Generic placeholder image

Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Research Article

Proteomic analysis of a hom-disrupted, cephamycin C overproducing Streptomyces clavuligerus

Author(s): Eser Ünsaldı, Aslıhan Kurt-Kızıldoğan, Servet Özcan, Dörte Becher, Birgit Voigt, Caner Aktaş and Gülay Özcengiz*

Volume 28, Issue 2, 2021

Published on: 23 July, 2020

Page: [205 - 220] Pages: 16

DOI: 10.2174/0929866527666200723163655

Price: $65

Open Access Journals Promotions 2
Abstract

Background: Streptomyces clavuligerus is prolific producer of cephamycin C, a medically important antibiotic. In our former study, cephamycin C titer was 2-fold improved by disrupting homoserine dehydrogenase (hom) gene of aspartate pahway in Streptomyces clavuligerus NRRL 3585.

Objective: In this article, we aimed to provide a comprehensive understanding at the proteome level on potential complex metabolic changes as a consequence of hom disruption in Streptomyces clavuligerus AK39.

Methods: A comparative proteomics study was carried out between the wild type and its hom disrupted AK39 strain by 2 Dimensional Electrophoresis-Matrix Assisted Laser Desorption and Ionization Time-Of-Flight Mass Spectrometry (2DE MALDI-TOF/MS) and Nanoscale Liquid Chromatography- Tandem Mass Spectrometry (nanoLC-MS/MS) analyses. Clusters of Orthologous Groups (COG) database was used to determine the functional categories of the proteins. The theoretical pI and Mw values of the proteins were calculated using Expasy pI/Mw tool.

Results: “Hypothetical/Unknown” and “Secondary Metabolism” were the most prominent categories of the differentially expressed proteins. Upto 8.7-fold increased level of the positive regulator CcaR was a key finding since CcaR was shown to bind to cefF promoter thereby direcly controlling its expression. Consistently, CeaS2, the first enzyme of CA biosynthetic pathway, was 3.3- fold elevated. There were also many underrepresented proteins associated with the biosynthesis of several Non-Ribosomal Peptide Synthases (NRPSs), clavams, hybrid NRPS/Polyketide synthases (PKSs) and tunicamycin. The most conspicuously underrepresented protein of amino acid metabolism was 4-Hydroxyphenylpyruvate dioxygenase (HppD) acting in tyrosine catabolism. The levels of a Two Component System (TCS) response regulator containing a CheY-like receiver domain and an HTH DNA-binding domain as well as DNA-binding protein HU were elevated while a TetR-family transcriptional regulator was underexpressed.

Conclusion: The results obtained herein will aid in finding out new targets for further improvement of cephamycin C production in Streptomyces clavuligerus.

Keywords: Cephamycin C, Streptomyces clavuligerus, hom-disruption, proteomics, MALDI-TOF/MS, nanoLC-MS/MS.

