Generic placeholder image

Current Biotechnology

Editor-in-Chief

ISSN (Print): 2211-5501
ISSN (Online): 2211-551X

Review Article

Ribosomal Protein S12 and its Effects on Specialized Metabolism of Streptomyces Bacteria

Author(s): Bohdan Ostash*

Volume 12, Issue 2, 2023

Published on: 30 May, 2023

Page: [94 - 102] Pages: 9

DOI: 10.2174/2211550112666230505105656

Price: $65

Abstract

Species within the actinobacterial genus Streptomyces represent one of the most gifted natural chemists in the microbial world. Their specialized metabolites attract the interest of the pharmaceutical industry as a source of novel drugs. A majority of these molecules pose an insurmountable challenge for economically justified production via chemical synthesis. Therefore, submerged fermentation-based isolation of such molecules often remains the only viable way to obtain them. This in turn fuels interest in process development programs aiming to maximize the yield of specialized metabolite per volume unit of fermentation medium. Along with the optimization of the medium and the fermentation mode itself, strain improvement remains an important part of an overall process development endeavor. An improved strain can be generated via application of traditional approaches of selection for random or induced mutants and genomics-enabled genetic engineering methods. Here I focus on a specific class of mutations with the gene rpsL for ribosomal protein S12, which often confer resistance to streptomycin in bacteria and upregulate specialized metabolism in Streptomyces. The review will portray the evolution of our understanding of the mechanisms behind rpsL mutations, as well as how technological advances change the way these mutations are introduced into the genomes of interest.

Keywords: Streptomyces, natural products, antibiotics, gene rpsL, ribosome, engineering.

