A novel locus for mycelial aggregation forms a gateway to improved Streptomyces cell factories

Microbial Cell Factories

Volumn 14, Issue 1, 2015, Pages

  van Dissel, Dino ^a   Claessen, Dennis ^a   Roth, Martin ^b   Van Wezel, Gilles P ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b HANS KNÖLL INSTITUTE   (Germany)

Author keywords

Actinomycete; Antibiotic; Genome sequencing; Morphology; Pellet; Reverse engineering

Indexed keywords

MESSENGER RNA; POLYSACCHARIDE SYNTHASE; SYNTHETASE; UNCLASSIFIED DRUG; AMIDASE; BACTERIAL PROTEIN; GLUCOSYLTRANSFERASE; POLYSACCHARIDE DEACETYLASE;

ARTICLE; BACTERIAL GENETICS; BACTERIAL GROWTH; BIOREACTOR; COSMID; DNA FLANKING REGION; GENE CLUSTER; GENE DELETION; GENE FUNCTION; GENE LOCUS; GENE MUTATION; GROWTH RATE; HOMOLOGOUS RECOMBINATION; INDUSTRIAL PRODUCTION; LOXP SITE; METAMORPHOSIS; MICROBIAL MORPHOLOGY; MORPHOGENESIS; MYCELIUM; NONHUMAN; PHENOTYPE; PHYLOGENY; REVERSE ENGINEERING; SINGLE NUCLEOTIDE POLYMORPHISM; STOP CODON; STREPTOMYCES; STREPTOMYCES LIVIDANS; STREPTOMYCETACEAE; TRANSPOSON; WILD TYPE; BIOMASS; DEVICES; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; MULTIGENE FAMILY; MUTATION; PROCEDURES; REPRODUCIBILITY;

STREPTOMYCES; STREPTOMYCES LIVIDANS; STREPTOMYCINEAE;

AMIDOHYDROLASES; BACTERIAL PROTEINS; BACTERIOLOGICAL TECHNIQUES; BIOMASS; GLUCOSYLTRANSFERASES; INDUSTRIAL MICROBIOLOGY; MULTIGENE FAMILY; MUTATION; POLYMORPHISM, SINGLE NUCLEOTIDE; REPRODUCIBILITY OF RESULTS; STREPTOMYCES LIVIDANS;

EID: 84926675935     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/s12934-015-0224-6     Document Type: Article

References (76)

