PCR-based Screening Approach: A Rapid Method to Detect the Biosynthetic Potential of Antimicrobials in Actinobacterial Strains

Arasu MV, Duraipandiyan V, Ignacimuthu S. Antibacterial and antifungal activities of polyketide metabolite from marine Streptomyces sp. AP-123 and its cytotoxic effect. Chemosphere. 2013 Jan; 90(2):479–487. https://doi.org/10.1016/j.chemosphere.2012.08.006 Arasu MV Duraipandiyan V Ignacimuthu S. Antibacterial and antifungal activities of polyketide metabolite from marine Streptomyces sp. AP-123 and its cytotoxic effect . Chemosphere. 2013 Jan ; 90 ( 2 ): 479 – 487 . https://doi.org/10.1016/j.chemosphere.2012.08.006 10.1016/j.chemosphere.2012.08.006 Search in Google Scholar

Ayuso-Sacido A, Genilloud O. New PCR primers for the screening of NRPS and PKS-I systems in actinomycetes: detection and distribution of these biosynthetic gene sequences in major taxonomic groups. Microb Ecol. 2005 Jan;49(1):10–24. https://doi.org/10.1007/s00248-004-0249-6 Ayuso-Sacido A Genilloud O. New PCR primers for the screening of NRPS and PKS-I systems in actinomycetes: detection and distribution of these biosynthetic gene sequences in major taxonomic groups . Microb Ecol. 2005 Jan ; 49 ( 1 ): 10 – 24 . https://doi.org/10.1007/s00248-004-0249-6 10.1007/s00248-004-0249-6 Search in Google Scholar

Bischoff D, Pelzer S, Bister B, Nicholson GJ, Stockert S, Schirle M, Wohlleben W, Jung G, Süssmuth RD. The biosynthesis of vancomycin-type glycopeptide antibiotics – the order of the cyclization steps. Angew Chem Int Ed. 2001 Dec 17; 40(24): 4688–4691. https://doi.org/10.1002/1521-3773(20011217)40:24<4688::AID-ANIE4688>3.0.CO;2-M Bischoff D Pelzer S Bister B Nicholson GJ Stockert S Schirle M Wohlleben W Jung G Süssmuth RD. The biosynthesis of vancomycin-type glycopeptide antibiotics – the order of the cyclization steps . Angew Chem Int Ed. 2001 Dec 17 ; 40 ( 24 ): 4688 – 4691 . https://doi.org/10.1002/1521-3773(20011217)40:24<4688::AID-ANIE4688>3.0.CO;2-M 10.1002/1521-3773(20011217)40:24<4688::AID-ANIE4688>3.0.CO;2-M Search in Google Scholar

Brautaset T, Bruheim P, Sletta H, Hagen L, Ellingsen TE, Strøm AR, Valla S, Zotchev SB. Hexaene derivatives of nystatin produced as a result of an induced rearrangement within the nysC polyketide synthase gene in S. noursei ATCC 11455. Chem Biol. 2002 Mar;9(3):367–373. https://doi.org/10.1016/S1074-5521(02)00108-4 Brautaset T Bruheim P Sletta H Hagen L Ellingsen TE Strøm AR Valla S Zotchev SB. Hexaene derivatives of nystatin produced as a result of an induced rearrangement within the nysC polyketide synthase gene in S. noursei ATCC 11455 . Chem Biol. 2002 Mar ; 9 ( 3 ): 367 – 373 . https://doi.org/10.1016/S1074-5521(02)00108-4 10.1016/S1074-5521(02)00108-4 Search in Google Scholar

Bu QT, Yu P, Wang J, Li ZY, Chen XA, Mao XM, Li YQ. Rational construction of genome-reduced and high-efficient industrial Streptomyces chassis based on multiple comparative genomic approaches. Microb Cell Fact. 2019 Dec;18(1):16. https://doi.org/10.1186/s12934-019-1055-7 Bu QT Yu P Wang J Li ZY Chen XA Mao XM Li YQ. Rational construction of genome-reduced and high-efficient industrial Streptomyces chassis based on multiple comparative genomic approaches . Microb Cell Fact. 2019 Dec ; 18 ( 1 ): 16 . https://doi.org/10.1186/s12934-019-1055-7 10.1186/s12934-019-1055-7 Search in Google Scholar

