2012) Diversity, biogenesis and function of microbial amyloids. Trends Microbiol 20:66–73

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bokhove M, Claessen D, de Jong W, Dijkhuizen L, Boekema EJ, Oostergetel GT (2013) Chaplins of Streptomyces coelicolor self-assemble into two distinct functional amyloids. J Struct Biol 184:301–309

    Article  CAS  PubMed  Google Scholar 

  • Capstick DS, Willey JM, Buttner MJ, Elliot MA (2007) SapB and the chaplins: connections between morphogenetic proteins in Streptomyces coelicolor. Mol Microbiol 64:602–613

    Article  CAS  PubMed  Google Scholar 

  • Capstick DS, Jomaa A, Hanke C, Ortega J, Elliot MA (2011) Dual amyloid domains promote differential functioning of the chaplin proteins during Streptomyces aerial morphogenesis. Proc Natl Acad Sci USA 108:9821–9826

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Celler K, Picioreanu C, van Loosdrecht MC, van Wezel GP (2012) Structured morphological modeling as a framework for rational strain design of Streptomyces species. Antonie Van Leeuwenhoek 102:409–423

    Article  PubMed Central  PubMed  Google Scholar 

  • Chater KF, Biro S, Lee KJ, Palmer T, Schrempf H (2010) The complex extracellular biology of Streptomyces. FEMS Microbiol Rev 34:171–198

    Article  CAS  PubMed  Google Scholar 

  • Claessen D, Wösten HAB, van Keulen G, Faber OG, Alves AM, Meijer WG, Dijkhuizen L (2002) Two novel homologous proteins of Streptomyces coelicolor and Streptomyces lividans are involved in the formation of the rodlet layer and mediate attachment to a hydrophobic surface. Mol Microbiol 44:1483–1492

    Article  CAS  PubMed  Google Scholar 

  • Claessen D, Rink R, de Jong W, Siebring J, de Vreugd P, Boersma FG, Dijkhuizen L, Wösten HAB (2003) A novel class of secreted hydrophobic proteins is involved in aerial hyphae formation in Streptomyces coelicolor by forming amyloid-like fibrils. Genes Dev 17:1714–1726

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Claessen D, Stokroos I, Deelstra HJ, Penninga NA, Bormann C, Salas JA, Dijkhuizen L, Wösten HAB (2004) The formation of the rodlet layer of streptomycetes is the result of the interplay between rodlins and chaplins. Mol Microbiol 53:433–443

    Article  CAS  PubMed  Google Scholar 

  • Cot M, Ray A, Gilleron M, Vercellone A, Larrouy-Maumus G, Armau E, Gauthier S, Tiraby G, Puzo G, Nigou J (2011) Lipoteichoic acid in Streptomyces hygroscopicus: structural model and immunomodulatory activities. PLoS ONE 6:e26316

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • de Jong W, Wösten HAB, Dijkhuizen L, Claessen D (2009) Attachment of Streptomyces coelicolor is mediated by amyloidal fimbriae that are anchored to the cell surface via cellulose. Mol Microbiol 73:1128–1140

    Article  PubMed  Google Scholar 

  • de Jong W, Vijgenboom E, Dijkhuizen L, Wösten HAB, Claessen D (2012) SapB and the rodlins are required for development of Streptomyces coelicolor in high osmolarity media. FEMS Microbiol Lett 329:154–159

    Article  PubMed  Google Scholar 

  • de Vocht ML, Reviakine I, Ulrich W-P, Bergsma-Schutter W, Wösten HAB, Vogel H, Brisson A, Wessels JGH, Robillard GT (2002) Self-assembly of the hydrophobin SC3 proceeds via two structural intermediates. Protein Sci 11:1199–1205

    Article  PubMed Central  PubMed  Google Scholar 

  • den Hengst CD, Tran NT, Bibb MJ, Chandra G, Leskiw BK, Buttner MJ (2010) Genes essential for morphological development and antibiotic production in Streptomyces coelicolor are targets of BldD during vegetative growth. Mol Microbiol 78:361–379

    Article  Google Scholar 

  • 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 190:5879–5889

    Article  PubMed Central  PubMed  Google Scholar 

  • Dueholm MS, Petersen SV, Sonderkaer M, Larsen P, Christiansen G, Hein KL, Enghild JJ, Nielsen JL, Nielsen KL, Nielsen PH, Otzen DE (2010) Functional amyloid in Pseudomonas. Mol Microbiol 77:1009–1020

    CAS  Google Scholar 

  • Duong A, Capstick DS, Di Berardo C, Findlay KC, Hesketh A, Hong HJ, Elliot MA (2012) Aerial development in Streptomyces coelicolor requires sortase activity. Mol Microbiol 83:992–1005

    Article  CAS  PubMed  Google Scholar 

  • Ekkers DM, Claessen D, Galli F, Stamhuis EJ (2014) Surface modification using interfacial assembly of the Streptomyces chaplin proteins. Appl Microbiol Biotechnol (in press). doi:10.1007/s00253-013-5463-z

  • Elliot MA, Talbot NJ (2004) Building filaments in the air: aerial morphogenesis in bacteria and fungi. Curr Opin Microbiol 7:594–601

    Article  CAS  PubMed  Google Scholar 

  • 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 17:1727–1740

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Flärdh K, Buttner MJ (2009) Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat Rev Microbiol 7:36–49

    Article  PubMed  Google Scholar 

  • Gaskell AA, Giovinazzo JA, Fonte V, Willey JM (2012) Multi-tier regulation of the streptomycete morphogenetic peptide SapB. Mol Microbiol 84:501–515

    Article  CAS  PubMed  Google Scholar 

  • Gebbink MFBG, Claessen D, Bouma B, Dijkhuizen L, Wösten HAB (2005) Amyloids—a functional coat for microorganisms. Nat Rev Microbiol 3:333–341

    Article  CAS  PubMed  Google Scholar 

  • Gras SL, Claessen D (2014) Functional amyloid fibrils: lessons from microbes. In: Havlicek V, Spizek J (eds) Natural products analysis: instrumentation, methods, and applications. Wiley, New York (in press)

  • Hammer ND, Schmidt JC, Chapman MR (2007) The curli nucleator protein, CsgB, contains an amyloidogenic domain that directs CsgA polymerization. Proc Natl Acad Sci USA 104:12494–12499

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hengge R (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7:263–273

    Article  CAS  PubMed  Google Scholar 

  • Hong HJ, Paget MSB, Buttner MJ (2002) A signal transduction system in Streptomyces coelicolor that activates the expression of a putative cell wall glycan operon in response to vancomycin and other cell wall-specific antibiotics. Mol Microbiol 44:1199–1211

    Article  CAS  PubMed  Google Scholar 

  • Hopwood DA (2007) Streptomyces in nature and medicine: the antibiotic makers. Oxford University Press, USA

    Google Scholar 

  • Hughes AH, Hancock IC, Baddiley J (1973) The function of teichoic acids in cation control in bacterial membranes. Biochem J 132:83–93

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hull TD, Ryu MH, Sullivan MJ, Johnson RC, Klena NT, Geiger RM, Gomelsky M, Bennett JA (2012) Cyclic Di-GMP phosphodiesterases RmdA and RmdB are involved in regulating colony morphology and development in Streptomyces coelicolor. J Bacteriol 194:4642–4651

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kershaw MJ, Talbot NJ (1998) Hydrophobins and repellents: proteins with fundamental roles in fungal morphogenesis. Fungal Genet Biol 23:18–33

    Article  CAS  PubMed  Google Scholar 

  • Khurana R, Uversky VN, Nielsen L, Fink AL (2001) Is Congo red an amyloid-specific dye? J Biol Chem 276:22715–22721

    Article  CAS  PubMed  Google Scholar 

  • Kim YM, Kim JH (2004) Formation and dispersion of mycelial pellets of Streptomyces coelicolor A3(2). J Microbiol 42:64–67

    PubMed  Google Scholar 

  • Kirschner DA, Abraham C, Selkoe DJ (1986) X-ray diffraction from intraneuronal paired helical filaments and extraneuronal amyloid fibers in Alzheimer disease indicates cross-β conformation. Proc Natl Acad Sci USA 83:503–507

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kleinschnitz EM, Latus A, Sigle S, Maldener I, Wohlleben W, Muth G (2011) Genetic analysis of SCO2997, encoding a TagF homologue, indicates a role for wall teichoic acids in sporulation of Streptomyces coelicolor A3(2). J Bacteriol 193:6080–6085

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kodani S, Hudson ME, Durrant MC, Buttner MJ, Nodwell JR, Willey JM (2004) The SapB morphogen is a antibiotic-like peptide derived from the product of the developmental gene ramS in Streptomyces coelicolor. Proc Natl Acad Sci USA 101:11448–11453