Graphical Abstract
[1]
Antimicrobial resistance in the age of COVID-19. Nat Microbiol 2020; 5(6): 779.
[http://dx.doi.org/10.1038/s41564-020-0739-4] [PMID: 32433531]
[2]
Carpouron JE, de Hoog S, Gentekaki E, Hyde KD. Emerging animal-associated fungal diseases. J Fungi 2022; 8(6): 611.
[http://dx.doi.org/10.3390/jof8060611] [PMID: 35736094]
[3]
Ribeiro da Cunha B, Fonseca LP, Calado CRC. Antibiotic discovery: Where have we come from, where do we go? Antibiotics 2019; 8(2): 45.
[http://dx.doi.org/10.3390/antibiotics8020045] [PMID: 31022923]
[4]
Gratia A, Dath S. Proprietes bacteriolytiques de certaines moisissures. Compt Rend Soc Biol 1924; 91: 1442-3.
[5]
Welsch M. Bacteriostatic and bacteriolytic properties of actinomycetes. J Bacteriol 1942; 44(5): 571-88.
[http://dx.doi.org/10.1128/jb.44.5.571-588.1942] [PMID: 16560596]
[6]
Landwehr W, Wolf C, Wink J. Actinobacteria and myxobacteria - two of the most important bacterial resources for novel antibiotics. Curr Top Microbiol Immunol 2016; 398: 273-302.
[http://dx.doi.org/10.1007/82_2016_503] [PMID: 27704272]
[7]
Walesch S, Birkelbach J, Jézéquel G, et al. Fighting antibiotic resistance-strategies and (pre)clinical developments to find new antibacterials. EMBO Rep 2023; 24(1): e56033.
[http://dx.doi.org/10.15252/embr.202256033] [PMID: 36533629]
[8]
Kautsar SA, Blin K, Shaw S, Weber T, Medema MH. BiG-FAM: The biosynthetic gene cluster families database. Nucleic Acids Res 2021; 49(D1): D490-7.
[http://dx.doi.org/10.1093/nar/gkaa812] [PMID: 33010170]
[9]
Pye CR, Bertin MJ, Lokey RS, Gerwick WH, Linington RG. Retrospective analysis of natural products provides insights for future discovery trends. Proc Natl Acad Sci 2017; 114(22): 5601-6.
[http://dx.doi.org/10.1073/pnas.1614680114] [PMID: 28461474]
[10]
Gavriilidou A, Kautsar SA, Zaburannyi N, et al. Compendium of specialized metabolite biosynthetic diversity encoded in bacterial genomes. Nat Microbiol 2022; 7(5): 726-35.
[http://dx.doi.org/10.1038/s41564-022-01110-2]
[11]
Liu Z, Zhao Y, Huang C, Luo Y. Recent advances in silent gene cluster activation in Streptomyces. Front Bioeng Biotechnol 2021; 9: 632230.
[http://dx.doi.org/10.3389/fbioe.2021.632230] [PMID: 33681170]
[12]
van Bergeijk DA, Terlouw BR, Medema MH, van Wezel GP. Ecology and genomics of Actinobacteria: New concepts for natural product discovery. Nat Rev Microbiol 2020; 18(10): 546-58.
[http://dx.doi.org/10.1038/s41579-020-0379-y] [PMID: 32483324]
[13]
Arakawa K. Manipulation of metabolic pathways controlled by signaling molecules, inducers of antibiotic production, for genome mining in Streptomyces spp. Antonie van Leeuwenhoek 2018; 111(5): 743-51.
[http://dx.doi.org/10.1007/s10482-018-1052-6] [PMID: 29476430]
[14]
Baltz RH. Genetic manipulation of secondary metabolite biosynthesis for improved production in Streptomyces and other actinomycetes. J Ind Microbiol Biotechnol 2016; 43(2-3): 343-70.
[http://dx.doi.org/10.1007/s10295-015-1682-x] [PMID: 26364200]
[15]
Ostash B. Pleiotropic regulatory genes as a tool for Streptomyces strains bioprospecting and improvement. Curr Biotechnol 2021; 10(1): 18-31.
[http://dx.doi.org/10.2174/2211550110666210217105112]
[16]
Ochi K. From microbial differentiation to ribosome engineering. Biosci Biotechnol Biochem 2007; 71(6): 1373-86.
[http://dx.doi.org/10.1271/bbb.70007] [PMID: 17587668]
[17]
Ochi K. Insights into microbial cryptic gene activation and strain improvement: Principle, application and technical aspects. J Antibiot 2017; 70(1): 25-40.
