期刊论文详细信息
BMC Genomics
Genome mining for ribosomally synthesized and post-translationally modified peptides (RiPPs) in anaerobic bacteria
Christian Hertweck1  Sacha J Pidot2  Anne-Catrin Letzel3 
[1]Chair of Natural Product Chemistry, Friedrich Schiller University, Jena 07743, Germany
[2]Current address: Doherty Institute, The University of Melbourne, Parkville, Melbourne, Victoria 3010, Australia
[3]Leibniz Institute for Natural Product Research and Infection Biology HKI, Beutenbergstr. 11a, Jena 07745, Germany
关键词: Natural product biosynthesis;    Genomics;    Clostridia;    Anaerobic bacteria;    RiPP;    Genome mining;   
Others  :  1092383
DOI  :  10.1186/1471-2164-15-983
 received in 2014-05-30, accepted in 2014-09-23,  发布年份 2014
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【 摘 要 】

Background

Ribosomally synthesized and post-translationally modified peptides (RiPPs) are a diverse group of biologically active bacterial molecules. Due to the conserved genomic arrangement of many of the genes involved in their synthesis, these secondary metabolite biosynthetic pathways can be predicted from genome sequence data. To date, however, despite the myriad of sequenced genomes covering many branches of the bacterial phylogenetic tree, such an analysis for a broader group of bacteria like anaerobes has not been attempted.

Results

We investigated a collection of 211 complete and published genomes, focusing on anaerobic bacteria, whose potential to encode RiPPs is relatively unknown. We showed that the presence of RiPP-genes is widespread among anaerobic representatives of the phyla Actinobacteria, Proteobacteria and Firmicutes and that, collectively, anaerobes possess the ability to synthesize a broad variety of different RiPP classes. More than 25% of anaerobes are capable of producing RiPPs either alone or in conjunction with other secondary metabolites, such as polyketides or non-ribosomal peptides.

Conclusion

Amongst the analyzed genomes, several gene clusters encode uncharacterized RiPPs, whilst others show similarity with known RiPPs. These include a number of potential class II lanthipeptides; head-to-tail cyclized peptides and lactococcin 972-like RiPP. This study presents further evidence in support of anaerobic bacteria as an untapped natural products reservoir.

【 授权许可】

   
2014 Letzel et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Arnison PG, Bibb MJ, Bierbaum G, Bowers AA, Bugni TS, Bulaj G, Camarero JA, Campopiano DJ, Challis GL, Clardy J, Cotter PD, Craik DJ, Dawson M, Dittmann E, Donadio S, Dorrestein PC, Entian KD, Fischbach MA, Garavelli JS, Göransson U, Gruber CW, Haft DH, Hemscheidt TK, Hertweck C, Hill C, Horswill AR, Jaspars M, Kelly WL, Klinman JP, Kuipers OP, et al.: Ribosomally synthesized and post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature. Nat Prod Rep 2013, 30:108-160.
  • [2]McIntosh JA, Donia MS, Schmidt EW: Ribosomal peptide natural products: bridging the ribosomal and nonribosomal worlds. Nat Prod Rep 2009, 26:537-559.
  • [3]Cotter PD, Ross RP, Hill C: Bacteriocins - a viable alternative to antibiotics? Nat Rev Microbiol 2013, 11:95-105.
  • [4]Sang Y, Blecha F: Antimicrobial peptides and bacteriocins: alternatives to traditional antibiotics. Anim Health Res Rev 2008, 9:227-235.
  • [5]Willey JM, van der Donk WA: Lantibiotics: peptides of diverse structure and function. Annu Rev Microbiol 2007, 61:477-501.
  • [6]Winter JM, Behnken S, Hertweck C: Genomics-inspired discovery of natural products. Curr Opin Chem Biol 2011, 15:22-31.
  • [7]Donadio S, Sosio M, Stegmann E, Weber T, Wohlleben W: Comparative analysis and insights into the evolution of gene clusters for glycopeptide antibiotic biosynthesis. Mol Genet Genomics 2005, 274:40-50.
  • [8]Letzel A-C, Pidot SJ, Hertweck C: A genomic approach to the cryptic secondary metabolome of the anaerobic world. Nat Prod Rep 2013, 30:392-428.