Graphical Abstract
[1]
Nett, M.; Ikeda, H.; Moore, B.S. Genomic basis for natural product biosynthetic diversity in the actinomycetes. Nat. Prod. Rep., 2009, 26(11), 1362-1384.
[http://dx.doi.org/10.1039/b817069j] [PMID: 19844637]
[2]
Medema, M.H.; Trefzer, A.; Kovalchuk, A.; van den Berg, M.; Müller, U.; Heijne, W.; Wu, L.; Alam, M.T.; Ronning, C.M.; Nierman, W.C.; Bovenberg, R.A.; Breitling, R.; Takano, E. The sequence of a 1.8-mb bacterial linear plasmid reveals a rich evolutionary reservoir of secondary metabolic pathways. Genome Biol. Evol., 2010, 2, 212-224.
[http://dx.doi.org/10.1093/gbe/evq013] [PMID: 20624727]
[3]
Song, J.Y.; Jeong, H.; Yu, D.S.; Fischbach, M.A.; Park, H.S.; Kim, J.J.; Seo, J.S.; Jensen, S.E.; Oh, T.K.; Lee, K.J.; Kim, J.F. Draft genome sequence of Streptomyces clavuligerus NRRL 3585, a producer of diverse secondary metabolites. J. Bacteriol., 2010, 192(23), 6317-6318.
[http://dx.doi.org/10.1128/JB.00859-10] [PMID: 20889745]
[4]
Liras, P.; Gomez-Escribano, J.P.; Santamarta, I. Regulatory mechanisms controlling antibiotic production in Streptomyces clavuligerus. J. Ind. Microbiol. Biotechnol., 2008, 35(7), 667-676.
[http://dx.doi.org/10.1007/s10295-008-0351-8] [PMID: 18446393]
[5]
Özcengiz, G.; Demain, A.L. Recent advances in the biosynthesis of penicillins, cephalosporins and clavams and its regulation. Biotechnol. Adv., 2013, 31(2), 287-311.
[http://dx.doi.org/10.1016/j.biotechadv.2012.12.001] [PMID: 23228980]
[6]
Kenig, M.; Reading, C. Holomycin and an antibiotic (MM 19290) related to tunicamycin, metabolites of Streptomyces clavuligerus. J. Antibiot. (Tokyo), 1979, 32(6), 549-554.
[http://dx.doi.org/10.7164/antibiotics.32.549] [PMID: 468729]
[7]
Bussari, B.; Saudagar, P.S.; Shaligram, N.S.; Survase, S.A.; Singhal, R.S. Production of cephamycin C by Streptomyces clavuligerus NT4 using solid-state fermentation. J. Ind. Microbiol. Biotechnol., 2008, 35(1), 49-58.
[http://dx.doi.org/10.1007/s10295-007-0265-x] [PMID: 17940818]
[8]
Saudagar, P.S.; Survase, S.A.; Singhal, R.S. Clavulanic acid: a review. Biotechnol. Adv., 2008, 26(4), 335-351.
[http://dx.doi.org/10.1016/j.biotechadv.2008.03.002] [PMID: 18450406]
[9]
Ward, J.M.; Hodgson, J.E. The biosynthetic genes for clavulanic acid and cephamycin production occur as a ‘super-cluster’ in three Streptomyces. FEMS Microbiol. Lett., 1993, 110(2), 239-242.
[http://dx.doi.org/10.1111/j.1574-6968.1993.tb06326.x] [PMID: 8349096]
[10]
Liras, P.; Martín, J.F. Gene clusters for beta-lactam antibiotics and control of their expression: why have clusters evolved, and from where did they originate? Int. Microbiol., 2006, 9(1), 9-19.
[PMID: 16636985]
[11]
Tunca, S.; Yilmaz, E.I.; Piret, J.; Liras, P.; Özcengiz, G. Cloning, characterization and heterologous expression of the aspartokinase and aspartate semialdehyde dehydrogenase genes of cephamycin C-producer Streptomyces clavuligerus. Res. Microbiol., 2004, 155(7), 525-534.
[http://dx.doi.org/10.1016/j.resmic.2004.03.007] [PMID: 15313252]
[12]
Paradkar, A.S.; Mosher, R.H.; Anders, C.; Griffin, A.; Griffin, J.; Hughes, C.; Greaves, P.; Barton, B.; Jensen, S.E. Applications of gene replacement technology to Streptomyces clavuligerus strain development for clavulanic acid production. Appl. Environ. Microbiol., 2001, 67(5), 2292-2297.
[http://dx.doi.org/10.1128/AEM.67.5.2292-2297.2001] [PMID: 11319114]
[13]