[http://dx.doi.org/10.1038/ja.2016.82] [PMID: 27381522]
[18]
Gorini L, Kataja E. Phenotypic repair by streptomycin of defective genotypes in E. coli. Proc Natl Acad Sci 1964; 51(3): 487-93.
[http://dx.doi.org/10.1073/pnas.51.3.487] [PMID: 14171463]
[19]
Biswas DK, Gorini L. Restriction, de-restriction and mistranslation in missense suppression. Ribosomal discrimination of transfer RNA’s. J Mol Biol 1972; 64(1): 119-34.
[http://dx.doi.org/10.1016/0022-2836(72)90324-5] [PMID: 4552481]
[20]
Sharma D, Cukras AR, Rogers EJ, Southworth DR, Green R. Mutational analysis of S12 protein and implications for the accuracy of decoding by the ribosome. J Mol Biol 2007; 374(4): 1065-76.
[http://dx.doi.org/10.1016/j.jmb.2007.10.003] [PMID: 17967466]
[21]
Vila-Sanjurjo A, Lu Y, Aragonez JL, Starkweather RE, Sasikumar M, O’Connor M. Modulation of 16S rRNA function by ribosomal protein S12. Biochim Biophys Acta Gene Struct Expr 2007; 1769(7-8): 462-71.
[http://dx.doi.org/10.1016/j.bbaexp.2007.04.004] [PMID: 17512991]
[22]
Maisnier-Patin S, Paulander W, Pennhag A, Andersson DI. Compensatory evolution reveals functional interactions between ribosomal proteins S12, L14 and L19. J Mol Biol 2007; 366(1): 207-15.
[http://dx.doi.org/10.1016/j.jmb.2006.11.047] [PMID: 17157877]
[23]
Stark H, Rodnina MV, Wieden HJ, Zemlin F, Wintermeyer W, van Heel M. Ribosome interactions of aminoacyl-tRNA and elongation factor Tu in the codon-recognition complex. Nat Struct Biol 2002; 9(11): 849-54.
[http://dx.doi.org/10.1038/nsb859] [PMID: 12379845]
[24]
Cukras AR, Southworth DR, Brunelle JL, Culver GM, Green R. Ribosomal proteins S12 and S13 function as control elements for translocation of the mRNA:tRNA complex. Mol Cell 2003; 12(2): 321-8.
[http://dx.doi.org/10.1016/S1097-2765(03)00275-2] [PMID: 14536072]
[25]
Gregory ST, Carr JF, Dahlberg AE. A signal relay between ribosomal protein S12 and elongation factor EF-Tu during decoding of mRNA. RNA 2009; 15(2): 208-14.
[http://dx.doi.org/10.1261/rna.1355709] [PMID: 19095621]
[26]
Ninio J. Multiple stages in codon-anticodon recognition:Double-trigger mechanisms and geometric constraints. Biochimie 2006; 88(8): 963-92.
[http://dx.doi.org/10.1016/j.biochi.2006.06.002] [PMID: 16843583]
[27]
Demirci H, Murphy F IV, Murphy E, Gregory ST, Dahlberg AE, Jogl G. A structural basis for streptomycin-induced misreading of the genetic code. Nat Commun 2013; 4(1): 1355.
[http://dx.doi.org/10.1038/ncomms2346] [PMID: 23322043]
[28]
Paulander W, Maisnier-Patin S, Andersson DI. The fitness cost of streptomycin resistance depends on rpsL mutation, carbon source and RpoS (sigmaS). Genetics 2009; 183(2): 539-46.
[http://dx.doi.org/10.1534/genetics.109.106104] [PMID: 19652179]
[29]
Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci 2000; 97(12): 6640-5.
[http://dx.doi.org/10.1073/pnas.120163297] [PMID: 10829079]
[30]
Agarwal D, Gregory ST, O’Connor M. Error-prone and error-restrictive mutations affecting ribosomal protein S12. J Mol Biol 2011; 410(1): 1-9.
[http://dx.doi.org/10.1016/j.jmb.2011.04.068] [PMID: 21575643]
[31]
Taylor DE, Trieber CA, Trescher G, Bekkering M. Host mutations (miaA and rpsL) reduce tetracycline resistance mediated by Tet(O) and Tet(M). Antimicrob Agents Chemother 1998; 42(1): 59-64.
[http://dx.doi.org/10.1128/AAC.42.1.59] [PMID: 9449261]
[32]
Rodnina MV, Gromadski KB, Kothe U, Wieden HJ. Recognition and selection of tRNA in translation. FEBS Lett 2005; 579(4): 938-42.
[http://dx.doi.org/10.1016/j.febslet.2004.11.048] [PMID: 15680978]
[33]