  • [9]Udwary DW, Gontang EA, Jones AC, Jones CS, Schultz AW, Winter JM, Yang JY, Beauchemin N, Capson TL, Clark BR, Esquenazi E, Eustáquio AS, Freel K, Gerwick L, Gerwick WH, Gonzalez D, Liu WT, Malloy KL, Maloney KN, Nett M, Nunnery JK, Penn K, Prieto-Davo A, Simmons TL, Weitz S, Wilson MC, Tisa LS, Dorrestein PC, Moore BS: Significant natural product biosynthetic potential of actinorhizal symbionts of the genus frankia, as revealed by comparative genomic and proteomic analyses. Appl Environ Microbiol 2011, 77:3617-3625.
  • [10]Seedorf H, Fricke WF, Veith B, Bruggemann H, Liesegang H, Strittmatter A, Miethke M, Buckel W, Hinderberger J, Li F, Hagemeier C, Thauer RK, Gottschalk G: The genome of Clostridium kluyveri, a strict anaerobe with unique metabolic features. Proc Natl Acad Sci U S A 2008, 105:2128-2133.
  • [11]Behnken S, Hertweck C: Cryptic polyketide synthase genes in non-pathogenic Clostridium spp. PLoS One 2012, 7:e29609.
  • [12]Behnken S, Hertweck C: Anaerobic bacteria as producers of antibiotics. Appl Microbiol Biotechnol 2012, 96:61-67.
  • [13]Pidot S, Ishida K, Cyrulies M, Hertweck C: Discovery of clostrubin, an exceptional polyphenolic polyketide antibiotic from a strictly anaerobic bacterium. Angew Chem Int Ed 2014, 53:7856-7859.
  • [14]Lincke T, Behnken S, Ishida K, Roth M, Hertweck C: Closthioamide: an unprecedented polythioamide antibiotic from the strictly anaerobic bacterium Clostridium cellulolyticum. Angew Chem Int Ed 2010, 49:2011-2013.
  • [15]Medema MH, Blin K, Cimermancic P, de Jager V, Zakrzewski P, Fischbach MA, Weber T, Takano E, Breitling R: antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nucleic Acids Res 2011, 39:W339-W346.
  • [16]Blin K, Medema MH, Kazempour D, Fischbach MA, Breitling R, Takano E, Weber T: antiSMASH 2.0–a versatile platform for genome mining of secondary metabolite producers. Nucleic Acids Res 2013, 41:W204-W212.
  • [17]van Heel AJ, de Jong A, Montalban-Lopez M, Kok J, Kuipers OP: BAGEL3: Automated identification of genes encoding bacteriocins and (non-)bactericidal posttranslationally modified peptides. Nucleic Acids Res 2013, 41:W448-W453.
  • [18]Hammami R, Zouhir A, Le Lay C, Ben Hamida J, Fliss I: BACTIBASE second release: a database and tool platform for bacteriocin characterization. BMC Microbiol 2010, 10:22. BioMed Central Full Text
  • [19]Bierbaum G, Sahl HG: Lantibiotics: mode of action, biosynthesis and bioengineering. Curr Pharm Biotechnol 2009, 10:2-18.
  • [20]Chatterjee C, Paul M, Xie L, van der Donk WA: Biosynthesis and mode of action of lantibiotics. Chem Rev 2005, 105:633-684.
  • [21]Meindl K, Schmiederer T, Schneider K, Reicke A, Butz D, Keller S, Guhring H, Vertesy L, Wink J, Hoffmann H, Brönstrup M, Sheldrick GM, Süssmuth RD: Labyrinthopeptins: a new class of carbacyclic lantibiotics. Angew Chem Int Ed 2010, 49:1151-1154.
  • [22]Pesic A, Henkel M, Sussmuth RD: Identification of the amino acid labionin and its desulfurised derivative in the type-III lantibiotic LabA2 by means of GC/MS. Chem Comm 2011, 47:7401-7403.
  • [23]Iorio M, Sasso O, Maffioli SI, Bertorelli R, Monciardini P, Sosio M, Bonezzi F, Summa M, Brunati C, Bordoni R, Corti G, Tarozzo G, Piomelli D, Reggiani A: A glycosylated, labionin-containing lanthipeptide with marked antinociceptive activity. ACS Chem Biol 2014, 9:398-404.