Busti E, Monciardini P, Cavaletti L, Bamonte R, Lazzarini A, Sosio M, Donadio S. Antibiotic-producing ability by representatives of a newly discovered lineage of actinomycetes. Microbiology. 2006 Mar 01;152(3):675–683. https://doi.org/10.1099/mic.0.28335-0 Busti E Monciardini P Cavaletti L Bamonte R Lazzarini A Sosio M Donadio S. Antibiotic-producing ability by representatives of a newly discovered lineage of actinomycetes . Microbiology. 2006 Mar 01 ; 152 ( 3 ): 675 – 683 . https://doi.org/10.1099/mic.0.28335-0 10.1099/mic.0.28335-0 Search in Google Scholar

Chou WKW, Fanizza I, Uchiyama T, Komatsu M, Ikeda H, Cane DE. Genome mining in Streptomyces avermitilis: cloning and characterization of SAV_76, the synthase for a new sesquiterpene, avermitilol. J Am Chem Soc. 2010 Jul 07;132(26):8850–8851. https://doi.org/10.1021/ja103087w Chou WKW Fanizza I Uchiyama T Komatsu M Ikeda H Cane DE. Genome mining in Streptomyces avermitilis: cloning and characterization of SAV_76, the synthase for a new sesquiterpene, avermitilol . J Am Chem Soc. 2010 Jul 07 ; 132 ( 26 ): 8850 – 8851 . https://doi.org/10.1021/ja103087w 10.1021/ja103087w Search in Google Scholar

Dhaneesha M, Benjamin Naman C, Krishnan KP, Sinha RK, Jayesh P, Joseph V, Bright Singh IS, Gerwick WH, Sajeevan TP. Streptomyces artemisiae MCCB 248 isolated from Arctic fjord sediments has unique PKS and NRPS biosynthetic genes and produces potential new anticancer natural products. 3 Biotech. 2017 May;7(1):32. https://doi.org/10.1007/s13205-017-0610-3 Dhaneesha M Benjamin Naman C Krishnan KP Sinha RK Jayesh P Joseph V Bright Singh IS Gerwick WH Sajeevan TP. Streptomyces artemisiae MCCB 248 isolated from Arctic fjord sediments has unique PKS and NRPS biosynthetic genes and produces potential new anticancer natural products . 3 Biotech. 2017 May ; 7 ( 1 ): 32 . https://doi.org/10.1007/s13205-017-0610-3 10.1007/s13205-017-0610-3 Search in Google Scholar

Du L, Chen M, Sánchez C, Shen B. An oxidation domain in the BlmIII non-ribosomal peptide synthetase probably catalyzing thiazole formation in the biosynthesis of the anti-tumor drug bleomycin in Streptomyces verticillus ATCC15003. FEMS Microbiol Lett. 2000;189(2):171–175. https://doi.org/10.1111/j.1574-6968.2000.tb09225.x Du L Chen M Sánchez C Shen B. An oxidation domain in the BlmIII non-ribosomal peptide synthetase probably catalyzing thiazole formation in the biosynthesis of the anti-tumor drug bleomycin in Streptomyces verticillus ATCC15003 . FEMS Microbiol Lett. 2000 ; 189 ( 2 ): 171 – 175 . https://doi.org/10.1111/j.1574-6968.2000.tb09225.x 10.1111/j.1574-6968.2000.tb09225.x Search in Google Scholar

Encheva-Malinova M, Stoyanova M, Avramova H, Pavlova Y, Gocheva B, Ivanova I, Moncheva P. Antibacterial potential of streptomycete strains from Antarctic soils. Biotechnol Biotechnol Equip. 2014 Jul 04;28(4):721–727. https://doi.org/10.1080/13102818.2014.947066 Encheva-Malinova M Stoyanova M Avramova H Pavlova Y Gocheva B Ivanova I Moncheva P. Antibacterial potential of streptomycete strains from Antarctic soils . Biotechnol Biotechnol Equip. 2014 Jul 04 ; 28 ( 4 ): 721 – 727 . https://doi.org/10.1080/13102818.2014.947066 10.1080/13102818.2014.947066 Search in Google Scholar