Pérez-Llarena, F.J.; Liras, P.; Rodríguez-García, A.; Martín, J.F. A regulatory gene (ccaR) required for cephamycin and clavulanic acid production in Streptomyces clavuligerus: amplification results in overproduction of both β-lactam compounds. J. Bacteriol., 1997, 179(6), 2053-2059.
[http://dx.doi.org/10.1128/JB.179.6.2053-2059.1997] [PMID: 9068654]
[14]
Martínez-Burgo, Y.; Álvarez-Álvarez, R.; Rodríguez-García, A.; Liras, P. The pathway-specific regulator ClaR of Streptomyces clavuligerus has a global effect on the expression of genes for secondary metabolism and differentiation. Appl. Environ. Microbiol., 2015, 81(19), 6637-6648.
[http://dx.doi.org/10.1128/AEM.00916-15] [PMID: 26187955]
[15]
López-García, M.T.; Santamarta, I.; Liras, P. Morphological differentiation and clavulanic acid formation are affected in a Streptomyces clavuligerus adpA-deleted mutant. Microbiology, 2010, 156(Pt 8), 2354-2365.
[http://dx.doi.org/10.1099/mic.0.035956-0] [PMID: 20447998]
[16]
Gomez-Escribano, J.P.; Martín, J.F.; Hesketh, A.; Bibb, M.J.; Liras, P. Streptomyces clavuligerus relA-null mutants overproduce clavulanic acid and cephamycin C: negative regulation of secondary metabolism by (p)ppGpp. Microbiology, 2008, 154(Pt 3), 744-755.
[http://dx.doi.org/10.1099/mic.0.2007/011890-0] [PMID: 18310021]
[17]
Yilmaz, E.I.; Çaydasi, A.K.; Özcengiz, G. Targeted disruption of homoserine dehydrogenase gene and its effect on cephamycin C production in Streptomyces clavuligerus. J. Ind. Microbiol. Biotechnol., 2008, 35(1), 1-7.
[http://dx.doi.org/10.1007/s10295-007-0259-8] [PMID: 17909870]
[18]
Özcengiz, G.; Okay, S.; Ünsaldı, E.; Taşkın, B.; Liras, P.; Piret, J. Homologous expression of aspartokinase (ask) gene in Streptomyces clavuligerus and its hom-deleted mutant: effects on cephamycin C production. Bioeng. Bugs, 2010, 1(3), 191-197.
[http://dx.doi.org/10.4161/bbug.1.3.11244] [PMID: 21326925]
[19]
Martínez-Burgo, Y.; Álvarez-Álvarez, R.; Pérez-Redondo, R.; Liras, P. Heterologous expression of Streptomyces clavuligerus ATCC 27064 cephamycin C gene cluster. J. Biotechnol., 2014, 186, 21-29.
[http://dx.doi.org/10.1016/j.jbiotec.2014.06.002] [PMID: 24975573]
[20]
Fernández, M.; Cuadrado, Y.; Recio, E.; Aparicio, J.F.; Martı N, J.F. Characterization of the hom-thrC-thrB cluster in aminoethoxyvinylglycine-producing Streptomyces sp. NRRL 5331. Microbiology, 2002, 148(Pt 5), 1413-1420.
[http://dx.doi.org/10.1099/00221287-148-5-1413] [PMID: 11988515]
[21]
Chaudhary, A.K.; Dhakal, D.; Sohng, J.K. An insight into the "-omics" based engineering of streptomycetes for secondary metabolite overproduction. BioMed Res. Int., 2013, 2013, 968518.
[http://dx.doi.org/10.1155/2013/968518] [PMID: 24078931]
[22]
Ferguson, N.L.; Peña-Castillo, L.; Moore, M.A.; Bignell, D.R.D.; Tahlan, K. Proteomics analysis of global regulatory cascades involved in clavulanic acid production and morphological development in Streptomyces clavuligerus. J. Ind. Microbiol. Biotechnol., 2016, 43(4), 537-555.
[http://dx.doi.org/10.1007/s10295-016-1733-y] [PMID: 26790415]
[23]
Ünsaldı, E.; Kurt-Kızıldoğan, A.; Voigt, B.; Becher, D.; Özcengiz, G. Proteome-wide alterations in an industrial clavulanic acid producing strain of Streptomyces clavuligerus. Synth Syst Biotechnol, 2016, 2(1), 39-48.
[http://dx.doi.org/10.1016/j.synbio.2016.10.003] [PMID: 29062960]
[24]
Faurobert, M.; Pelpoir, E.; Chaïb, J. Phenol extraction of proteins for proteomic studies of recalcitrant plant tissues. Methods Mol. Biol., 2007, 355, 9-14.
[PMID: 17093297]
[25]