  • [24]Velasquez JE, van der Donk WA: Genome mining for ribosomally synthesized natural products. Curr Opin Chem Biol 2011, 15:11-21.
  • [25]Begley M, Cotter PD, Hill C, Ross RP: Identification of a novel two-peptide lantibiotic, lichenicidin, following rational genome mining for LanM proteins. Appl Environ Microbiol 2009, 75:5451-5460.
  • [26]Voller GH, Krawczyk JM, Pesic A, Krawczyk B, Nachtigall J, Sussmuth RD: Characterization of new class III lantibiotics–erythreapeptin, avermipeptin and griseopeptin from Saccharopolyspora erythraea, Streptomyces avermitilis and Streptomyces griseus demonstrates stepwise N-terminal leader processing. Chembiochem 2012, 13:1174-1183.
  • [27]Wang H, van der Donk WA: Biosynthesis of the class III lantipeptide catenulipeptin. ACS Chem Biol 2012, 7:1529-1535.
  • [28]Kodani S, Hudson ME, Durrant MC, Buttner MJ, Nodwell JR, Willey JM: The SapB morphogen is a lantibiotic-like peptide derived from the product of the developmental gene ramS in Streptomyces coelicolor. Proc Natl Acad Sci U S A 2004, 101:11448-11453.
  • [29]Willey JM, Willems A, Kodani S, Nodwell JR: Morphogenetic surfactants and their role in the formation of aerial hyphae in Streptomyces coelicolor. Mol Microbiol 2006, 59:731-742.
  • [30]Shenkarev ZO, Finkina EI, Nurmukhamedova EK, Balandin SV, Mineev KS, Nadezhdin KD, Yakimenko ZA, Tagaev AA, Temirov YV, Arseniev AS, Ovchinnikova TV: Isolation, structure elucidation, and synergistic antibacterial activity of a novel two-component lantibiotic lichenicidin from Bacillus licheniformis VK21. Biochemistry 2010, 49:6462-6472.
  • [31]Caetano T, Krawczyk JM, Mosker E, Sussmuth RD, Mendo S: Heterologous expression, biosynthesis, and mutagenesis of type II lantibiotics from Bacillus licheniformis in Escherichia coli. Chem Biol 2011, 18:90-100.
  • [32]Singh M, Sareen D: Novel LanT associated lantibiotic clusters identified by genome database mining. PLoS One 2014, 9:e91352.
  • [33]Caetano T, Krawczyk JM, Mosker E, Sussmuth RD, Mendo S: Lichenicidin biosynthesis in Escherichia coli: licFGEHI immunity genes are not essential for lantibiotic production or self-protection. Appl Environ Microbiol 2011, 77:5023-5026.
  • [34]Fluhe L, Marahiel MA: Radical S-adenosylmethionine enzyme catalyzed thioether bond formation in sactipeptide biosynthesis. Curr Opin Chem Biol 2013, 17:605-612.
  • [35]Fluhe L, Knappe TA, Gattner MJ, Schafer A, Burghaus O, Linne U, Marahiel MA: The radical SAM enzyme AlbA catalyzes thioether bond formation in subtilosin A. Nat Chem Biol 2012, 8:350-357.
  • [36]Fluhe L, Burghaus O, Wieckowski BM, Giessen TW, Linne U, Marahiel MA: Two [4Fe-4S] clusters containing radical SAM enzyme SkfB catalyze thioether bond formation during the maturation of the sporulation killing factor. J Am Chem Soc 2013, 135:959-962.
  • [37]Murphy K, O'Sullivan O, Rea MC, Cotter PD, Ross RP, Hill C: Genome mining for radical SAM protein determinants reveals multiple sactibiotic-like gene clusters. PLoS One 2011, 6:e20852.
  • [38]Kawulka K, Sprules T, McKay RT, Mercier P, Diaper CM, Zuber P, Vederas JC: Structure of subtilosin A, an antimicrobial peptide from Bacillus subtilis with unusual posttranslational modifications linking cysteine sulfurs to alpha-carbons of phenylalanine and threonine. J Am Chem Soc 2003, 125:4726-4727.