Fatima A, Aftab U, Shaaban KA, Thorson JS, Sajid I. Spore forming Actinobacterial diversity of Cholistan Desert Pakistan: polyphasic taxonomy, antimicrobial potential and chemical profiling. BMC Microbiol. 2019 Dec;19(1):49. https://doi.org/10.1186/s12866-019-1414-x Fatima A Aftab U Shaaban KA Thorson JS Sajid I. Spore forming Actinobacterial diversity of Cholistan Desert Pakistan: polyphasic taxonomy, antimicrobial potential and chemical profiling . BMC Microbiol. 2019 Dec ; 19 ( 1 ): 49 . https://doi.org/10.1186/s12866-019-1414-x 10.1186/s12866-019-1414-x Search in Google Scholar

Genilloud O, González I, Salazar O, Martín J, Tormo JR, Vicente F. Current approaches to exploit actinomycetes as a source of novel natural products. J Ind Microbiol Biotechnol. 2011 Mar; 38(3):375–389. https://doi.org/10.1007/s10295-010-0882-7 Genilloud O González I Salazar O Martín J Tormo JR Vicente F. Current approaches to exploit actinomycetes as a source of novel natural products . J Ind Microbiol Biotechnol. 2011 Mar ; 38 ( 3 ): 375 – 389 . https://doi.org/10.1007/s10295-010-0882-7 10.1007/s10295-010-0882-7 Search in Google Scholar

Gontang EA, Gaudêncio SP, Fenical W, Jensen PR. Sequence-based analysis of secondary-metabolite biosynthesis in marine actinobacteria. Appl Environ Microbiol. 2010;76(8):2487–2499. https://doi.org/10.1128/AEM.02852-09 Gontang EA Gaudêncio SP Fenical W Jensen PR. Sequence-based analysis of secondary-metabolite biosynthesis in marine actinobacteria . Appl Environ Microbiol. 2010 ; 76 ( 8 ): 2487 – 2499 . https://doi.org/10.1128/AEM.02852-09 10.1128/AEM.02852-09 Search in Google Scholar

Hwang KS, Kim HU, Charusanti P, Palsson BØ, Lee SY. Systems biology and biotechnology of Streptomyces species for the production of secondary metabolites. Biotechnol Adv. 2014 Mar;32(2):255–268. https://doi.org/10.1016/j.biotechadv.2013.10.008 Hwang KS Kim HU Charusanti P Palsson BØ, Lee SY. Systems biology and biotechnology of Streptomyces species for the production of secondary metabolites . Biotechnol Adv. 2014 Mar ; 32 ( 2 ): 255 – 268 . https://doi.org/10.1016/j.biotechadv.2013.10.008 10.1016/j.biotechadv.2013.10.008 Search in Google Scholar

Hwang YB, Lee MY, Park HJ, Han K, Kim ES. Isolation of putative polyene-producing actinomycetes strains via PCR-based genome screening for polyene-specific hydroxylase genes. Process Biochem. 2007 Jan;42(1):102–107. https://doi.org/10.1016/j.procbio.2006.06.031 Hwang YB Lee MY Park HJ Han K Kim ES. Isolation of putative polyene-producing actinomycetes strains via PCR-based genome screening for polyene-specific hydroxylase genes . Process Biochem. 2007 Jan ; 42 ( 1 ): 102 – 107 . https://doi.org/10.1016/j.procbio.2006.06.031 10.1016/j.procbio.2006.06.031 Search in Google Scholar

Komaki H, Ichikawa N, Tamura T, Oguchi A, Hamada M, Fujita N. Genome-based survey of nonribosomal peptide synthetase and polyketide synthase gene clusters in type strains of the genus Microtetraspora. J Antibiot (Tokyo). 2016 Sep;69(9):712–718. https://doi.org/10.1038/ja.2015.139 Komaki H Ichikawa N Tamura T Oguchi A Hamada M Fujita N. Genome-based survey of nonribosomal peptide synthetase and polyketide synthase gene clusters in type strains of the genus Microtetraspora . J Antibiot (Tokyo). 2016 Sep ; 69 ( 9 ): 712 – 718 . https://doi.org/10.1038/ja.2015.139 10.1038/ja.2015.139 Search in Google Scholar