1. Hopwood DA. Streptomyces in nature and medicine: the antibiotic makers. New York: Oxford University Press; 2007.
2. Vrancken K, Anne J. Secretory production of recombinant proteins by Streptomyces. Future Microbiol. 2009;4:181-8.
3. Claessen D, Rozen DE, Kuipers OP, Sogaard-Andersen L, van Wezel GP. Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodies. Nat Rev Microbiol. 2014;12:115-24.
4. Chater KF, Losick R. Mycelial life style of Streptomyces coelicolor A3(2) and its relatives. In: Shapiro JA, Dworkin M, editors. Bacteria as multicellular organisms. New York: Oxford University Press; 1997. p. 149-82.
5. Jakimowicz D, van Wezel GP. Cell division and DNA segregation in Streptomyces: how to build a septum in the middle of nowhere? Mol Microbiol. 2012;85:393-404.
6. McCormick JR. Cell division is dispensable but not irrelevant in Streptomyces. Curr Opin Biotechnol. 2009;12:689-98.
7. van Dissel D, Claessen D, Van Wezel GP. Morphogenesis of Streptomyces in submerged cultures. Adv Appl Microbiol. 2014;89:1-45.
8. Celler K, Picioreanu C, van Loosdrecht MC, van Wezel GP. Structured morphological modeling as a framework for rational strain design of Streptomyces species. Antonie Van Leeuwenhoek. 2012;102:409-23.
9. Cerri MO, Badino AC. Shear conditions in clavulanic acid production by Streptomyces clavuligerus in stirred tank and airlift bioreactors. Bioprocess Biosyst Eng. 2012;35:977-84.
10. Tough AJ, Prosser JI. Experimental verification of a mathematical model for pelleted growth of Streptomyces coelicolor A3(2) in submerged batch culture. Microbiology. 1996;142:1332.
11. Roubos JA, Krabben P, Luiten RG, Verbruggen HB, Heijnen JJ. A quantitative approach to characterizing cell lysis caused by mechanical agitation of Streptomyces clavuligerus. Biotechnol Prog. 2001;17:336-47.
12. Crook N, Alper HS. Classical Strain Improvement. In: Patnaik R, editor. Engineering Complex Phenotypes in Industrial Strains. Hoboken: John Wiley & Sons, Inc; 2013. p. 1-33.
13. van den Berg MA, Albang R, Albermann K, Badger JH, Daran JM, Driessen AJ, et al. Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum. Nat Biotechnol. 2008;26:1161-8.
14. Koekman B, Hans M. The Clavulanic Acid Strain Improvement Program at DSM Anti-Infectives. In: Patnaik R, editor. Engineering Complex Phenotypes in Industrial Strains. Hoboken: John Wiley & Sons, Inc; 2013. p. 169-83.
15. Oud B, van Maris AJ, Daran JM, Pronk JT. Genome-wide analytical approaches for reverse metabolic engineering of industrially relevant phenotypes in yeast. FEMS Yeast Res. 2012;12:183-96.
16. van Wezel GP, Krabben P, Traag BA, Keijser BJ, Kerste R, Vijgenboom E, et al. Unlocking Streptomyces spp. for use as sustainable industrial production platforms by morphological engineering. Appl Environ Microbiol. 2006;72:5283-8.
17. Traag BA, van Wezel GP. The SsgA-like proteins in actinomycetes: small proteins up to a big task. Antonie Van Leeuwenhoek. 2008;94:85-97.
18. Noens EE, Mersinias V, Willemse J, Traag BA, Laing E, Chater KF, et al. Loss of the controlled localization of growth stage-specific cell-wall synthesis pleiotropically affects developmental gene expression in an ssgA mutant of Streptomyces coelicolor. Mol Microbiol. 2007;64:1244-59.
19. van Wezel GP, van der Meulen J, Kawamoto S, Luiten RG, Koerten HK, Kraal B. ssgA is essential for sporulation of Streptomyces coelicolor A3(2) and affects hyphal development by stimulating septum formation. J Bacteriol. 2000;182:5653-62.
20. Koebsch I, Overbeck J, Piepmeyer S, Meschke H, Schrempf H. A molecular key for building hyphae aggregates: the role of the newly identified Streptomyces protein HyaS. Microb Biotechnol. 2009;2:343-60.
21. van Veluw GJ, Petrus ML, Gubbens J, de Graaf R, de Jong IP, van Wezel GP, et al. Analysis of two distinct mycelial populations in liquid-grown Streptomyces cultures using a flow cytometry-based proteomics approach. Appl Microbiol Biotechnol. 2012;96:1301-12.
22. Bailey JE, Sburlati A, Hatzimanikatis V, Lee K, Renner WA, Tsai PS. Inverse metabolic engineering: A strategy for directed genetic engineering of useful phenotypes. Biotechnol Bioeng. 1996;52:109-21.
23. Smith KM, Liao JC. An evolutionary strategy for isobutanol production strain development in Escherichia coli. Metab Eng. 2011;13:674-81.
24. Swinnen S, Schaerlaekens K, Pais T, Claesen J, Hubmann G, Yang Y, et al. Identification of novel causative genes determining the complex trait of high ethanol tolerance in yeast using pooled-segregant whole-genome sequence analysis. Genome Res. 2012;22:975-84.
25. Ikeda M, Ohnishi J, Hayashi M, Mitsuhashi S. A genome-based approach to create a minimally mutated Corynebacterium glutamicum strain for efficient L-lysine production. J Ind Microbiol Biotechnol. 2006;33:610-5.