  • [39]Huang T, Geng H, Miyyapuram VR, Sit CS, Vederas JC, Nakano MM: Isolation of a variant of subtilosin A with hemolytic activity. J Bacteriol 2009, 191:5690-5696.
  • [40]Rea MC, Sit CS, Clayton E, O'Connor PM, Whittal RM, Zheng J, Vederas JC, Ross RP, Hill C: Thuricin CD, a posttranslationally modified bacteriocin with a narrow spectrum of activity against Clostridium difficile. Proc Natl Acad Sci U S A 2010, 107:9352-9357.
  • [41]Sit CS, van Belkum MJ, McKay RT, Worobo RW, Vederas JC: The 3D solution structure of thurincin H, a bacteriocin with four sulfur to alpha-carbon crosslinks. Angew Chem Int Ed 2011, 50:8718-8721.
  • [42]Liu WT, Yang YL, Xu Y, Lamsa A, Haste NM, Yang JY, Ng J, Gonzalez D, Ellermeier CD, Straight PD, Pevzner PA, Pogliano J, Nizet V, Pogliano K, Dorrestein PC: Imaging mass spectrometry of intraspecies metabolic exchange revealed the cannibalistic factors of Bacillus subtilis. Proc Natl Acad Sci U S A 2010, 107:16286-16290.
  • [43]Haft DH, Basu MK: Biological systems discovery in silico: radical S-adenosylmethionine protein families and their target peptides for posttranslational modification. J Bacteriol 2011, 193:2745-2755.
  • [44]Nizet V, Beall B, Bast DJ, Datta V, Kilburn L, Low DE, De Azavedo JC: Genetic locus for streptolysin S production by group A streptococcus. Infect Immun 2000, 68:4245-4254.
  • [45]San Millan JL, Hernandez-Chico C, Pereda P, Moreno F: Cloning and mapping of the genetic determinants for microcin B17 production and immunity. J Bacteriol 1985, 163:275-281.
  • [46]Scholz R, Molohon KJ, Nachtigall J, Vater J, Markley AL, Sussmuth RD, Mitchell DA, Borriss R: Plantazolicin, a novel microcin B17/streptolysin S-like natural product from Bacillus amyloliquefaciens FZB42. J Bacteriol 2011, 193:215-224.
  • [47]Molohon KJ, Melby JO, Lee J, Evans BS, Dunbar KL, Bumpus SB, Kelleher NL, Mitchell DA: Structure determination and interception of biosynthetic intermediates for the plantazolicin class of highly discriminating antibiotics. ACS Chem Biol 2011, 6:1307-1313.
  • [48]Onaka H, Tabata H, Igarashi Y, Sato Y, Furumai T: Goadsporin, a chemical substance which promotes secondary metabolism and morphogenesis in streptomycetes. I. Purification and characterization. J Antibiot 2001, 54:1036-1044.
  • [49]Igarashi Y, Kan Y, Fujii K, Fujita T, Harada K, Naoki H, Tabata H, Onaka H, Furumai T: Goadsporin, a chemical substance which promotes secondary metabolism and Morphogenesis in streptomycetes. II Structure determination. J Antibiot 2001, 54:1045-1053.
  • [50]Gonzalez DJ, Lee SW, Hensler ME, Markley AL, Dahesh S, Mitchell DA, Bandeira N, Nizet V, Dixon JE, Dorrestein PC: Clostridiolysin S, a post-translationally modified biotoxin from Clostridium botulinum. J Biol Chem 2010, 285:28220-28228.
  • [51]Lee SW, Mitchell DA, Markley AL, Hensler ME, Gonzalez D, Wohlrab A, Dorrestein PC, Nizet V, Dixon JE: Discovery of a widely distributed toxin biosynthetic gene cluster. Proc Natl Acad Sci U S A 2008, 105:5879-5884.
  • [52]Bagley MC, Dale JW, Merritt EA, Xiong X: Thiopeptide antibiotics. Chem Rev 2005, 105:685-714.
  • [53]Li C, Kelly WL: Recent advances in thiopeptide antibiotic biosynthesis. Nat Prod Rep 2010, 27:153-164.