Demeshkina N, Jenner L, Westhof E, Yusupov M, Yusupova G. A new understanding of the decoding principle on the ribosome. Nature 2012; 484(7393): 256-9.
[http://dx.doi.org/10.1038/nature10913] [PMID: 22437501]
[34]
Rozov A, Demeshkina N, Westhof E, Yusupov M, Yusupova G. Structural insights into the translational infidelity mechanism. Nat Commun 2015; 6(1): 7251.
[http://dx.doi.org/10.1038/ncomms8251] [PMID: 26037619]
[35]
Chumpolkulwong N, Hori-Takemoto C, Hosaka T, et al. Effects of Escherichia coli ribosomal protein S12 mutations on cell-free protein synthesis. Eur J Biochem 2004; 271(6): 1127-34.
[http://dx.doi.org/10.1111/j.1432-1033.2004.04016.x] [PMID: 15009191]
[36]
Hosaka T, Tamehiro N, Chumpolkulwong N, et al. The novel mutation K87E in ribosomal protein S12 enhances protein synthesis activity during the late growth phase in Escherichia coli. Mol Genet Genomics 2004; 271(3): 317-24.
[http://dx.doi.org/10.1007/s00438-004-0982-z] [PMID: 14966659]
[37]
Shima J, Hesketh A, Okamoto S, Kawamoto S, Ochi K. Induction of actinorhodin production by rpsL (encoding ribosomal protein S12) mutations that confer streptomycin resistance in Streptomyces lividans and Streptomyces coelicolor A3(2). J Bacteriol 1996; 178(24): 7276-84.
[http://dx.doi.org/10.1128/jb.178.24.7276-7284.1996] [PMID: 8955413]
[38]
Zhu S, Duan Y, Huang Y. The application of ribosome engineering to natural product discovery and yield improvement in Streptomyces. Antibiotics 2019; 8(3): 133.
[http://dx.doi.org/10.3390/antibiotics8030133] [PMID: 31480298]
[39]
Gromyko O, Rebets Y, Ostash B, et al. Generation of Streptomyces globisporus SMY622 strain with increased landomycin E production and it’s initial characterization. J Antibiot 2004; 57(6): 383-9.
[http://dx.doi.org/10.7164/antibiotics.57.383] [PMID: 15323127]
[40]
Okamoto-Hosoya Y, Hosaka T, Ochi K. An aberrant protein synthesis activity is linked with antibiotic overproduction in rpsL mutants of Streptomyces coelicolor A3(2). Microbiolog 2003; 149(11): 3299-309.
[http://dx.doi.org/10.1099/mic.0.26490-0] [PMID: 14600242]
[41]
Wang G, Inaoka T, Okamoto S, Ochi K. A novel insertion mutation in Streptomyces coelicolor ribosomal S12 protein results in paromomycin resistance and antibiotic overproduction. Antimicrob Agents Chemother 2009; 53(3): 1019-26.
[http://dx.doi.org/10.1128/AAC.00388-08] [PMID: 19104019]
[42]
Hosaka T, Xu J, Ochi K. Increased expression of ribosome recycling factor is responsible for the enhanced protein synthesis during the late growth phase in an antibiotic-overproducing Streptomyces coelicolor ribosomal rpsL mutant. Mol Microbiol 2006; 61(4): 883-97.
[http://dx.doi.org/10.1111/j.1365-2958.2006.05285.x] [PMID: 16859496]
[43]
Tamehiro N, Hosaka T, Xu J, Hu H, Otake N, Ochi K. Innovative approach for improvement of an antibiotic-overproducing industrial strain of Streptomyces albus. Appl Environ Microbiol 2003; 69(11): 6412-7.
[http://dx.doi.org/10.1128/AEM.69.11.6412-6417.2003] [PMID: 14602594]
[44]
Tanaka Y, Komatsu M, Okamoto S, et al. Antibiotic overproduction by rpsL and rsmG mutants of various actinomycetes. Appl Environ Microbiol 2009; 75(14): 4919-22.
[http://dx.doi.org/10.1128/AEM.00681-09] [PMID: 19447953]
[45]
Lv XA, Jin YY, Li YD, Zhang H, Liang XL. Genome shuffling of Streptomyces viridochromogenes for improved production of avilamycin. Appl Microbiol Biotechnol 2013; 97(2): 641-8.
[http://dx.doi.org/10.1007/s00253-012-4322-7] [PMID: 22911092]
[46]
