Transcriptional characterisation of the negative effect exerted by a deficiency in type II signal peptidase on extracellular protein secretion in Streptomyces lividans

Applied Microbiology and Biotechnology

Volumn 97, Issue 23, 2013, Pages 10069-10080

  Gullón, Sonia ^a   Arranz, Esther I G ^a   Mellado, Rafael P ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

Secretion stress response; Secretory protein production; Streptomyces lividans; Stringent response; Type II signal peptidase deficiency

Indexed keywords

PROTEIN PRODUCTION; SIGNAL PEPTIDASE; STREPTOMYCES LIVIDANS; STRESS RESPONSE; STRINGENT RESPONSE;

AMINO ACIDS; CELL ADHESION; CELL MEMBRANES; INDUSTRIAL APPLICATIONS;

LIPOPROTEINS;

CARRIER PROTEIN; SECRETORY PROTEIN; SIGNAL PEPTIDASE II;

ENZYME ACTIVITY; INDUSTRIAL PRODUCTION; MEMBRANE; PROTEIN; SECRETION; SIGNALING; VIRULENCE;

ARTICLE; BACTERIAL STRAIN; CELL METABOLISM; CONTROLLED STUDY; GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN CLEAVAGE; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SECRETORY PATHWAY; STREPTOMYCES LIVIDANS;

ASPARTIC ACID ENDOPEPTIDASES; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; LIPOPROTEINS; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; STREPTOMYCES LIVIDANS; TRANSCRIPTION, GENETIC;

EID: 84888175660     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-013-5219-9     Document Type: Article

References (47)