  • [54]Morris RP, Leeds JA, Naegeli HU, Oberer L, Memmert K, Weber E, LaMarche MJ, Parker CN, Burrer N, Esterow S, Hein AE, Schmitt EK, Krastel P: Ribosomally synthesized thiopeptide antibiotics targeting elongation factor Tu. J Am Chem Soc 2009, 131:5946-5955.
  • [55]Haft DH, Basu MK, Mitchell DA: Expansion of ribosomally produced natural products: a nitrile hydratase- and Nif11-related precursor family. BMC Biol 2010, 8:70. BioMed Central Full Text
  • [56]Maksimov MO, Link AJ: Prospecting genomes for lasso peptides. J Ind Microbiol Biotechnol 2014, 41:333-344.
  • [57]Maksimov MO, Pan SJ, James Link A: Lasso peptides: structure, function, biosynthesis, and engineering. Nat Prod Rep 2012, 29:996-1006.
  • [58]Tsunakawa M, Hu SL, Hoshino Y, Detlefson DJ, Hill SE, Furumai T, White RJ, Nishio M, Kawano K, Yamamoto S: Siamycins I and II, new anti-HIV peptides: I. Fermentation, isolation, biological activity and initial characterization. J Antibiot 1995, 48:433-434.
  • [59]Helynck G, Dubertret C, Mayaux JF, Leboul J: Isolation of RP 71955, a new anti-HIV-1 peptide secondary metabolite. J Antibiot 1993, 46:1756-1757.
  • [60]Wilson KA, Kalkum M, Ottesen J, Yuzenkova J, Chait BT, Landick R, Muir T, Severinov K, Darst SA: Structure of microcin J25, a peptide inhibitor of bacterial RNA polymerase, is a lassoed tail. J Am Chem Soc 2003, 125:12475-12483.
  • [61]Rosengren KJ, Clark RJ, Daly NL, Goransson U, Jones A, Craik DJ: Microcin J25 has a threaded sidechain-to-backbone ring structure and not a head-to-tail cyclized backbone. J Am Chem Soc 2003, 125:12464-12474.
  • [62]Iwatsuki M, Tomoda H, Uchida R, Gouda H, Hirono S, Omura S: Lariatins, antimycobacterial peptides produced by Rhodococcus sp. K01-B0171, have a lasso structure. J Am Chem Soc 2006, 128:7486-7491.
  • [63]Knappe TA, Linne U, Zirah S, Rebuffat S, Xie X, Marahiel MA: Isolation and structural characterization of capistruin, a lasso peptide predicted from the genome sequence of Burkholderia thailandensis E264. J Am Chem Soc 2008, 130:11446-11454.
  • [64]Knappe TA, Linne U, Robbel L, Marahiel MA: Insights into the biosynthesis and stability of the lasso peptide capistruin. Chem Biol 2009, 16:1290-1298.
  • [65]Knappe TA, Linne U, Xie X, Marahiel MA: The glucagon receptor antagonist BI-32169 constitutes a new class of lasso peptides. FEBS Lett 2010, 584:785-789.
  • [66]Potterat O, Wagner K, Gemmecker G, Mack J, Puder C, Vettermann R, Streicher R: BI-32169, a bicyclic 19-peptide with strong glucagon receptor antagonist activity from Streptomyces sp. J Nat Prod 2004, 67:1528-1531.
  • [67]Duquesne S, Destoumieux-Garzon D, Zirah S, Goulard C, Peduzzi J, Rebuffat S: Two enzymes catalyze the maturation of a lasso peptide in Escherichia coli. Chem Biol 2007, 14:793-803.
  • [68]Clarke DJ, Campopiano DJ: Maturation of McjA precursor peptide into active microcin MccJ25. Org Biomol Chem 2007, 5:2564-2566.
  • [69]Pan SJ, Rajniak J, Maksimov MO, Link AJ: The role of a conserved threonine residue in the leader peptide of lasso peptide precursors. Chem Comm 2012, 48:1880-1882.
  • [70]Severinov K, Semenova E, Kazakov A, Kazakov T, Gelfand MS: Low-molecular-weight post-translationally modified microcins. Mol Microbiol 2007, 65:1380-1394.
  • [71]Maksimov MO, Pelczer I, Link AJ: Precursor-centric genome-mining approach for lasso peptide discovery. Proc Natl Acad Sci U S A 2012, 109:15223-15228.