26. Ravasi P, Peiru S, Gramajo H, Menzella HG. Design and testing of a synthetic biology framework for genetic engineering of Corynebacterium glutamicum. Microb Cell Fact. 2012;11:147.
27. Roth M, Noack D, Geuther R. Maintenance of the recombinant plasmid pIJ2 in chemostat cultures of Streptomyces lividans 66 (pIJ2). J Basic Microbiol. 1985;25:265-71.
28. Roth M, Hoffmeier C, Geuther R, Muth G, Wohlleben W. Segregational stability of pSG5-derived vector plasmids in continuous cultures. Biotechnol Lett. 1994;16:1225-30.
29. Cruz-Morales P, Vijgenboom E, Iruegas-Bocardo F, Girard G, Yanez-Guerra LA, Ramos-Aboites HE, et al. The genome sequence of Streptomyces lividans 66 reveals a novel tRNA-dependent peptide biosynthetic system within a metal-related genomic island. Genome Biol Evol. 2013;5:1165-75.
30. Lawlor EJ, Baylis HA, Chater KF. Pleiotropic morphological and antibiotic deficiencies result from mutations in a gene encoding a tRNA-like product in Streptomyces coelicolor A3(2). Genes Dev. 1987;1:1305-10.
31. Leskiw BK, Bibb MJ, Chater KF. The use of a rare codon specifically during development? Mol Microbiol. 1991;5:2861-7.
32. Chatfield CH, Koo H, Quivey Jr RG. The putative autolysin regulator LytR in Streptococcus mutans plays a role in cell division and is growth-phase regulated. Microbiology. 2005;151:625-31.
33. Kawai Y, Marles-Wright J, Cleverley RM, Emmins R, Ishikawa S, Kuwano M, et al. A widespread family of bacterial cell wall assembly proteins. EMBO J. 2011;30:4931-41.
34. Hübscher J, McCallum N, Sifri CD, Majcherczyk PA, Entenza JM, Heusser R, et al. MsrR contributes to cell surface characteristics and virulence in Staphylococcus aureus. FEMS Microbiol Lett. 2009;295:251-60.
35. Fernandez-Martinez LT, Del Sol R, Evans MC, Fielding S, Herron PR, Chandra G, et al. A transposon insertion single-gene knockout library and new ordered cosmid library for the model organism Streptomyces coelicolor A3(2). Antonie Van Leeuwenhoek. 2011;99:515-22.
36. Levin-Karp A, Barenholz U, Bareia T, Dayagi M, Zelcbuch L, Antonovsky N, et al. Quantifying translational coupling in E. coli synthetic operons using RBS modulation and fluorescent reporters. ACS Synth Biol. 2013;2:327-36.
37. Gust B, O'Rourke S, Bird N, Kieser T, Chater K. Recombineering in Streptomyces coelicolor. Norwich: The John Innes Foundation; 2003.
38. Katz E, Thompson CJ, Hopwood DA. Cloning and expression of the tyrosinase gene from Streptomyces antibioticus in Streptomyces lividans. J Gen Microbiol. 1983;129(Pt 9):2703-14.
39. Novick A, Szilard L. Experiments with the Chemostat on spontaneous mutations of bacteria. Proc Natl Acad Sci U S A. 1950;36:708-19.
40. O'Toole G, Kaplan HB, Kolter R. Biofilm formation as microbial development. Annu Rev Microbiol. 2000;54:49-79.
41. J-h K, Hancock IC. Pellet forming and fragmentation in liquid culture of Streptomyces griseus. Biotechnol Lett. 2000;22:189-92.
42. Archer NK, Mazaitis MJ, Costerton JW, Leid JG, Powers ME, Shirtliff ME. Staphylococcus aureus biofilms: properties, regulation, and roles in human disease. Virulence. 2011;2:445-59.
43. Mack D, Fischer W, Krokotsch A, Leopold K, Hartmann R, Egge H, et al. The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1,6-linked glucosaminoglycan: purification and structural analysis. J Bacteriol. 1996;178:175-83.
44. McKenney D, Hubner J, Muller E, Wang Y, Goldmann DA, Pier GB. The ica locus of Staphylococcus epidermidis encodes production of the capsular polysaccharide/adhesin. Infect Immun. 1998;66:4711-20.
45. Götz F. Staphylococcus and biofilms. Mol Microbiol. 2002;43:1367-78.
46. Wang X, Preston 3rd JF, Romeo T. The pgaABCD locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation. J Bacteriol. 2004;186:2724-34.
47. Abu Khweek A, Fetherston JD, Perry RD. Analysis of HmsH and its role in plague biofilm formation. Microbiology. 2010;156:1424-38.
48. Xu H, Chater KF, Deng Z, Tao M. A cellulose synthase-like protein involved in hyphal tip growth and morphological differentiation in Streptomyces. J Bacteriol. 2008;190:4971-8.
49. Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, Minguez P, et al. The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res. 2011;39:D561-8.
50. Pogliano J, Pogliano K, Weiss DS, Losick R, Beckwith J. Inactivation of FtsI inhibits constriction of the FtsZ cytokinetic ring and delays the assembly of FtsZ rings at potential division sites. Proc Natl Acad Sci U S A. 1997;94:559-64.
51. Ikeda M, Wachi M, Jung HK, Ishino F, Matsuhashi M. The Escherichia coli mraY gene encoding UDP-N-acetylmuramoyl-pentapeptide: undecaprenyl-phosphate phospho-N-acetylmuramoyl-pentapeptide transferase. J Bacteriol. 1991;173:1021-6.