Yin, P.; Wang, Y.H.; Zhang, S.L.; Chu, J.; Zhuang, Y.P.; Wang, M.L.; Zhou, J. Isolation of soluble proteins from an industrial strain Streptomyces avermitilis in complex culture medium for two-dimensional gel electrophoresis. J. Microbiol. Methods, 2008, 73(2), 105-110.
[http://dx.doi.org/10.1016/j.mimet.2008.02.012] [PMID: 18378344]
[26]
Ramagli, L.S.; Rodriguez, L.V. Quantitation of microgram amounts of protein in two-dimensional polyacrylamide gel electrophoresis sample buffer. Electrophoresis, 1985, 6(11), 559-563.
[http://dx.doi.org/10.1002/elps.1150061109]
[27]
Neuhoff, V.; Arold, N.; Taube, D.; Ehrhardt, W. Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis, 1988, 9(6), 255-262.
[http://dx.doi.org/10.1002/elps.1150090603] [PMID: 2466658]
[28]
Wiśniewski, J.R.; Zougman, A.; Nagaraj, N.; Mann, M. Universal sample preparation method for proteome analysis. Nat. Methods, 2009, 6(5), 359-362.
[http://dx.doi.org/10.1038/nmeth.1322] [PMID: 19377485]
[29]
Old, W.M.; Meyer-Arendt, K.; Aveline-Wolf, L.; Pierce, K.G.; Mendoza, A.; Sevinsky, J.R.; Resing, K.A.; Ahn, N.G. Comparison of label-free methods for quantifying human proteins by shotgun proteomics. Mol. Cell. Proteomics, 2005, 4(10), 1487-1502.
[http://dx.doi.org/10.1074/mcp.M500084-MCP200] [PMID: 15979981]
[30]
Gasteiger, E.; Gattiker, A.; Hoogland, C.; Ivanyi, I.; Appel, R.D.; Bairoch, A. ExPASy: The proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res., 2003, 31(13), 3784-3788.
[http://dx.doi.org/10.1093/nar/gkg563] [PMID: 12824418]
[31]
Aigle, B.; Wietzorrek, A.; Takano, E.; Bibb, M.J. A single amino acid substitution in region 1.2 of the principal sigma factor of Streptomyces coelicolor A3(2) results in pleiotropic loss of antibiotic production. Mol. Microbiol., 2000, 37(5), 995-1004.
[http://dx.doi.org/10.1046/j.1365-2958.2000.02022.x] [PMID: 10972819]
[32]
Pfaffl, M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res., 2001, 29(9), e45.
[http://dx.doi.org/10.1093/nar/29.9.e45] [PMID: 11328886]
[33]
Pérez-Redondo, R.; Santamarta, I.; Bovenberg, R.; Martín, J.F.; Liras, P. The enigmatic lack of glucose utilization in Streptomyces clavuligerus is due to inefficient expression of the glucose permease gene. Microbiology, 2010, 156(Pt 5), 1527-1537.
[http://dx.doi.org/10.1099/mic.0.035840-0] [PMID: 20110297]
[34]
Chen, W.; Qu, D.; Zhai, L.; Tao, M.; Wang, Y.; Lin, S.; Price, N.P.; Deng, Z. Characterization of the tunicamycin gene cluster unveiling unique steps involved in its biosynthesis. Protein Cell, 2010, 1(12), 1093-1105.
[http://dx.doi.org/10.1007/s13238-010-0127-6] [PMID: 21153459]
[35]
Wyszynski, F.J.; Lee, S.S.; Yabe, T.; Wang, H.; Gomez-Escribano, J.P.; Bibb, M.J.; Lee, S.J.; Davies, G.J.; Davis, B.G. Biosynthesis of the tunicamycin antibiotics proceeds via unique exo-glycal intermediates. Nat. Chem., 2012, 4(7), 539-546.
[http://dx.doi.org/10.1038/nchem.1351] [PMID: 22717438]
[36]
Yin, H.; Xiang, S.; Zheng, J.; Fan, K.; Yu, T.; Yang, X.; Peng, Y.; Wang, H.; Feng, D.; Luo, Y.; Bai, H.; Yang, K. Induction of holomycin production and complex metabolic changes by the argR mutation in Streptomyces clavuligerus NP1. Appl. Environ. Microbiol., 2012, 78(9), 3431-3441.
[http://dx.doi.org/10.1128/AEM.07699-11] [PMID: 22344669]
[37]
Novotna, J.; Vohradsky, J.; Berndt, P.; Gramajo, H.; Langen, H.; Li, X.M.; Minas, W.; Orsaria, L.; Roeder, D.; Thompson, C.J. Proteomic studies of diauxic lag in the differentiating prokaryote Streptomyces coelicolor reveal a regulatory network of stress-induced proteins and central metabolic enzymes. Mol. Microbiol., 2003, 48(5), 1289-1303.