Komatsu M, Uchiyama T, Ōmura S, Cane DE, Ikeda H. Genome-minimized Streptomyces host for the heterologous expression of secondary metabolism. Proc Natl Acad Sci USA. 2010 Feb 09; 107(6):2646–2651. https://doi.org/10.1073/pnas.0914833107 Komatsu M Uchiyama T Ōmura S Cane DE Ikeda H. Genome-minimized Streptomyces host for the heterologous expression of secondary metabolism . Proc Natl Acad Sci USA. 2010 Feb 09 ; 107 ( 6 ): 2646 – 2651 . https://doi.org/10.1073/pnas.0914833107 10.1073/pnas.0914833107 Search in Google Scholar

Lamb DC, Ikeda H, Nelson DR, Ishikawa J, Skaug T, Jackson C, Omura S, Waterman MR, Kelly SL. Cytochrome P450 complement (CYPome) of the avermectin-producer Streptomyces avermitilis and comparison to that of Streptomyces coelicolor A3(2). Biochem Biophys Res Commun. 2003 Aug;307(3):610–619. https://doi.org/10.1016/S0006-291X(03)01231-2 Lamb DC Ikeda H Nelson DR Ishikawa J Skaug T Jackson C Omura S Waterman MR Kelly SL. Cytochrome P450 complement (CYPome) of the avermectin-producer Streptomyces avermitilis and comparison to that of Streptomyces coelicolor A3(2) . Biochem Biophys Res Commun. 2003 Aug ; 307 ( 3 ): 610 – 619 . https://doi.org/10.1016/S0006-291X(03)01231-2 10.1016/S0006-291X(03)01231-2 Search in Google Scholar

Le TH, Sivachidambaram V, Yi X, Li X, Zhou Z. Quantification of polyketide synthase genes in tropical urban soils using real-time PCR. J Microbiol Methods. 2014 Nov;106:135–142. https://doi.org/10.1016/j.mimet.2014.08.010 Le TH Sivachidambaram V Yi X Li X Zhou Z. Quantification of polyketide synthase genes in tropical urban soils using real-time PCR . J Microbiol Methods. 2014 Nov ; 106 : 135 – 142 . https://doi.org/10.1016/j.mimet.2014.08.010 10.1016/j.mimet.2014.08.01025181693 Search in Google Scholar

Lee MY, Myeong JS, Park HJ, Han K, Kim ES. Isolation and partial characterization of a cryptic polyene gene cluster in Pseudonocardia autotrophica. J Ind Microbiol Biotechnol. 2006 Feb;33(2):84–87. https://doi.org/10.1007/s10295-005-0018-7 Lee MY Myeong JS Park HJ Han K Kim ES. Isolation and partial characterization of a cryptic polyene gene cluster in Pseudonocardia autotrophica . J Ind Microbiol Biotechnol. 2006 Feb ; 33 ( 2 ): 84 – 87 . https://doi.org/10.1007/s10295-005-0018-7 10.1007/s10295-005-0018-716096834 Search in Google Scholar

Omura S, Ikeda H, Ishikawa J, Hanamoto A, Takahashi C, Shinose M, Takahashi Y, Horikawa H, Nakazawa H, Osonoe T, et al. Genome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites. Proc Natl Acad Sci USA. 2001 Oct 09;98(21): 12215–12220. https://doi.org/10.1073/pnas.211433198 Omura S Ikeda H Ishikawa J Hanamoto A Takahashi C Shinose M Takahashi Y Horikawa H Nakazawa H Osonoe T , Genome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites . Proc Natl Acad Sci USA. 2001 Oct 09 ; 98 ( 21 ): 12215 – 12220 . https://doi.org/10.1073/pnas.211433198 10.1073/pnas.211433198 Search in Google Scholar

Silambarasan S, Murugan T, Saravanan D, Balagurunathan R. Antibacterial and antifungal activities of Actinobacteria isolated from Rathnagiri hills. J Appl Pharm Sci. 2012 Oct 28;2:99. https://doi.org/10.7324/JAPS.2012.21020 Silambarasan S Murugan T Saravanan D Balagurunathan R. Antibacterial and antifungal activities of Actinobacteria isolated from Rathnagiri hills . J Appl Pharm Sci. 2012 Oct 28 ; 2 : 99 . https://doi.org/10.7324/JAPS.2012.21020 10.7324/JAPS.2012.21020 Search in Google Scholar