Wang Q, Zhang D, Li Y, Zhang F, Wang C, Liang X. Genome shuffling and ribosome engineering of Streptomyces actuosus for high-yield nosiheptide production. Appl Biochem Biotechnol 2014; 173(6): 1553-63.
[http://dx.doi.org/10.1007/s12010-014-0948-5] [PMID: 24828581]
[47]
Liu L, Pan J, Wang Z, et al. Ribosome engineering and fermentation optimization leads to overproduction of tiancimycin A, a new enediyne natural product from Streptomyces sp. CB03234. J Ind Microbiol Biotechnol 2018; 45(3): 141-51.
[http://dx.doi.org/10.1007/s10295-018-2014-8] [PMID: 29396746]
[48]
Westhoff S, van Leeuwe TM, Qachach O, Zhang Z, van Wezel GP, Rozen DE. The evolution of no-cost resistance at sub-MIC concentrations of streptomycin in Streptomyces coelicolor. ISME J 2017; 11(5): 1168-78.
[http://dx.doi.org/10.1038/ismej.2016.194] [PMID: 28094796]
[49]
Shemediuk AL, Dolia BS, Ochi K, Fedorenko VO, Ostash BO. Properties of spontaneous rpsL mutant of Streptomyces albus KO-1297. Cytol Genet 2022; 56(1): 31-6.
[http://dx.doi.org/10.3103/S009545272201011X] [PMID: 35194265]
[50]
Robinson LJ, Cameron ADS, Stavrinides J. Spontaneous and on point: Do spontaneous mutations used for laboratory experiments cause pleiotropic effects that might confound bacterial infection and evolution assays? FEMS Microbiol Lett 2015; 362(21): fnv177.
[http://dx.doi.org/10.1093/femsle/fnv177] [PMID: 26420853]
[51]
Okamoto-Hosoya Y, Okamoto S, Ochi K. Development of antibiotic-overproducing strains by site-directed mutagenesis of the rpsL gene in Streptomyces lividans. Appl Environ Microbiol 2003; 69(7): 4256-9.
[http://dx.doi.org/10.1128/AEM.69.7.4256-4259.2003] [PMID: 12839808]
[52]
Hosaka T, Ohnishi-Kameyama M, Muramatsu H, et al. Antibacterial discovery in actinomycetes strains with mutations in RNA polymerase or ribosomal protein S12. Nat Biotechnol 2009; 27(5): 462-4.
[http://dx.doi.org/10.1038/nbt.1538] [PMID: 19396160]
[53]
Myronovskyi M, Luzhetskyy A. Heterologous production of small molecules in the optimized Streptomyces hosts. Nat Prod Rep 2019; 36(9): 1281-94.
[http://dx.doi.org/10.1039/C9NP00023B] [PMID: 31453623]
[54]
Yuzawa S, Mirsiaghi M, Jocic R, et al. Short-chain ketone production by engineered polyketide synthases in Streptomyces albus. Nat Commun 2018; 9(1): 4569.
[http://dx.doi.org/10.1038/s41467-018-07040-0] [PMID: 30385744]
[55]
Tan GY, Deng K, Liu X, et al. Heterologous biosynthesis of spinosad: An omics-guided large polyketide synthase gene cluster reconstitution in Streptomyces. ACS Synth Biol 2017; 6(6): 995-1005.
[http://dx.doi.org/10.1021/acssynbio.6b00330] [PMID: 28264562]
[56]
Marín L, Gutiérrez-del-Río I, Villar CJ, Lombó F. De novo biosynthesis of garbanzol and fustin in Streptomyces albus based on a potential flavanone 3‐hydroxylase with 2‐hydroxylase side activity. Microb Biotechnol 2021; 14(5): 2009-24.
[http://dx.doi.org/10.1111/1751-7915.13874] [PMID: 34216097]
[57]
Herrmann S, Siegl T, Luzhetska M, et al. Site-specific recombination strategies for engineering actinomycete genomes. Appl Environ Microbiol 2012; 78(6): 1804-12.
[http://dx.doi.org/10.1128/AEM.06054-11] [PMID: 22247163]
[58]
Koshla O, Lopatniuk M, Borys O, et al. Genetically engineered rpsL merodiploidy impacts secondary metabolism and antibiotic resistance in Streptomyces. World J Microbiol Biotechnol 2021; 37(4): 62.
[http://dx.doi.org/10.1007/s11274-021-03030-5] [PMID: 33730177]
[59]
Yushchuk O, Kharel M, Ostash I, Ostash B. Landomycin biosynthesis and its regulation in Streptomyces. Appl Microbiol Biotechnol 2019; 103(4): 1659-65.
[http://dx.doi.org/10.1007/s00253-018-09601-1] [PMID: 30635689]
[60]
