Abstract
Streptomyces coelicolor genome carries two apparently paralogous genes, SCO4164 and SCO5854, that encode putative thiosulfate sulfurtransferases (rhodaneses). These genes (and their presumed translation products) are highly conserved and widely distributed across actinobacterial genomes. The SCO4164 knockout strain was unable to grow on minimal media with either sulfate or sulfite as the sole sulfur source. The SCO5854 mutant had no growth defects in the presence of various sulfur sources; however, it produced significantly less amounts of actinorhodin. Furthermore, we discuss possible links between basic interconversions of inorganic sulfur species and secondary metabolism in S. coelicolor.
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References
Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Klenk HP, Clément C, Ouhdouch Y, van Wezel GP (2015) Taxonomy, physiology, and natural products of Actinobacteria. Microbiol Mol Biol Rev 80(1):1–43. https://doi.org/10.1128/MMBR.00019-15
Bishop A, Fielding S, Dyson P, Herron P (2004) Systematic insertional mutagenesis of streptomycete genome: a link between osmoadaptation and antibiotic production. Genome Res 14:893–900. https://doi.org/10.1101/gr.1710304
Cipollone R, Ascenzi P, Visca P (2007) Common themes and variations in the rhodanese superfamily. IUBMB Life 59(2):51–19. https://doi.org/10.1080/15216540701206859
Chang Z, Vining LC (2002) Biosynthesis of sulfur-containing amino acids in Streptomyces venezuelae ISP5230: roles for cystathionine beta-synthase and transsulfuration. Microbiology 148(7):2135–2247
Dereeper A, Guignon V, Blanc G, Audic S et al (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acid Res 36:W465–W469. https://doi.org/10.1093/nar/gkn180
Donadio S, Shafiee A, Hutchinson CR (1990) Disruption of a rhodaneselike gene results in cysteine auxotrophy in Saccharopolyspora erythraea. J Bacteriol 172(1):350–360
Hertweck C, Luzhetskyy A, Rebets Y, Bechthold A (2007) Type II polyketide synthases: gaining a deeper insight into enzymatic teamwork. Nat Prod Rep 24(1):162–190. https://doi.org/10.1039/b507395m
Hodgson DA (2000) Primary metabolism and its control in streptomycetes: a most unusual group of bacteria. Adv Microb Physiol 42:47–238
Huang J, Shi J, Molle V, Sohlberg B, Weaver D, Bibb MJ, Karoonuthaisiri N, Lih CJ, Kao CM, Buttner MJ, Cohen SN (2005) Cross-regulation among disparate antibiotic biosynthetic pathways of Streptomyces coelicolor. Mol Microbiol 58:1276-1287
Ishizuka H, Horinouchi S, Kieser HM, Hopwood DA, Beppu T (1992) A putative two-component regulatory system involved in secondary metabolism in Streptomyces spp. J Bacteriol 174:7585–7594
Jeong Y, Kim JN, Kim MW, Bucca G, Cho S, Yoon YJ, Kim BG, Roe JH, Kim SC, Smith CP, Cho BK (2016) The dynamic transcriptional and translational landscape of the model antibiotic producer Streptomyces coelicolor A3(2). Nat Commun 7:11605. https://doi.org/10.1038/ncomms11605
Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA (2000) Practical Streptomyces genetics. John Innes Foundation, Norwich
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Kitano K, Nozaki Y, Imada A (1985) Selective accumulation of unsulfated carbapenem antibiotics by sulfate transport negative mutants of S. griseus subsp. cryophilus. Agric Biol Chem 49:677–684
Kredich NM (2008) Biosynthesis of cysteine. EcoSal Plus 3(1):1–30. https://doi.org/10.1128/ecosalplus.3.6.1.11
Lee EJ, Karoonuthaisiri N, Kim HS, Park JH, Cha CJ, Kao CM, Roe JH (2005 Sep) A master regulator sigmaB governs osmotic and oxidative response as well as differentiation via a network of sigma factors in Streptomyces coelicolor. Mol Microbiol 57(5):1252–1264
Leustek T, Martin MN, Bick JA, Davies JP (2000) Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu Rev Plant Physiol Plant Mol Biol 51:141–165
Lydiate DJ, Mendez C, Kieser HM, Hopwood DA (1988) Mutation and cloning of clustered Streptomyces genes essential for sulfate metabolism. Mol Gen Genet 211:415–423
Marzluf GA (1997) Molecular genetics of sulfur assimilation in filamentous fungi and yeast. Annu Rev Microbiol 51:73–96
Mueller EG (2006) Trafficking in persulfides: delivering sulfur in biosynthetic pathways. Nat Chem Biol 2(4):185–194. https://doi.org/10.1038/nchembio779
Nárdiz N, Santamarta I, Lorenzana LM, Martín JF, Liras P (2011) A rhodanese-like protein is highly overrepresented in the mutant S. clavuligerus oppA2::aph: effect on holomycin and other secondary metabolites production. Microb Biotechnol 4(2):216–225. https://doi.org/10.1111/j.1751-7915.2010.00222.x
Rückert C, Koch DJ, Rey DA, Albersmeier A, Mormann S, Pühler A, Kalinowski J (2005) Functional genomics and expression analysis of the Corynebacterium glutamicum fpr2-cysIXHDNYZ gene cluster involved in assimilatory sulphate reduction. BMC Genomics 6:121
Rückert C (2016) Sulfate reduction in microorganisms – recent advances and biotechnological applications. Curr Opin Microbiol 33:140–146. https://doi.org/10.1016/j.mib.2016.07.007
Sambrook J, Russell DW (2001) Molecular Cloning: a Laboratory Manual, 3rd edn. NY: Cold Spring Harbor Laboratory
Sienko M, Natorff R, Skoneczny M, Kruszewska J, Paszewski A, Brzywczy J (2014) Regulatory mutations affecting sulfur metabolism induce environmental stress response in Aspergillus nidulans. Fungal Genet Biol 65:37–47. https://doi.org/10.1016/j.fgb.2014.02.001
Vandenbergh PA, Bawdon RE, Berk RS (1979) Rapid test for determining the intracellular rhodanese activity of various bacteria. Int J Syst Bacteriol 29(4):339–344
Zeng L, Shi T, Zhao Q, Xie J (2013) Mycobacterium sulfur metabolism and implications for novel drug targets. Cell Biochem Biophys 65(2):77–83. https://doi.org/10.1007/s12013-012-9410-x
Acknowledgements
This work was supported by grants Bg-46F (to V.O.) and Bg-41Nr (to B.O.) from Ministry of Education and Science of Ukraine. T.G. was supported by DAAD fellowships. Prof. Paul Dyson (Swansea University, UK) is thanked for cosmids from S. coelicolor transposon library. We thank Lijiang Song (Univerity of Warwick, UK) for proofreading the manuscript.
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Gren, T., Ostash, B., Babiy, V. et al. Analysis of Streptomyces coelicolor M145 genes SCO4164 and SCO5854 encoding putative rhodaneses. Folia Microbiol 63, 197–201 (2018). https://doi.org/10.1007/s12223-017-0551-6
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DOI: https://doi.org/10.1007/s12223-017-0551-6