Sosio M, Stinchi S, Beltrametti F, Lazzarini A, Donadio S. The gene cluster for the biosynthesis of the glycopeptide antibiotic A40926 by nonomuraea species. Chem Biol. 2003 Jun;10(6):541–549. https://doi.org/10.1016/S1074-5521(03)00120-0 Sosio M Stinchi S Beltrametti F Lazzarini A Donadio S. The gene cluster for the biosynthesis of the glycopeptide antibiotic A40926 by nonomuraea species . Chem Biol. 2003 Jun ; 10 ( 6 ): 541 – 549 . https://doi.org/10.1016/S1074-5521(03)00120-0 10.1016/S1074-5521(03)00120-0 Search in Google Scholar

Winter JM, Behnken S, Hertweck C. Genomics-inspired discovery of natural products. Curr Opin Chem Biol. 2011 Feb;15(1):22–31. https://doi.org/10.1016/j.cbpa.2010.10.020 Winter JM Behnken S Hertweck C. Genomics-inspired discovery of natural products . Curr Opin Chem Biol. 2011 Feb ; 15 ( 1 ): 22 – 31 . https://doi.org/10.1016/j.cbpa.2010.10.020 10.1016/j.cbpa.2010.10.02021111667 Search in Google Scholar

Wood SA, Kirby BM, Goodwin CM, Le Roes M, Meyers PR. PCR screening reveals unexpected antibiotic biosynthetic potential in Amycolatopsis sp. strain UM16. J Appl Microbiol. 2007 Jan; 102(1):245–253. https://doi.org/10.1111/j.1365-2672.2006.03043.x Wood SA Kirby BM Goodwin CM Le Roes M Meyers PR. PCR screening reveals unexpected antibiotic biosynthetic potential in Amycolatopsis sp. strain UM16 . J Appl Microbiol. 2007 Jan ; 102 ( 1 ): 245 – 253 . https://doi.org/10.1111/j.1365-2672.2006.03043.x 10.1111/j.1365-2672.2006.03043.x17184341 Search in Google Scholar

Wu L, Chen G, Feng G. Complete genome sequence of Streptomyces griseochromogenes ATCC 14511T, a producer of nucleoside compounds and diverse secondary metabolites. J Biotechnol. 2017 May; 249:16–19. https://doi.org/10.1016/j.jbiotec.2017.03.017 Wu L Chen G Feng G. Complete genome sequence of Streptomyces griseochromogenes ATCC 14511^T, a producer of nucleoside compounds and diverse secondary metabolites . J Biotechnol. 2017 May ; 249 : 16 – 19 . https://doi.org/10.1016/j.jbiotec.2017.03.017 10.1016/j.jbiotec.2017.03.01728342817 Search in Google Scholar

Xu L, Ye K-X, Dai W-H, Sun C, Xu L-H, Han B-N. Comparative genomic insights into secondary metabolism biosynthetic gene cluster distributions of marine Streptomyces. Mar Drugs. 2019 Aug 26;17(9):E498. https://doi.org/10.3390/md17090498 Xu L Ye K-X Dai W-H Sun C Xu L-H Han B-N. Comparative genomic insights into secondary metabolism biosynthetic gene cluster distributions of marine Streptomyces . Mar Drugs. 2019 Aug 26 ; 17 ( 9 ): E498 . https://doi.org/10.3390/md17090498 10.3390/md17090498678007931454987 Search in Google Scholar

Ye S, Molloy B, Braña AF, Zabala D, Olano C, Cortés J, Morís F, Salas JA, Méndez C. Identification by genome mining of a type I polyketide gene cluster from Streptomyces argillaceus involved in the biosynthesis of pyridine and piperidine alkaloids argimycins P. Front Microbiol. 2017 Feb 10;8:194. https://doi.org/10.3389/fmicb.2017.00194 Ye S Molloy B Braña AF Zabala D Olano C Cortés J Morís F Salas JA Méndez C. Identification by genome mining of a type I polyketide gene cluster from Streptomyces argillaceus involved in the biosynthesis of pyridine and piperidine alkaloids argimycins P . Front Microbiol. 2017 Feb 10 ; 8 : 194 . https://doi.org/10.3389/fmicb.2017.00194 10.3389/fmicb.2017.00194530097228239372 Search in Google Scholar