Medema MH, Trefzer A, Kovalchuk A, et al. The sequence of a 1.8-mb bacterial linear plasmid reveals a rich evolutionary reservoir of secondary metabolic pathways. Genome Biol Evol 2010; 2: 212-24.
[http://dx.doi.org/10.1093/gbe/evq013] [PMID: 20624727]
[61]
Shaikh AA, Nothias LF, Srivastava SK, Dorrestein PC, Tahlan K. Specialized metabolites from ribosome engineered strains of Streptomyces clavuligerus. Metabolites 2021; 11(4): 239.
[http://dx.doi.org/10.3390/metabo11040239] [PMID: 33924621]
[62]
Gomez-Escribano JP, Bibb MJ. Engineering Streptomyces coelicolor for heterologous expression of secondary metabolite gene clusters. Microb Biotechnol 2011; 4(2): 207-15.
[http://dx.doi.org/10.1111/j.1751-7915.2010.00219.x] [PMID: 21342466]
[63]
Kumar K, Bruheim P. A comparative study at bioprocess and metabolite levels of superhost strain Streptomyces coelicolor M1152 and its derivative M1581 heterologously expressing chloramphenicol biosynthetic gene cluster. Biotechnol Bioeng 2022; 119(1): 145-61.
[http://dx.doi.org/10.1002/bit.27958] [PMID: 34636422]
[64]
Sidda JD, Poon V, Song L, Wang W, Yang K, Corre C. Overproduction and identification of butyrolactones SCB1-8 in the antibiotic production superhost Streptomyces M1152. Org Biomol Chem 2016; 14(27): 6390-3.
[http://dx.doi.org/10.1039/C6OB00840B] [PMID: 27180870]
[65]
Cobb RE, Wang Y, Zhao H. High-efficiency multiplex genome editing of Streptomyces species using an engineered CRISPR/Cas system. ACS Synth Biol 2015; 4(6): 723-8.
[http://dx.doi.org/10.1021/sb500351f] [PMID: 25458909]
[66]
Jakočiūnas T, Jensen MK, Keasling JD. CRISPR/Cas9 advances engineering of microbial cell factories. Metab Eng 2016; 34: 44-59.
[http://dx.doi.org/10.1016/j.ymben.2015.12.003] [PMID: 26707540]
[67]
Huang H, Zheng G, Jiang W, Hu H, Lu Y. One-step high-efficiency CRISPR/Cas9-mediated genome editing in <italic>Streptomyces</italic>. Acta Biochim Biophys Sin (Shanghai) 2015; 47(4): 231-43.
[http://dx.doi.org/10.1093/abbs/gmv007] [PMID: 25739462]
[68]
Lopatniuk M, Myronovskyi M, Nottebrock A, et al. Effect of “ribosome engineering” on the transcription level and production of S. albus indigenous secondary metabolites. Appl Microbiol Biotechnol 2019; 103(17): 7097-110.
[http://dx.doi.org/10.1007/s00253-019-10005-y] [PMID: 31324940]
[69]
Schrader SM, Vaubourgeix J, Nathan C. Biology of antimicrobial resistance and approaches to combat it. Sci Transl Med 2020; 12(549): eaaz6992.
[http://dx.doi.org/10.1126/scitranslmed.aaz6992] [PMID: 32581135]
[70]
Wright GD. Q&A: Antibiotic resistance: What more do we know and what more can we do? BMC Biol 2013; 11(1): 51.
[http://dx.doi.org/10.1186/1741-7007-11-51] [PMID: 23683650]
[71]
Linardi D, She W, Zhang Q, Yu Y, Qian PY, Lam H. Proteomining-based elucidation of natural product biosynthetic pathways in Streptomyces. Front Microbiol 2022; 13: 913756.
[http://dx.doi.org/10.3389/fmicb.2022.913756] [PMID: 35898901]
[72]
Ameruoso A, Villegas Kcam MC, Cohen KP, Chappell J. Activating natural product synthesis using CRISPR interference and activation systems in Streptomyces. Nucleic Acids Res 2022; 50(13): 7751-60.
[http://dx.doi.org/10.1093/nar/gkac556] [PMID: 35801861]
[73]
Pepler MA, Zhang X. Hindra, Elliot MA. Hindra, Elliot MA. Inducing global expression of actinobacterial biosynthetic gene clusters. Methods Mol Biol 2022; 2489: 157-71.
[http://dx.doi.org/10.1007/978-1-0716-2273-5_9] [PMID: 35524050]
[74]
Lacey HJ, Rutledge PJ. Recently discovered secondary metabolites from Streptomyces species. Molecules 2022; 27(3): 887.