[http://dx.doi.org/10.1046/j.1365-2958.2003.03529.x] [PMID: 12787356]
[38]
Bender, RA Regulation of the Histidine Utilization (Hut) system in bacteria. Microbiol. Mol. Biol. Rev., 2012, 76(3), 565-584.
[http://dx.doi.org/10.1128/MMBR.00014-12]
[39]
Rigali, S.; Titgemeyer, F.; Barends, S.; Mulder, S.; Thomae, A.W.; Hopwood, D.A.; van Wezel, G.P. Feast or famine: the global regulator DasR links nutrient stress to antibiotic production by Streptomyces. EMBO Rep., 2008, 9(7), 670-675.
[http://dx.doi.org/10.1038/embor.2008.83] [PMID: 18511939]
[40]
Moran, G.R. 4-Hydroxyphenylpyruvate dioxygenase. Arch. Biochem. Biophys., 2005, 433(1), 117-128.
[http://dx.doi.org/10.1016/j.abb.2004.08.015] [PMID: 15581571]
[41]
Denoya, C.D.; Fedechko, R.W.; Hafner, E.W.; McArthur, H.A.; Morgenstern, M.R.; Skinner, D.D.; Stutzman-Engwall, K.; Wax, R.G.; Wernau, W.C. A second branched-chain alpha-keto acid dehydrogenase gene cluster (bkdFGH) from Streptomyces avermitilis: its relationship to avermectin biosynthesis and the construction of a bkdF mutant suitable for the production of novel antiparasitic avermectins. J. Bacteriol., 1995, 177(12), 3504-3511.
[http://dx.doi.org/10.1128/JB.177.12.3504-3511.1995] [PMID: 7768860]
[42]
Yang, H.; Wang, L.; Xie, Z.; Tian, Y.; Liu, G.; Tan, H. The tyrosine degradation gene hppD is transcriptionally activated by HpdA and repressed by HpdR in Streptomyces coelicolor, while hpdA is negatively autoregulated and repressed by HpdR. Mol. Microbiol., 2007, 65(4), 1064-1077.
[http://dx.doi.org/10.1111/j.1365-2958.2007.05848.x] [PMID: 17640269]
[43]
Petrícek, M.; Petrícková, K.; Havlícek, L.; Felsberg, J. Occurrence of two 5-aminolevulinate biosynthetic pathways in Streptomyces nodosus subsp. asukaensis is linked with the production of asukamycin. J. Bacteriol., 2006, 188(14), 5113-5123.
[http://dx.doi.org/10.1128/JB.01919-05] [PMID: 16816183]
[44]
Garrido-Peritierra, A.; Cooper, R.A. Identification and purification of distinct isomerase and decarboxylase enzymes involved in the 4-hydroxyphenylacetate catabolic pathway of Escherichia coli. Eur. J. Biochem., 1981, 117(3), 581-584.
[http://dx.doi.org/10.1111/j.1432-1033.1981.tb06377.x] [PMID: 7026235]
[45]
Vaijayanthi, G.; Vijayakumar, R.; Dhanasekaran, D. Actinobacteria — A Biofactory of Novel Enzymes. Actinobacteria - Basics and Biotechnological Applications., 2016, , 329-352.
[http://dx.doi.org/10.5772/61436]
[46]
Trivedi, V.; Gupta, A; Jala, VR; Saravanan, P; Rao, GJ; Rao, NA. Crystal structure of binary and ternary complexes of serine hydroxymethyltransferase from Bacillus stearothermophilus: insights into the catalytic mechanism. J Bioll Chem, 2002, 277(19), 17161-17169..
[http://dx.doi.org/10.1074/jbc.M111976200]
[47]
Zelyas, N.J.; Cai, H.; Kwong, T.; Jensen, S.E. Alanylclavam biosynthetic genes are clustered together with one group of clavulanic acid biosynthetic genes in Streptomyces clavuligerus. J. Bacteriol., 2008, 190(24), 7957-7965.
[http://dx.doi.org/10.1128/JB.00698-08] [PMID: 18931110]
[48]
Alvarez-Álvarez, R.; Rodríguez-García, A.; Santamarta, I.; Pérez-Redondo, R.; Prieto-Domínguez, A.; Martínez-Burgo, Y.; Liras, P. Transcriptomic analysis of Streptomyces clavuligerus ΔccaR:tsr: effects of the cephamycin C-clavulanic acid cluster regulator CcaR on global regulation. Microb. Biotechnol., 2014, 7(3), 221-231.
[http://dx.doi.org/10.1111/1751-7915.12109] [PMID: 24450885]
[49]