1. Anné J, Van Mellaert L (1993) Streptomyces lividans as host for heterologous protein production. FEMS Microbiol Lett 114:121-128
2. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc 57:289-300
3. Berks BC, Sargent F, De Leeuw E, Hinsley AP, Stanley NR, Jack RL, Buchanan G, Palmer T (2000) A novel protein transport system involved in the biogenesis of bacterial electron transfer chains. Biochim Biophys Acta 1459:325-330
4. Bernfeld P (1955) Amylases alpha and beta. In: Colowick SP, Kaplan ON (eds) Methods in enzymology. Academia Press, New Cork, pp 140-146
5. Bertram R, Schlicht M, Mahr K, Nothaft H, Saier MH Jr, Titgemeyer F (2004) In silico and transcriptional analysis of carbohydrate uptake systems of Streptomyces coelicolor A3(2). J Bacteriol 186:1362-1373
6. Binnie C, Cossar JD, Stewart DIH (1997) Heterologous biopharmaceutical protein expression in Streptomyces. Trends Biotechnol 15:315-320
7. Davidson AL, Dassa E, Orelle C, Chen J (2008) Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol Mol Biol Rev 72:317-364
8. Escutia MR, Val G, Palacín A, Geukens AJ, Mellado RP (2006) Compensatory effect of the minor Streptomyces lividans type I signal peptidases on the SipY major signal peptidase deficiency as determined by extracellular proteome analysis. Proteomics 6:4137-4146
9. Gilbert M, Morosoli R, Shareck F, Kluepfel D (1995) Production and secretion of proteins by Streptomycetes. Cri Rev Biotechnol 15:13-39
10. U activity in Streptomyces coelicolor. J Bacteriol 190:894-904
11. Gralnick JA, Vali H, Lies DP, Newman DK (2006) Extracellular respiration of dimethyl sulfoxide by Shewanella oneidensis strain MR-1. Proc Natl Acad Sci U S A 103:4669-4674
12. Gullón S, Palomino C, Navajas R, Paradela A, Mellado RP (2012a) Translocase and major signal peptidase malfunctions affect aerial mycelium formation in Streptomyces lividans. J Biotechnol 160:112-122
13. Gullón S, Vicente LR, Mellado RP (2012b) A novel two-component system involved in secretion stress response in Streptomyces lividans. PLoS One 7(11):e48987. doi: 10.1371/journal.pone.0048987
14. Gust B, Challis GL, Fowler K, Kieser T, Chater KF (2003) PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterne soil odor geosmin. Proc Natl Acad Sci U S A 100:1541-1546
15. Helmann JD (2002) The extracytoplasmic (ECF) sigma factors. Adv Microb Physiol 46:47-110
16. Hesketh A, Chen JW, 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:R161.1-R161.18
17. Hopwood DA, Bibb MJ, Chater KF (1985) Genetic manipulation of Streptomyces. A laboratory manual. John Innes Foundation, Norwich, UK
18. E cell envelope stress response of Streptomyces coelicolor is influenced by a novel lipoprotein, CseA. Mol Microbiol 188:7222-7229
19. Hutchings MI, Palmer T, Harrington DJ, Sutcliffe IC (2009) Lipoprotein biogenesis in Gram-positive bacteria: knowing when to hold 'em, knowing when to fold 'em. Trends Microbiol 17:13-21
20. Kieser T, Bibb MJ, Chater KF, Hopwood DA (2000) Practical Streptomyces genetics. John Innes Foundation, Norwich, UK
21. Kontinen VP, Sarvas M (1993) The PsrA lipoprotein is essential for protein secretion in Bacillus subtilis and sets a limit for high-level secretion. Mol Microbiol 8:727-737
22. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685
23. Lammertyn E, Van Mellaert L, Schacht S, Dillen C, Sablon A, Van Broekhoven A, Anné J (1997) Evaluation of a novel subtilisin inhibitor gene and mutant derivatives for the expression and secretion of mouse tumor necrosis factor alpha by Streptomyces lividans. Appl Environ Microbiol 63:1808-1813
24. MacNeil DJ, Gewain KM, Ruby CL, Dezeny G, Gibbons PH, MacNeil T (1992) Analysis of Streptomyces avermitilis genes required for avermectin biosynthesis utilizing a novel integration vector. Gene 111:61-68
25. Martinez-Costa OH, Arias P, Romero NM, Parro V, Mellado RP, Malpartida F (1996) A relA/spoT homologous gene from Streptomyces coelicolor A3(2) controls antibiotic biosynthtic genes. J Biol Chem 271:10627-10634
26. Pahl A, Keller U (1994) Streptomyces chrysomallus FKBP-33 is a novel immunophilin consisting of two FK506 binding domains; its gene is transcriptionally coupled to the FKBP-12 gene. EMBO J 13:3472-3480
27. Palacín A, de la Fuente R, Valle I, Rivas LA and Mellado RP (2003) Streptomyces lividans contains a minimal functional signal recognition particle that is involved in protein secretion. Microbiology 149: 2435-2442
28. Palomino C, Mellado RP (2008) Influence of a Streptomyces lividans SecG functional analogue on protein secretion. Int Microbiol 11:25-31
29. Parro V, Mellado RP (1994) Effect of glucose on agarase overproduction by Streptomyces. Gene 145:49-55
30. Rabindran SK, Haroun RI, Wisniewski J, Wu C (1993) Regulation of heat shock factor trimer formation: role of a conserved leucine zipper. Science 259:230-234
31. Redenbach M, Kieser HM, Denapaite D, Eichner A, Cullum J, Kinashi H, Hopwood DA (1996) A set of ordered cosmids and a detailed genetic and physical map for the 8 Mb Streptomyces coelicolor A3(2) chromosome. Mol Microbiol 21:77-96
32. Robichon C, Vidal-Ingigliardi D, Pugsley AP (2005) Depletion of apolipoprotein N-acyltransferase causes mislocalization of outer membrane lipoproteins in Escherichia coli. J Biol Chem 280:974-983
33. Rozas D, Gullón S, Mellado RP (2012) A novel two-component system involved in the transition to secondary metabolism in Streptomyces coelicolor. PLoS ONE 7(2):e31760. doi: 10.1371/journal.pone.0031760
34. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
35. T method. Nature protocols 3:1101-1108
36. Smyth GK (2004). Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article 3. Available from http://www.bepress.com/sagm/vol3/iss1/art3
37. Smyth GK, Speed T (2003) Normalization of cDNA microarray data. Methods 31:265-273
38. Strumeyer DH (1967) A modified starch for use in amylase assays. Anal Biochem 19:61-71
39. Sun J, Hesketh A, Bibb MJ (2001) Functional analysis of relA and rshA, two relA/spoT homologues of Streptomyces coelicolor A3(2). J Bacteriol 183:3488-3498
40. Thompson CJ, Kieser T, Ward JM, Hopwood DA (1982) Physical analysis of antibiotic-resistant genes from Streptomyces and their use in vector construction. Gene 20:51-62
41. Thompson BJ, Widdick DA, Hicks MG, Chandra G, Sutcliffe IC, Palmer T, Hutchings MI (2010) Investigating lipoprotein biogenesis and function in the model Gram-positive bacterium Streptomyces coelicolor. Mol Microbiol 77:943-957
42. Timmons TM, Dunbar BS (1990) Protein blotting and immunodetection. Methods Enzymol 182:679-688
43. Tokuda H (2009) Biogenesis of outer membranes in Gram-negative bacteria. Biosci Biotechnol Biochem 73:465-473
44. Valente FM, Pereira PM, Venceslau SS, Regalla M, Coelho AV, Pereira IA (2007) The [NiFeSe] hydrogenase from Desulfovibrio vulgaris Hildenborough is a bacterial lipoprotein lacking a typical lipoprotein signal peptide. FEBS Lett 581:3341-3344
45. Van Mellaert L, Anné J (1994) Protein secretion in Gram-positive bacteria with high GC-content. Recent Res Dev Microbiol 3:324-340
46. Vitikainen M, Lappalainen I, Seppala R, Antelmann H, Boer H, Taira S, Savilahti H, Hecker M, Vihinen M, Sarvas M, Kontinen VP (2004) Structure-function analysis of PrsA reveals roles for the parvulin-like and flanking N- and C-terminal domains in protein folding and secretion in Bacillus subtilis. J Biol Chem 279:19302-19314
47. Widdick DA, Hicks MG, Thompson BJ, Tschumi A, Chandra G, Sutcliffe IC, Bruelle JK, Sander P, Palmer T, Hutchings MI (2011) Dissecting the complete lipoprotein biogenesis pathway in Streptomyces scabies. Mol Microbiol 80:1395-1412