  • [72]Hegemann JD, Zimmermann M, Zhu S, Klug D, Marahiel MA: Lasso peptides from proteobacteria: genome mining employing heterologous expression and mass spectrometry. Biopolymers 2013, 100:527-542.
  • [73]Inokoshi J, Matsuhama M, Miyake M, Ikeda H, Tomoda H: Molecular cloning of the gene cluster for lariatin biosynthesis of Rhodococcus jostii K01-B0171. Appl Microbiol Biotechnol 2012, 95:451-460.
  • [74]Solbiati JO, Ciaccio M, Farias RN, Gonzalez-Pastor JE, Moreno F, Salomon RA: Sequence analysis of the four plasmid genes required to produce the circular peptide antibiotic microcin J25. J Bacteriol 1999, 181:2659-2662.
  • [75]Nissen-Meyer J, Rogne P, Oppegard C, Haugen HS, Kristiansen PE: Structure-function relationships of the non-lanthionine-containing peptide (class II) bacteriocins produced by gram-positive bacteria. Curr Pharm Biotechnol 2009, 10:19-37.
  • [76]Martinez B, Fernandez M, Suarez JE, Rodriguez A: Synthesis of lactococcin 972, a bacteriocin produced by Lactococcus lactis IPLA 972, depends on the expression of a plasmid-encoded bicistronic operon. Microbiology 1999, 145(Pt 11):3155-3161.
  • [77]Martinez B, Suarez JE, Rodriguez A: Lactococcin 972: a homodimeric lactococcal bacteriocin whose primary target is not the plasma membrane. Microbiology 1996, 142(Pt 9):2393-2398.
  • [78]Martinez B, Rodriguez A, Suarez JE: Lactococcin 972, a bacteriocin that inhibits septum formation in lactococci. Microbiology 2000, 146(Pt 4):949-955.
  • [79]Martinez B, Bottiger T, Schneider T, Rodriguez A, Sahl HG, Wiedemann I: Specific interaction of the unmodified bacteriocin Lactococcin 972 with the cell wall precursor lipid II. Appl Environ Microbiol 2008, 74:4666-4670.
  • [80]Holo H, Nilssen O, Nes IF: Lactococcin A, a new bacteriocin from Lactococcus lactis subsp. cremoris: isolation and characterization of the protein and its gene. J Bacteriol 1991, 173:3879-3887.
  • [81]Stoddard GW, Petzel JP, van Belkum MJ, Kok J, McKay LL: Molecular analyses of the lactococcin A gene cluster from Lactococcus lactis subsp. lactis biovar diacetylactis WM4. Appl Environ Microbiol 1992, 58:1952-1961.
  • [82]van Belkum MJ, Kok J, Venema G, Holo H, Nes IF, Konings WN, Abee T: The bacteriocin lactococcin A specifically increases permeability of lactococcal cytoplasmic membranes in a voltage-independent, protein-mediated manner. J Bacteriol 1991, 173:7934-7941.
  • [83]van Belkum MJ, Martin-Visscher LA, Vederas JC: Structure and genetics of circular bacteriocins. Trends Microbiol 2011, 19:411-418.
  • [84]Sanchez-Hidalgo M, Montalban-Lopez M, Cebrian R, Valdivia E, Martinez-Bueno M, Maqueda M: AS-48 bacteriocin: close to perfection. Cell Mol Life Sci 2011, 68:2845-2857.
  • [85]Kemperman R, Kuipers A, Karsens H, Nauta A, Kuipers O, Kok J: Identification and characterization of two novel clostridial bacteriocins, circularin A and closticin 574. Appl Environ Microbiol 2003, 69:1589-1597.
  • [86]Kemperman R, Jonker M, Nauta A, Kuipers OP, Kok J: Functional analysis of the gene cluster involved in production of the bacteriocin circularin A by Clostridium beijerinckii ATCC 25752. Appl Environ Microbiol 2003, 69:5839-5848.
  • [87]Mohimani H, Kersten RD, Liu WT, Wang M, Purvine SO, Wu S, Brewer HM, Pasa-Tolic L, Bandeira N, Moore BS, Pevzner PA, Dorrestein PC: Automated Genome Mining of Ribosomal Peptide Natural Products. ACS Chem Biol 2014, 9:1545-1551.
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