Gago, G.; Diacovich, L.; Arabolaza, A.; Tsai, S.C.; Gramajo, H. Fatty acid biosynthesis in actinomycetes. FEMS Microbiol. Rev., 2011, 35(3), 475-497.
[http://dx.doi.org/10.1111/j.1574-6976.2010.00259.x] [PMID: 21204864]
[50]
Zhang, Y.M.; Lu, Y.J.; Rock, C.O. The reductase steps of the type II fatty acid synthase as antimicrobial targets. Lipids, 2004, 39(11), 1055-1060.
[http://dx.doi.org/10.1007/s11745-004-1330-3] [PMID: 15726819]
[51]
Rodríguez, E.; Banchio, C.; Diacovich, L.; Bibb, M.J.; Gramajo, H. Role of an essential acyl coenzyme A carboxylase in the primary and secondary metabolism of Streptomyces coelicolor A3(2). Appl. Environ. Microbiol., 2001, 67(9), 4166-4176.
[http://dx.doi.org/10.1128/AEM.67.9.4166-4176.2001] [PMID: 11526020]
[52]
Park, S.J.; Lee, S.Y. Identification and characterization of a new enoyl coenzyme A hydratase involved in biosynthesis of medium-chain-length polyhydroxyalkanoates in recombinant Escherichia coli. J. Bacteriol., 2003, 185(18), 5391-5397.
[http://dx.doi.org/10.1128/JB.185.18.5391-5397.2003] [PMID: 12949091]
[53]
Ghisla, S.; Thorpe, C. Acyl-CoA dehydrogenases. A mechanistic overview. Eur. J. Biochem., 2004, 271(3), 494-508.
[http://dx.doi.org/10.1046/j.1432-1033.2003.03946.x] [PMID: 14728676]
[54]
Zhang, Y.X.; Denoya, C.D.; Skinner, D.D.; Fedechko, R.W.; McArthur, H.A.I.; Morgenstern, M.R.; Davies, R.A.; Lobo, S.; Reynolds, K.A.; Hutchinson, C.R. Genes encoding acyl-CoA dehydrogenase (AcdH) homologues from Streptomyces coelicolor and Streptomyces avermitilis provide insights into the metabolism of small branched-chain fatty acids and macrolide antibiotic production. Microbiology, 1999, 145(Pt 9), 2323-2334.
[http://dx.doi.org/10.1099/00221287-145-9-2323] [PMID: 10517585]
[55]
Ashmarina, L.I.; Rusnak, N.; Miziorko, H.M.; Mitchell, G.A. 3-Hydroxy-3-methylglutaryl-CoA lyase is present in mouse and human liver peroxisomes. J. Biol. Chem., 1994, 269(50), 31929-31932.
[PMID: 7527399]
[56]
Walton, L.J.; Corre, C.; Challis, G.L. Mechanisms for incorporation of glycerol-derived precursors into polyketide metabolites. J. Ind. Microbiol. Biotechnol., 2006, 33(2), 105-120.
[http://dx.doi.org/10.1007/s10295-005-0026-7] [PMID: 16187096]
[57]
Jost, M.; Born, D.A.; Cracan, V.; Banerjee, R.; Drennan, C.L. Structural basis for substrate specificity in adenosylcobalamin-dependent isobutyryl-CoA mutase and related Acyl-CoA mutases. J. Biol. Chem., 2015, 290(45), 26882-26898.
[http://dx.doi.org/10.1074/jbc.M115.676890] [PMID: 26318610]
[58]
Salie, M.J.; Thelen, J.J. Regulation and structure of the heteromeric acetyl-CoA carboxylase. Biochim. Biophys. Acta, 2016, 1861(9 Pt B), 1207-1213.
[http://dx.doi.org/10.1016/j.bbalip.2016.04.004] [PMID: 27091637]
[59]
Santamarta, I.; López-García, M.T.; Kurt, A.; Nárdiz, N.; Alvarez-Álvarez, R.; Pérez-Redondo, R.; Martín, J.F.; Liras, P. Characterization of DNA-binding sequences for CcaR in the cephamycin-clavulanic acid supercluster of Streptomyces clavuligerus. Mol. Microbiol., 2011, 81(4), 968-981.
[http://dx.doi.org/10.1111/j.1365-2958.2011.07743.x] [PMID: 21696462]
[60]
Komeda, H.; Asano, Y. Gene cloning, nucleotide sequencing, and purification and characterization of the D-stereospecific amino-acid amidase from Ochrobactrum anthropi SV3. Eur. J. Biochem., 2000, 267(7), 2028-2035.
[http://dx.doi.org/10.1046/j.1432-1327.2000.01208.x] [PMID: 10727942]
[61]
Nakano, S.; Okazaki, S.; Ishitsubo, E.; Kawahara, N.; Komeda, H.; Tokiwa, H.; Asano, Y. Structural and computational analysis of peptide recognition mechanism of class-C type penicillin binding protein, alkaline D-peptidase from Bacillus cereus DF4-B. Sci. Rep., 2015, 5, 13836.