52. Boyle DS, Donachie WD. mraY is an essential gene for cell growth in Escherichia coli. J Bacteriol. 1998;180:6429-32.
53. de Leeuw E, Graham B, Phillips GJ, ten Hagen-Jongman CM, Oudega B, Luirink J. Molecular characterization of Escherichia coli FtsE and FtsX. Mol Microbiol. 1999;31:983-93.
54. Ferrer-Miralles N, Villaverde A. Bacterial cell factories for recombinant protein production; expanding the catalogue. Microb Cell Fact. 2013;12:113.
55. Schaerlaekens K, Lammertyn E, Geukens N, De Keersmaeker S, Anne J, van Mellaert L. Comparison of the Sec and Tat secretion pathways for heterologous protein production by Streptomyces lividans. J Biotechnol. 2004;112:279-88.
56. van Wezel GP, McKenzie NL, Nodwell JR. Chapter 5. Applying the genetics of secondary metabolism in model actinomycetes to the discovery of new antibiotics. Methods Enzymol. 2009;458:117-41.
57. Martin SM, Bushell ME. Effect of hyphal micromorphology on bioreactor performance of antibiotic-producing Saccharopolyspora erythraea cultures. Microbiology. 1996;142:1783-8.
58. Baltz RH. Renaissance in antibacterial discovery from actinomycetes. Current Opin Pharmacol. 2008;8:557-63.
59. Piddock LJ. The crisis of no new antibiotics-what is the way forward? Lancet Infect Dis. 2011;12:249-53.
60. Zhu H, Sandiford SK, van Wezel GP. Triggers and cues that activate antibiotic production by actinomycetes. J Ind Microbiol Biotechnol. 2014;41:371-86.
61. Medema MH, Breitling R, Bovenberg R, Takano E. Exploiting plug-and-play synthetic biology for drug discovery and production in microorganisms. Nat Rev Microbiol. 2011;9:131-7.
62. Komatsu M, Uchiyama T, Omura S, Cane DE, Ikeda H. Genome-minimized Streptomyces host for the heterologous expression of secondary metabolism. Proc Natl Acad Sci U S A. 2010;107:2646-51.
63. Flinspach K, Westrich L, Kaysser L, Siebenberg S, Gomez-Escribano JP, Bibb M, et al. Heterologous expression of the biosynthetic gene clusters of coumermycin A(1), clorobiocin and caprazamycins in genetically modified Streptomyces coelicolor strains. Biopolymers. 2010;93:823-32.
64. Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: a laboratory manual. 2nd ed. Cold Spring harbor, N.Y.: Cold Spring Harbor laboratory press; 1989.
65. MacNeil DJ, Gewain KM, Ruby CL, Dezeny G, Gibbons PH, MacNeil T. Analysis of Streptomyces avermitilis genes required for avermectin biosynthesis utilizing a novel integration vector. Gene. 1992;111:61-8.
66. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA. Practical Streptomyces genetics. Norwich: The John Innes Foundation; 2000.
67. Keijser BJ, van Wezel GP, Canters GW, Kieser T, Vijgenboom E. The ram-dependence of Streptomyces lividans differentiation is bypassed by copper. J Mol Microbiol Biotechnol. 2000;2:565-74.
68. Swiatek MA, Tenconi E, Rigali S, van Wezel GP. Functional analysis of the N-acetylglucosamine metabolic genes of Streptomyces coelicolor and role in the control of development and antibiotic production. J Bacteriol. 2012;194:1136-44.
69. Colson S, Stephan J, Hertrich T, Saito A, van Wezel GP, Titgemeyer F, et al. Conserved cis-acting elements upstream of genes composing the chitinolytic system of streptomycetes are DasR-responsive elements. J Mol Microbiol Biotechnol. 2007;12:60-6.
70. Vara J, Lewandowska-Skarbek M, Wang YG, Donadio S, Hutchinson CR. Cloning of genes governing the deoxysugar portion of the erythromycin biosynthesis pathway in Saccharopolyspora erythraea (Streptomyces erythreus). J Bacteriol. 1989;171:5872-81.
71. Khodakaramian G, Lissenden S, Gust B, Moir L, Hoskisson PA, Chater KF, et al. Expression of Cre recombinase during transient phage infection permits efficient marker removal in Streptomyces. Nucleic Acids Res. 2006;34:e20.
72. Fedoryshyn M, Welle E, Bechthold A, Luzhetskyy A. Functional expression of the Cre recombinase in actinomycetes. Appl Microbiol Biotechnol. 2008;78:1065-70.
73. Bierman M, Logan R, O'Brien K, Seno ET, Rao RN, Schoner BE. Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene. 1992;116:43-9.
74. Colson S, van Wezel GP, Craig M, Noens EE, Nothaft H, Mommaas AM, et al. The chitobiose-binding protein, DasA, acts as a link between chitin utilization and morphogenesis in Streptomyces coelicolor. Microbiology. 2008;154:373-82.
75. Busarakam K, Bull AT, Girard G, Labeda DP, van Wezel GP, Goodfellow M. Streptomyces leeuwenhoekii sp. nov., the producer of chaxalactins and chaxamycins, forms a distinct branch in Streptomyces gene trees. Antonie Van Leeuwenhoek. 2014;105:849-61.
76. Girard G, Willemse J, Zhu H, Claessen D, Bukarasam K, Goodfellow M, et al. Analysis of novel kitasatosporae reveals significant evolutionary changes in conserved developmental genes between Kitasatospora and Streptomyces. Antonie Van Leeuwenhoek. 2014;106:365-80.