[http://dx.doi.org/10.3390/molecules27030887] [PMID: 35164153]
[75]
Lee N, Choi M, Kim W, et al. Re-classification of Streptomyces venezuelae strains and mining secondary metabolite biosynthetic gene clusters. iScience 2021; 24(12): 103410.
[http://dx.doi.org/10.1016/j.isci.2021.103410] [PMID: 34877485]
[76]
Caicedo-Montoya C, Manzo-Ruiz M, Ríos-Estepa R. Pan-Genome of the genus Streptomyces and prioritization of biosynthetic gene clusters with potential to produce antibiotic compounds. Front Microbiol 2021; 12: 677558.
[http://dx.doi.org/10.3389/fmicb.2021.677558] [PMID: 34659136]
[77]
Martinet L, Naômé A, Baiwir D, De Pauw E, Mazzucchelli G, Rigali S. On the risks of phylogeny-based strain prioritization for drug discovery: Streptomyces lunaelactis as a case Study. Biomolecules 2020; 10(7): 1027.
[http://dx.doi.org/10.3390/biom10071027] [PMID: 32664387]
[78]
Hemmerling F, Piel J. Strategies to access biosynthetic novelty in bacterial genomes for drug discovery. Nat Rev Drug Discov 2022; 21(5): 359-78.
[http://dx.doi.org/10.1038/s41573-022-00414-6] [PMID: 35296832]
[79]
Kautsar SA, van der Hooft JJJ, de Ridder D, Medema MH. BiG-SLiCE: A highly scalable tool maps the diversity of 1.2 million biosynthetic gene clusters. Gigascience 2021; 10(1): giaa154.
[http://dx.doi.org/10.1093/gigascience/giaa154] [PMID: 33438731]
[80]
Hug J, Bader C, Remškar M, Cirnski K, Müller R. Concepts and methods to access novel antibiotics from actinomycetes. Antibiotics 2018; 7(2): 44.
[http://dx.doi.org/10.3390/antibiotics7020044] [PMID: 29789481]
[81]
Newman DJ, Cragg GM. Natural products as sources of new drugs over the nearly four decades from 01/1981 to 09/2019. J Nat Prod 2020; 83(3): 770-803.
[http://dx.doi.org/10.1021/acs.jnatprod.9b01285] [PMID: 32162523]
[82]
Belknap KC, Park CJ, Barth BM, Andam CP. Genome mining of biosynthetic and chemotherapeutic gene clusters in Streptomyces bacteria. Sci Rep 2020; 10(1): 2003.
[http://dx.doi.org/10.1038/s41598-020-58904-9] [PMID: 32029878]
[83]
Bisacchi GS, Manchester JI. A new-class antibacterial-almost. lessons in drug discovery and development: A critical analysis of more than 50 years of effort toward ATPase inhibitors of DNA gyrase and topoisomerase IV. ACS Infect Dis 2015; 1(1): 4-41.
[http://dx.doi.org/10.1021/id500013t] [PMID: 27620144]
[84]
Ostash B, Doud E, Fedorenko V. The molecular biology of moenomycins: Towards novel antibiotics based on inhibition of bacterial peptidoglycan glycosyltransferases. Biol Chem 2010; 391(5): 499-504.
[http://dx.doi.org/10.1515/bc.2010.053] [PMID: 20302515]
[85]
Kling A, Lukat P, Almeida DV, et al. Targeting DnaN for tuberculosis therapy using novel griselimycins. Science 2015; 348(6239): 1106-12.
[http://dx.doi.org/10.1126/science.aaa4690] [PMID: 26045430]
[86]
Bugg TDH, Kerr RV. Mechanism of action of nucleoside antibacterial natural product antibiotics. J Antibiot (Tokyo) 2019; 72(12): 865-76.
[http://dx.doi.org/10.1038/s41429-019-0227-3] [PMID: 31471595]
[87]
Bailly C. The bacterial thiopeptide thiostrepton. An update of its mode of action, pharmacological properties and applications. Eur J Pharmacol 2022; 914: 174661.
[http://dx.doi.org/10.1016/j.ejphar.2021.174661] [PMID: 34863996]
[88]
Zhang C, Seyedsayamdost MR. Discovery of a cryptic depsipeptide from Streptomyces ghanaensisvia MALDI-MS-guided high-throughput elicitor screening. Angew Chem Int Ed 2020; 59(51): 23005-9.
[http://dx.doi.org/10.1002/anie.202009611] [PMID: 32790054]
[89]
Covington BC, Xu F, Seyedsayamdost MR. A Natural product chemist’s guide to unlocking silent biosynthetic gene clusters. Annu Rev Biochem 2021; 90(1): 763-88.
[http://dx.doi.org/10.1146/annurev-biochem-081420-102432] [PMID: 33848426]
[90]
Montiel D, Kang HS, Chang FY, Charlop-Powers Z, Brady SF. Yeast homologous recombination-based promoter engineering for the activation of silent natural product biosynthetic gene clusters. Proc Natl Acad Sci USA 2015; 112(29): 8953-8.
[http://dx.doi.org/10.1073/pnas.1507606112] [PMID: 26150486]
[91]
Pishchany G, Mevers E, Ndousse-Fetter S, et al. Amycomicin is a potent and specific antibiotic discovered with a targeted interaction screen. Proc Natl Acad Sci USA 2018; 115(40): 10124-9.
[http://dx.doi.org/10.1073/pnas.1807613115] [PMID: 30228116]
[92]
Kavaliauskas D, Chen C, Liu W, Cooperman BS, Goldman YE, Knudsen CR. Structural dynamics of translation elongation factor Tu during aa-tRNA delivery to the ribosome. Nucleic Acids Res 2018; 46(16): 8651-61.
[http://dx.doi.org/10.1093/nar/gky651] [PMID: 30107527]
[93]
Pavlov MY, Liljas A, Ehrenberg M. A recent intermezzo at the Ribosome Club. Philos Trans R Soc Lond B Biol Sci 2017; 372(1716): 20160185.
[http://dx.doi.org/10.1098/rstb.2016.0185] [PMID: 28138071]
[94]
Ochi K, Okamoto S, Tozawa Y, et al. Ribosome engineering and secondary metabolite production. Adv Appl Microbiol 2004; 56: 155-84.
[http://dx.doi.org/10.1016/S0065-2164(04)56005-7] [PMID: 15566979]
[95]
Ma Z, Tao L, Bechthold A, Shentu X, Bian Y, Yu X. Overexpression of ribosome recycling factor is responsible for improvement of nucleotide antibiotic-toyocamycin in Streptomyces diastatochromogenes 1628. Appl Microbiol Biotechnol 2014; 98(11): 5051-8.
[http://dx.doi.org/10.1007/s00253-014-5573-2] [PMID: 24509772]
[96]
Funane K, Tanaka Y, Hosaka T, et al. Combined drug resistance mutations substantially enhance enzyme production in Paenibacillus agaridevorans. J Bacteriol 2018; 200(17): e00188-18.
[http://dx.doi.org/10.1128/JB.00188-18] [PMID: 29866810]
[97]
Tanaka Y, Kasahara K, Hirose Y, Morimoto Y, Izawa M, Ochi K. Enhancement of butanol production by sequential introduction of mutations conferring butanol tolerance and streptomycin resistance. J Biosci Bioeng 2017; 124(4): 400-7.
[http://dx.doi.org/10.1016/j.jbiosc.2017.05.003] [PMID: 28566234]
[98]
Tanaka Y, Kasahara K, Izawa M, Ochi K. Applicability of ribosome engineering to vitamin B12 production by Propionibacterium shermanii. Biosci Biotechnol Biochem 2017; 81(8): 1636-41.
[http://dx.doi.org/10.1080/09168451.2017.1329619] [PMID: 28532245]
[99]
Lopatniuk M, Ostash B, Luzhetskyy A, Walker S, Fedorenko V. Generation and study of the strains of streptomycetes-heterologous hosts for the production of moenomycin. Russ J Genet 2014; 50(4): 360-5.
[http://dx.doi.org/10.1134/S1022795414040085] [PMID: 25624747]
[100]
Bush MJ, Tschowri N, Schlimpert S, Flärdh K, Buttner MJ. c-di-GMP signalling and the regulation of developmental transitions in streptomycetes. Nat Rev Microbiol 2015; 13(12): 749-60.
[http://dx.doi.org/10.1038/nrmicro3546] [PMID: 26499894]
[101]
Latoscha A, Wörmann ME, Tschowri N. Nucleotide second messengers in Streptomyces. Microbiology (Reading) 2019; 165(11): 1153-65.
[http://dx.doi.org/10.1099/mic.0.000846] [PMID: 31535967]
[102]
Irving SE, Choudhury NR, Corrigan RM. The stringent response and physiological roles of (pp)pGpp in bacteria. Nat Rev Microbiol 2021; 19(4): 256-71.
[http://dx.doi.org/10.1038/s41579-020-00470-y] [PMID: 33149273]

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