Surface hydrophobicity and roughness influences the morphology and biochemistry of streptomycetes during attached growth and differentiation

FEMS Microbiology Letters

Volumn 342, Issue 2, 2013, Pages 147-156

  Petráčková, Denisa ^a   Buriánková, Karolína ^a   Tesařová, Eva ^a   Bobková, Šárka ^a   Bezoušková, Silvia ^a   Benada, Oldřich ^a   Kofroňová, Olga ^a   Janeček, Jiří ^a   Halada, Petr ^a   Weiser, Jaroslav ^a  

^a INSTITUTE OF MICROBIOLOGY   (Czech Republic)

Author keywords

Antibiotic production; Attached growth; Glass beads; Proteome; Streptomyces granaticolor; Streptomycetes

Indexed keywords

AMIDOPHOSPHORIBOSYLTRANSFERASE; CYSTATHIONINE BETA SYNTHASE; DIHYDROLIPOAMIDE DEHYDROGENASE; GLASS; GRANATICIN; SILICON DIOXIDE;

ARTICLE; BACTERIAL GROWTH; BACTERIUM ADHERENCE; BIOMASS; CONTROLLED STUDY; HYDROPHILICITY; HYDROPHOBICITY; MYCELIUM; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; ROUGHNESS; SPECIES CULTIVATION; STREPTOMYCES; STREPTOMYCES GRANATICOLOR; STRUCTURE ANALYSIS; SURFACE PROPERTY;

ANTI-BACTERIAL AGENTS; BACTERIAL ADHESION; BACTERIAL PROTEINS; BIOMASS; CELLS, IMMOBILIZED; GENE EXPRESSION; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; NAPHTHOQUINONES; STREPTOMYCES; SURFACE PROPERTIES;

BACTERIA (MICROORGANISMS); STREPTOMYCES GRANATICOLOR; STREPTOMYCINEAE;

EID: 84876857808     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/1574-6968.12129     Document Type: Article

References (42)