[http://dx.doi.org/10.1038/srep13836] [PMID: 26370172]
[62]
Jensen, S.E. Biosynthesis of clavam metabolites. J. Ind. Microbiol. Biotechnol., 2012, 39(10), 1407-1419.
[http://dx.doi.org/10.1007/s10295-012-1191-0] [PMID: 22948564]
[63]
AbuSara, N.F.; Brandon, M.; Piercey, B.M. Comparative genomics and metabolomics analyses of clavulanic acid-producing Streptomyces species provides insight into specialized metabolism. Microbiol., 2019, 10, 2550.
[http://dx.doi.org/10.3389/fmicb.2019.02550.]
[64]
Lallemand, P.; Leban, N.; Kunzelmann, S.; Chaloin, L.; Serpersu, E.H.; Webb, M.R.; Barman, T.; Lionne, C. Transient kinetics of aminoglycoside phosphotransferase(3′)-IIIa reveals a potential drug target in the antibiotic resistance mechanism. FEBS Lett., 2012, 586(23), 4223-4227.
[http://dx.doi.org/10.1016/j.febslet.2012.10.027] [PMID: 23108046]
[65]
Medema, M.H.; Alam, M.T.; Heijne, W.H.; van den Berg, M.A.; Müller, U.; Trefzer, A.; Bovenberg, R.A.; Breitling, R.; Takano, E. Genome-wide gene expression changes in an industrial clavulanic acid overproduction strain of Streptomyces clavuligerus. Microb. Biotechnol., 2011, 4(2), 300-305.
[http://dx.doi.org/10.1111/j.1751-7915.2010.00226.x] [PMID: 21342474]
[66]
Chen, L.; Helmann, J.D. Bacillus subtilis MrgA is a Dps(PexB) homologue: evidence for metalloregulation of an oxidative-stress gene. Mol. Microbiol., 1995, 18(2), 295-300.
[http://dx.doi.org/10.1111/j.1365-2958.1995.mmi_18020295.x] [PMID: 8709848]
[67]
De Mot, R.; Schoofs, G.; Nagy, I. Proteome analysis of Streptomyces coelicolor mutants affected in the proteasome system reveals changes in stress-responsive proteins. Arch. Microbiol., 2007, 188(3), 257-271.
[http://dx.doi.org/10.1007/s00203-007-0243-8] [PMID: 17486317]
[68]
Darwin, K.H.; Ehrt, S.; Gutierrez-Ramos, J.C.; Weich, N.; Nathan, C.F. The proteasome of Mycobacterium tuberculosis is required for resistance to nitric oxide. Science, 2003, 302(5652), 1963-1966.
[http://dx.doi.org/10.1126/science.1091176] [PMID: 14671303]
[69]
Hong, B.; Wang, L.; Lammertyn, E.; Geukens, N.; Van Mellaert, L.; Li, Y.; Anné, J. Inactivation of the 20S proteasome in Streptomyces lividans and its influence on the production of heterologous proteins. Microbiology, 2005, 151(Pt 9), 3137-3145.
[http://dx.doi.org/10.1099/mic.0.28034-0] [PMID: 16151224]
[70]
Höppner, A.; Widderich, N.; Lenders, M.; Bremer, E.; Smits, S.H.J. Crystal structure of the ectoine hydroxylase, a snapshot of the active site. J. Biol. Chem., 2014, 289(43), 29570-29583.
[http://dx.doi.org/10.1074/jbc.M114.576769] [PMID: 25172507]
[71]
Bobek, J.; Halada, P.; Angelis, J.; Vohradský, J.; Mikulík, K. Activation and expression of proteins during synchronous germination of aerial spores of Streptomyces granaticolor. Proteomics, 2004, 4(12), 3864-3880.
[http://dx.doi.org/10.1002/pmic.200400818] [PMID: 15378695]
[72]
Martín, J.F.; Liras, P. Engineering of regulatory cascades and networks controlling antibiotic biosynthesis in Streptomyces. Curr. Opin. Microbiol., 2010, 13(3), 263-273.
[http://dx.doi.org/10.1016/j.mib.2010.02.008] [PMID: 20303823]
[73]
Orozco, H.; Matallana, E.; Aranda, A. Genetic manipulation of longevity-related genes as a tool to regulate yeast life span and metabolite production during winemaking. Microb. Cell Fact., 2013, 12(1), 1.
[http://dx.doi.org/10.1186/1475-2859-12-1] [PMID: 23282100]