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kodani S, Lodato MA, Durrant MC, Picart F, Willey JM (2005) SapT, a lanthionine-containing peptide involved in aerial hyphae formation in the streptomycetes. Mol Microbiol 58:1368–1380

    Article  CAS  PubMed  Google Scholar 

  • Liman R, Facey PD, van Keulen G, Dyson PJ, Del Sol R (2013) A laterally acquired galactose oxidase-like gene is required for aerial development during osmotic stress in Streptomyces coelicolor. PLoS ONE 8:e54112

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lugones LG, de Jong JF, de Vries OMH, Jalving R, Dijksterhuis J, Wösten HAB (2004) The SC15 protein of Schizophyllum commune mediates formation of aerial hyphae and attachment in the absence of the SC3 hydrophobin. Mol Microbiol 53:707–716

    Article  CAS  PubMed  Google Scholar 

  • Manteca A, Alvarez R, Salazar N, Yagüe P, Sanchez J (2008) Mycelium differentiation and antibiotic production in submerged cultures of Streptomyces coelicolor. Appl Environ Microbiol 74:3877–3886

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Matthysse AG (1986) Initial interactions of Agrobacterium tumefaciens with plant host cells. Crit Rev Microbiol 13:281–307

    Article  CAS  PubMed  Google Scholar 

  • Nieminen L, Webb S, Smith MCM, Hoskisson PA (2013) A flexible mathematical model platform for studying branching networks: experimentally validated using the model actinomycete, Streptomyces coelicolor. PLoS One 8:e54316

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ostash B, Shashkov A, Streshinskaya G, Tul’skaya E, Baryshnikova L, Dmitrenok A, Dacyuk Y, Fedorenko V (2014) Identification of Streptomyces coelicolor M145 genomic region involved in biosynthesis of teichulosonic acid-cell wall glycopolymer. Folia Microbiol (in press). doi:10.1007/s12223-014-0306-6

  • Pastor MT, Esteras-Chopo A, Serrano L (2007) Hacking the code of amyloid formation: the amyloid stretch hypothesis. Prion 1:9–14

    Article  PubMed Central  PubMed  Google Scholar 

  • Potekhina NV, Streshinskaya GM, Tul’skaya EM, Shashkov AS (2011) Cell wall teichoic acids in the taxonomy and characterization of Gram-positive bacteria. Method Microbiol 38:131–164

    Article  CAS  Google Scholar 

  • Rahman O, Cummings SP, Sutcliffe IC (2009) Phenotypic variation in Streptomyces sp. DSM 40537, a lipoteichoic acid producing actinomycete. Lett Appl Microbiol 48:226–229

    Article  CAS  PubMed  Google Scholar 

  • Rioseras B, López-García MT, Yagüe P, Sánchez J, Manteca A (2013) Mycelium differentiation and development of Streptomyces coelicolor in lab-scale bioreactors: programmed cell death, differentiation, and lysis are closely linked to undecylprodigiosin and actinorhodin production. Bioresour Technol 151C:191–198

    Google Scholar 

  • Romero D, Aguilar C, Losick R, Kolter R (2010) Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc Natl Acad Sci USA 107:2230–2234

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Römling U (2002) Molecular biology of cellulose production in bacteria. Res Microbiol 153:205–212

    Article  PubMed  Google Scholar 

  • Ross P, Mayer R, Benziman M (1991) Cellulose biosynthesis and function in bacteria. Microbiol Rev 55:35–58

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sawyer EB, Claessen D, Haas M, Hurgobin B, Gras SL (2011) The assembly of individual chaplin peptides from Streptomyces coelicolor into functional amyloid fibrils. PLoS One 6:e18839

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sawyer EB, Claessen D, Gras SL, Perrett S (2012) Exploiting amyloid: how and why bacteria use cross-beta fibrils. Biochem Soc Trans 40:728–734

    Article  CAS  PubMed  Google Scholar 

  • Schäffer C, Messner P (2005) The structure of secondary cell wall polymers: how Gram-positive bacteria stick their cell walls together. Microbiology 151:643–651

    Article  PubMed  Google Scholar 

  • Schneewind O, Missiakas DM (2012) Protein secretion and surface display in Gram-positive bacteria. Philos Trans R Soc Lond B Biol Sci 367:1123–1139

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Scholtmeijer K, de Vocht ML, Rink R, Robillard GT, Wösten HAB (2009) Assembly of the fungal SC3 hydrophobin into functional amyloid fibrils depends on its concentration and is promoted by cell wall polysaccharides. J Biol Chem 284:26309–26314

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Serra DO, Richter AM, Hengge R (2013) Cellulose as an architectural element in spatially structured Escherichia coli biofilms. J Bacteriol 195:5540–5554

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shashkov AS, Kosmachevskaya LN, Streshinskaya GM, Evtushenko LI, Bueva OV, Denisenko VA, Naumova IB, Stackebrandt E (2002) A polymer with a backbone of 3-deoxy-d-glycero-d-galacto-non-2-ulopyranosonic acid, a teichuronic acid, and a beta-glucosylated ribitol teichoic acid in the cell wall of plant pathogenic Streptomyces sp. VKM Ac-2124. Eur J Biochem 269:6020–6025

    Article  CAS  PubMed  Google Scholar 

  • Silakowski B, Pospiech A, Neumann B, Schairer HU (1996) Stigmatella aurantiaca fruiting body formation is dependent on the fbfA gene encoding a polypeptide homologous to chitin synthases. J Bacteriol 178:6706–6713

    CAS  PubMed Central  PubMed  Google Scholar 

  • Silakowski B, Ehret H, Schairer HU (1998) fbfB, a gene encoding a putative galactose oxidase, is involved in Stigmatella aurantiaca fruiting body formation. J Bacteriol 180:1241–1247

    CAS  PubMed Central  PubMed  Google Scholar 

  • Simm R, Morr M, Kader A, Nimtz M, Römling U (2004) GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 53:1123–1134

    Article  CAS  PubMed  Google Scholar 

  • Sunde M, Serpell LC, Bartlam M, Fraser PE, Pepys MB, Blake CC (1997) Common core structure of amyloid fibrils by synchrotron X-ray diffraction. J Mol Biol 273:729–739

    Article  CAS  PubMed  Google Scholar 

  • Talbot NJ (1997) Growing into the air. Curr Biol 7:R78–R81

    Article  CAS  PubMed  Google Scholar 

  • Talbot NJ, Ebbole DJ, Hamer JE (1993) Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell 5:1575–1590

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Talbot NJ, Kershaw MJ, Wakley GE, De Vries OMH, Wessels JGH, Hamer JE (1996) MPG1 encodes a fungal hydrophobin Involved in surface interactions during infection-related development of Magnaporthe grisea. Plant Cell 8:985–999

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tillotson RD, Wösten HAB, Richter M, Willey JM (1998) A surface active protein involved in aerial hyphae formation in the filamentous fungus Schizophyllum commune restores the capacity of a bald mutant of the filamentous bacterium Streptomyces coelicolor to erect aerial structures. Mol Microbiol 30:595–602

    Article  CAS  PubMed  Google Scholar 

  • Tran NT, Den Hengst CD, Gomez-Escribano JP, Buttner MJ (2011) Identification and characterization of CdgB, a diguanylate cyclase involved in developmental processes in Streptomyces coelicolor. J Bacteriol 193:3100–3108

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tresner HD, Hayes JA, Backus EJ (1967) Morphology of submerged growth of streptomycetes as a taxonomic aid. I. Morphological development of Streptomyces aureofaciens in agitated liquid media. Appl Microbiol 15:1185–1191

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tul’skaya EM, Shashkov AS, Streshinskaya GM, Senchenkova SN, Potekhina NV, Kozlova YI, Evtushenko LI (2011) Teichuronic and teichulosonic acids of actinomycetes. Biochemistry (Moscow) 76:736–744

    Article  Google Scholar 

  • Ueda K, Oinuma K, Ikeda G, Hosono K, Ohnishi Y, Horinouchi S, Beppu T (2002) AmfS, an extracellular peptidic morphogen in Streptomyces griseus. J Bacteriol 184:1488–1492

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • van Keulen G, Jonkers HM, Claessen D, Dijkhuizen L, Wösten HAB (2003) Differentiation and anaerobiosis in standing liquid cultures of Streptomyces coelicolor. J Bacteriol 185:1455–1458

    Article  PubMed Central  PubMed  Google Scholar 

  • van Veluw GJ, Petrus MLC, Gubbens J, de Graaf R, de Jong IP, van Wezel GP, Wösten HAB, Claessen D (2012) Analysis of two distinct mycelial populations in liquid-grown Streptomyces cultures using a flow cytometry-based proteomics approach. Appl Microbiol Biotechnol 96:1301–1312

    Article  CAS  PubMed  Google Scholar 

  • van Wezel GP, Krabben P, Traag BA, Keijser BJF, Kerste R, Vijgenboom E, Heijnen JJ, Kraal B (2006) Unlocking Streptomyces spp. for use as sustainable industrial production platforms by morphological engineering. Appl Environ Microbiol 72:5283–5288

    Article  PubMed Central  PubMed  Google Scholar 

  • Vecht-Lifshitz SE, Magdassi S, Braun S (1990) Pellet formation and cellular aggregation in Streptomyces tendae. Biotechnol Bioeng 35:890–896

    Article  CAS  PubMed  Google Scholar 

  • Wardell JN, Stocks SM, Thomas CR, Bushell ME (2002) Decreasing the hyphal branching rate of Saccharopolyspora erythraea NRRL 2338 leads to increased resistance to breakage and increased antibiotic production. Biotechnol Bioeng 78:141–146

    Article  CAS  PubMed  Google Scholar 

  • Weidenmaier C, Peschel A (2008) Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat Rev Microbiol 6:276–287

    Article  CAS  PubMed  Google Scholar 

  • Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS (2002) Extracellular DNA required for bacterial biofilm formation. Science 295:1487

    Article  CAS  PubMed  Google Scholar 

  • White AP, Gibson DL, Collinson SK, Banser PA, Kay WW (2003) Extracellular polysaccharides associated with thin aggregative fimbriae of Salmonella enterica serovar enteritidis. J Bacteriol 185:5398–5407

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Whittaker MM, Whittaker JW (2006) Streptomyces coelicolor oxidase (SCO2837p): a new free radical metalloenzyme secreted by Streptomyces coelicolor A3(2). Arch Biochem Biophys 452:108–118

    Article  CAS  PubMed  Google Scholar 

  • Wildermuth H, Wehrli E, Horne RW (1971) The surface structure of spores and aerial mycelium in Streptomyces coelicolor. J Ultrastruct Res 35:168–180

    Article  CAS  PubMed  Google Scholar 

  • Willey J, Santamaria R, Guijarro J, Geistlich M, Losick R (1991) Extracellular complementation of a developmental mutation implicates a small sporulation protein in aerial mycelium formation by S. coelicolor. Cell 65:641–650

    Article  CAS  PubMed  Google Scholar 

  • Willey JM, Willems A, Kodani S, Nodwell JR (2006) Morphogenetic surfactants and their role in the formation of aerial hyphae in Streptomyces coelicolor. Mol Microbiol 59:731–742

    Article  CAS  PubMed  Google Scholar 

  • Wösten HAB, De Vries OMH, Wessels JGH (1993) Interfacial self-assembly of a fungal hydrophobin into a hydrophobic rodlet layer. Plant Cell 5:1567–1574

    Article  PubMed Central  PubMed  Google Scholar 

  • Wösten HAB, Schuren FHJ, Wessels JGH (1994) Interfacial self-assembly of a hydrophobin into an amphipathic protein membrane mediates fungal attachment to hydrophobic surfaces. EMBO J 13:5848–5854

    PubMed Central  PubMed  Google Scholar 

  • Wösten HAB, van Wetter MA, Lugones LG, van der Mei HC, Busscher HJ, Wessels JGH (1999) How a fungus escapes the water to grow into the air. Curr Biol 9:85–88

    Article  PubMed  Google Scholar 

  • Xu H, Chater KF, Deng Z, Tao M (2008) A cellulose synthase-like protein involved in hyphal tip growth and morphological differentiation in Streptomyces. J Bacteriol 190:4971–4978

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yeats C, Bentley S, Bateman A (2003) New knowledge from old: in silico discovery of novel protein domains in Streptomyces coelicolor. BMC Microbiol 3:3

    Article  PubMed Central  PubMed  Google Scholar 

  • Zogaj X, Nimtz M, Rohde M, Bokranz W, Römling U (2001) The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol Microbiol 39:1452–1463

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The work was supported by a Vidi grant from the Dutch Applied Research Council to D.C.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dennis Claessen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Petrus, M.L.C., Claessen, D. Pivotal roles for Streptomyces cell surface polymers in morphological differentiation, attachment and mycelial architecture. Antonie van Leeuwenhoek 106, 127–139 (2014). https://doi.org/10.1007/s10482-014-0157-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-014-0157-9

Keywords

Navigation