1. Amemiya M, Ueno M, Osono M, Masuda T, Kinoshita N, Nishida C, Hamada M, Ishizuka M & Takeuchi T (1994) Cytostatin, a novel inhibitor of cell-adhesion to components of extracellular-matrix produced by Streptomyces sp MJ654-NF4.I. Taxonomy, fermentation, isolation and biological-activities. J Antibiot 47: 536-540.
2. Bergmann S, Rohde M & Hammerschmidt S (2004) Glyceraldehyde-3-phosphate dehydrogenase of Streptococcus pneumoniae is a surface-displayed plasminogen-binding protein. Infect Immun 72: 2416-2419.
3. Bos R, van der Mei HC & Busscher HJ (1999) Physico-chemistry of initial microbial adhesive interactions - its mechanisms and methods for study. FEMS Microbiol Rev 23: 179-230.
4. Chater KF, Biró S, Lee KJ, Palmer T & Schrempf H (2010) The complex extracellular biology of Streptomyces. FEMS Microbiol Rev 34: 171-198.
5. Claessen D, de Jong W, Dijkhuizen L & Wosten HAB (2006) Regulation of Streptomyces development: reach for the sky!. Trends Microbiol 14: 313-319.
6. Danson MJ (1988) Dihydrolipoamide dehydrogenase: a new function for an old enzyme. Biochem Soc Trans 16: 87-89.
7. de Jong W, Vijgenboom E, Dijkhuizen L, Wosten 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.
8. Del Sol R, Armstrong I, Wright C & Dyson P (2007) Characterization of changes to the cell surface during the life cycle of Streptomyces coelicolor: atomic force microscopy of living cells. J Bacteriol 189: 2219-2225.
9. Doull JL & Vining LC (1989) Culture conditions promoting dispersed growth and biphasic production of actinorhodin in shaken cultures of Streptomyces coelicolor A3(2). FEMS Microbiol Lett 65: 265-268.
10. Dunne WM (2002) Bacterial adhesion: seen any good biofilms lately? Clin Microbiol Rev 15: 155-166.
11. Elliot MA, Karoonuthaisiri N, Huang JQ, 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.
12. Flemming HC & Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8: 623-633.
13. Hesketh AR, Chandra G, Shaw AD, Rowland JJ, Kell DB, Bibb MJ & Chater KF (2002) Primary and secondary metabolism, and post-translational protein modifications, as portrayed by proteomic analysis of Streptomyces coelicolor. Mol Microbiol 46: 917-932.
14. Hesketh A, Chen WQ, Ryding J, Chang S & Bibb M (2007) The global role of ppGpp synthesis in morphological differentiation and antibiotic production in Streptomyces coelicolor A3(2). Genome Biol 8: R161.
15. Hodgson DA (2000) Primary metabolism and its control in streptomycetes: a most unusual group of bacteria. Adv Microb Physiol 42: 47-238.
16. Holub M, Bezouskova S, Petrackova D, Kalachova L, Kofronova O, Benada O & Weiser J (2010) Comparative study of the life cycle dependent post-translation modifications of protein synthesis elongation factor Tu present in the membrane proteome of streptomycetes and mycobacteria. Folia Microbiol 55: 203-210.
17. James PDA & Edwards C (1989) The effects of temperature on growth and production of the antibiotic granaticin by a thermotolerant streptomycete. J Gen Microbiol 135: 1997-2003.
18. Kieser T, Bibb MJ, Buttner MJ, Chater KF & Hopwood DA (eds.) (2000) Preparation of aerial mycelium and spores separately. Practical Streptomycetes Genetics (Chapter 4: Specialised biochemical techniques), pp. 75-77. The John Innes Foundation, Norwich, UK.
19. Kofronova O, Nguyen LD, Weiser J & Benada O (2002) Streptomycetes cultured on glass beads - sample preparation for SEM. Microsc Res Tech 58: 111-113.
20. Liu Y, Yang SF, Li Y, Xu H, Qin L & Tay JH (2004) The influence of cell and substratum surface hydrophobicities on microbial attachment. J Biotechnol 110: 251-256.
21. Manteca A, Mader U, Connolly BA & Sanchez J (2006) A proteomic analysis of Streptomyces coelicolor programmed cell death. Proteomics 6: 6008-6022.
22. Manteca A, Alvarez R, Salazar N, Yague P & Sanchez J (2008) Mycelium differentiation and antibiotic production in submerged cultures of Streptomyces coelicolor. Appl Environ Microbiol 74: 3877-3886.
23. Manteca A, Jung HR, Schwammle V, Jensen ON & Sanchez J (2010) Quantitative proteome analysis of Streptomyces coelicolor nonsporulating liquid cultures demonstrates a complex differentiation process comparable to that occurring in sporulating solid cultures. J Proteome Res 9: 4801-4811.
24. Manteca A, Ye J, Sánchez J & Jensen ON (2011) Phosphoproteome analysis of Streptomyces development reveals extensive protein phosphorylation accompanying bacterial differentiation. J Proteome Res 10: 5481-5492.
25. Martin JF, Sola-Landa A, Santos-Beneit F, Fernandez-Martinez LT, Prieto C & Rodriguez-Garcia A (2011) Cross-talk of global nutritional regulators in the control of primary and secondary metabolism in Streptomyces. Microb Biotechnol 4: 165-174.
26. McDougald D, Rice SA, Barraud N, Steinberg PD & Kjelleberg S (2012) Should we stay or should we go: mechanisms and ecological consequences for biofilm dispersal. Nat Rev Microbiol 10: 39-50.
27. Nezbedova S, Bezouskova S, Kofronova O, Benada O, Rehulka P, Rehulkova H, Goldova J, Janecek J & Weiser J (2011) The use of glass beads cultivation system to study the global effect of the ppk gene inactivation in Streptomyces lividans. Folia Microbiol 56: 519-525.
28. Nguyen LD, Kalachova L, Novotna J, Holub M, Kofronova O, Benada O, Thompson CJ & Weiser J (2005) Cultivation system using glass beads immersed in liquid medium facilitates studies of Streptomyces differentiation. Appl Environ Microbiol 71: 2848-2852.
29. Perham RN, Packman LC & Radford SE (1987) 2-Oxo acid dehydrogenase multi-enzyme complexes: in the beginning and halfway there. Biochem Soc Symp 54: 67-81.
30. Phillips NJ, Steichen CT, Schilling B, Post DM, Niles RK, Bair TB, Falsetta ML, Apicella MA & Gibson BW (2012) Proteomic analysis of Neisseria gonorrhoeae biofilms shows shift to anaerobic respiration and changes in nutrient transport and outermembrane proteins. PLoS ONE 7: e38303.
31. Piattoni CV, Bustos DM, Guerrero SA & Iglesias AA (2011) Nonphosphorylating glyceraldehyde-3-phosphate dehydrogenase is phosphorylated in wheat endosperm at serine-404 by an SNF1-related protein kinase allosterically inhibited by ribose-5-phosphate. Plant Physiol 156: 1337-1350.
32. Raynal A, Karray F, Tuphile K, Darbon-Rongere E & Pernodet JL (2006) Excisable cassettes: new tools for functional analysis of Streptomyces genomes. Appl Environ Microbiol 72: 4839-4844.
33. Secor PR, James GA, Fleckman P, Olerud JE, McInnerney K & Stewart PS (2011) Staphylococcus aureus Biofilm and Planktonic cultures differentially impact gene expression, mapk phosphorylation, and cytokine production in human keratinocytes. BMC Microbiol 11: 143.
34. Severin A, Nickbarg E, Wooters J, Quazi SA, Matsuka YV, Murphy E, Moutsatsos IK, Zagursky RJ & Olmsted SB (2007) Proteomic analysis and identification of Streptococcus pyogenes surface-associated proteins. J Bacteriol 189: 1514-1522.
35. Siegmann A, Komarska A, Betzalel Y, Brudo I, Jindou S, Mor G & Fleminger G (2009) The titanium binding protein of Rhodococcus ruber GIN1 (NCIMB 40340) is a cell-surface homolog of the cytosolic enzyme dihydrolipoamide dehydrogenase. J Mol Recognit 22: 138-145.
36. Smith AW, Roche H, Trombe M-C, Briles DE & Håkansson A (2002) Characterization of the dihydrolipoamide dehydrogenase from Streptococcus pneumoniae and its role in pneumococcal infection. Mol Microbiol 44: 431-448.
37. Susstrunk U, Pidoux J, Taubert S, Ullmann A & Thompson CJ (1998) Pleiotropic effects of cAMP on germination, antibiotic biosynthesis and morphological development in Streptomyces coelicolor. Mol Microbiol 30: 33-46.
38. Tisdale EJ (2002) Glyceraldehyde-3-phosphate dehydrogenase is phosphorylated by protein kinase Cι/λ and plays a role in microtubule dynamics in the early secretory pathway. J Biol Chem 277: 3334-3341.
39. Van Hoogmoed CG, Van der Mei HC & Busscher HJ (1997) The influence of calcium on the initial adhesion of S.thermophilus to stainless steel under flow studied by metallurgical microscopy. Biofouling 11: 167-176.
40. Zhang QL, Schrader KK, ElSohly HN & Takamatsu S (2003) New cell-cell adhesion inhibitors from Streptomyces sp UMA-044. J Antibiot 56: 673-681.
41. Zhou Z, Gu JY, Du YL, Li YQ & Wang YF (2011) The -omics era- toward a systems-level understanding of Streptomyces. Curr Genomics 12: 404-416.
42. Zita A & Hermansson M (1997) Effects of bacterial cell surface structures and hydrophobicity on attachment to activated sludge flocs. Appl Environ Microbiol 63: 1168-1170.