[74]
Jnawali, H.N.; Oh, T.J.; Liou, K.; Park, B.C.; Sohng, J.K. A two-component regulatory system involved in clavulanic acid production. J. Antibiot. (Tokyo), 2008, 61(11), 651-659.
[http://dx.doi.org/10.1038/ja.2008.92] [PMID: 19168979]
[75]
Fu, J.; Qin, R.; Zong, G.; Liu, C.; Kang, N.; Zhong, C.; Cao, G. The CagRS two-component system regulates clavulanic acid metabolism via multiple pathways in Streptomyces clavuligerus F613-1. Front. Microbiol., 2019, 10, 244.
[http://dx.doi.org/10.3389/fmicb.2019.00244] [PMID: 30837970]
[76]
Fu, J.; Qin, R.; Zong, G.; Zhong, C.; Zhang, P.; Kang, N.; Qi, X.; Cao, G. The two-component system CepRS regulates the cephamycin C biosynthesis in Streptomyces clavuligerus F613-1. AMB Express, 2019, 9(1), 118.
[http://dx.doi.org/10.1186/s13568-019-0844-z] [PMID: 31352530]
[77]
Grove, A. Functional evolution of bacterial histone-like HU proteins. Curr. Issues Mol. Biol., 2011, 13(1), 1-12.
[PMID: 20484776]
[78]
Vierling, S.; Weber, T.; Wohlleben, W.; Muth, G. Evidence that an additional mutation is required to tolerate insertional inactivation of the Streptomyces lividans recA gene. J. Bacteriol., 2001, 183(14), 4374-4381.
[http://dx.doi.org/10.1128/JB.183.14.4374-4381.2001] [PMID: 11418579]
[79]
Volff, J.N.; Altenbuchner, J. Genetic instability of the Streptomyces chromosome. Mol. Microbiol., 1998, 27(2), 239-246.
[http://dx.doi.org/10.1046/j.1365-2958.1998.00652.x] [PMID: 9484880]
[80]
Yu, Z.; Reichheld, S.E.; Savchenko, A.; Parkinson, J.; Davidson, A.R. A comprehensive analysis of structural and sequence conservation in the TetR family transcriptional regulators. J. Mol. Biol., 2010, 400(4), 847-864.
[http://dx.doi.org/10.1016/j.jmb.2010.05.062] [PMID: 20595046]
[81]
Cuthbertson, L.; Nodwell, J.R. The TetR family of regulators. Microbiol. Mol. Biol. Rev., 2013, 77(3), 440-475.
[http://dx.doi.org/10.1128/MMBR.00018-13] [PMID: 24006471]
[82]
Guo, J.; Zhang, X.; Luo, S.; He, F.; Chen, Z.; Wen, Y.; Li, J. A novel TetR family transcriptional regulator, SAV576, negatively controls avermectin biosynthesis in Streptomyces avermitilis. PLoS One, 2013, 8(8), e71330.
[http://dx.doi.org/10.1371/journal.pone.0071330] [PMID: 23967193]
[83]
Deutscher, J.; Francke, C.; Postma, P.W. How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol. Mol. Biol. Rev., 2006, 70(4), 939-1031.
[http://dx.doi.org/10.1128/MMBR.00024-06] [PMID: 17158705]
[84]
Dyda, F.; Klein, D.C.; Hickman, A.B. GCN5-related N-acetyltransferases: a structural overview. Annu. Rev. Biophys. Biomol. Struct., 2000, 29(1), 81-103.
[http://dx.doi.org/10.1146/annurev.biophys.29.1.81] [PMID: 10940244]
[85]
Pukatzki, S.; Ma, A.T.; Sturtevant, D.; Krastins, B.; Sarracino, D.; Nelson, W.C.; Heidelberg, J.F.; Mekalanos, J.J. Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc. Natl. Acad. Sci. USA, 2006, 103(5), 1528-1533.
[http://dx.doi.org/10.1073/pnas.0510322103] [PMID: 16432199]
[86]
Mougous, J.D.; Cuff, M.E.; Raunser, S.; Shen, A.; Zhou, M.; Gifford, C.A.; Goodman, A.L.; Joachimiak, G.; Ordoñez, C.L.; Lory, S.; Walz, T.; Joachimiak, A.; Mekalanos, J.J. A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science, 2006, 312(5779), 1526-1530.
[http://dx.doi.org/10.1126/science.1128393] [PMID: 16763151]
[87]
Viars, S.; Valentine, J.; Hernick, M. Structure and function of the LmbE-like superfamily. Biomolecules, 2014, 4(2), 527-545.
[http://dx.doi.org/10.3390/biom4020527] [PMID: 24970229]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy