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RpoS Activates the Prodigionsin Production by Activating the Transcription of the RpoS-Dependent Pig Gene Cluster in Serratia marcescens FS14

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Abstract

RpoS, an alternative sigma factor of RNA polymerase, regulates the expression of a great deal of genes involved in stationary-phase survival and stress response. To identify the function of RpoS homologue in Serratia marcescens FS14, in-frame deletion mutant of rpoS was constructed. It was found that RpoS activates the biosynthesis of prodigiosin in FS14 which is just opposite to what was observed in Serratia sp. ATCC 39006. We also demonstrated that RpoS positively regulates the prodigiosin production by activating the transcription of pig cluster in FS14, and the transcription of pig cluster is RpoS-dependent. Further study showed that the differences in the promoters of pig clusters in FS14 and 39006 lead to the different selection of the sigma factors and result in the different regulation mechanisms. The -10 element and the spacer region between -10 and -35 elements of the pig cluster in FS14 are vital for the RpoS recognition in FS14.

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The genome data had been deposited into NCBI GenBank with the Accession number: CP005927.

References

  1. Harris AK, Williamson NR, Slater H, Cox A, Abbasi S, Foulds I et al (2004) The Serratia gene cluster encoding biosynthesis of the red antibiotic, prodigiosin, shows species- and strain-dependent genome context variation. Microbiology 150:3547–3560. https://doi.org/10.1099/mic.0.27222-0

    Article  CAS  PubMed  Google Scholar 

  2. Williamson NR, Simonsen HT, Ahmed RA, Goldet G, Slater H, Woodley L et al (2005) Biosynthesis of the red antibiotic, prodigiosin, in Serratia: identification of a novel 2-methyl-3-n-amyl-pyrrole (MAP) assembly pathway, definition of the terminal condensing enzyme, and implications for undecylprodigiosin biosynthesis in Streptomyces. Mol Microbiol 56:971–989. https://doi.org/10.1111/j.1365-2958.2005.04602.x

    Article  CAS  PubMed  Google Scholar 

  3. Williamson NR, Simonsen HT, Harris AK, Leeper FJ, Salmond GP (2006) Disruption of the copper efflux pump (CopA) of Serratia marcescens ATCC 274 pleiotropically affects copper sensitivity and production of the tripyrrole secondary metabolite, prodigiosin. J Ind Microbiol Biotechnol 33:151–158. https://doi.org/10.1007/s10295-005-0040-9

    Article  CAS  PubMed  Google Scholar 

  4. Han R, Xiang R, Li J, Wang F, Wang C (2021) High-level production of microbial prodigiosin A review. J Basic Microbiol. https://doi.org/10.1002/jobm.202100101

    Article  PubMed  Google Scholar 

  5. Stella NA, Fender JE, Lahr RM, Kalivoda EJ, Shanks RM (2012) The LysR transcription factor, HexS, is required for glucose inhibition of prodigiosin production by Serratia marcescens. Adv Microbiol 2:511–517. https://doi.org/10.4236/aim.2012.24065

    Article  CAS  Google Scholar 

  6. Paget MS, Helmann JD (2003) The sigma70 family of sigma factors. Genome Biol 4:203. https://doi.org/10.1186/gb-2003-4-1-203

  7. Wilf NM, Salmond GP (2012) The stationary phase sigma factor, RpoS, regulates the production of a carbapenem antibiotic, a bioactive prodigiosin and virulence in the enterobacterial pathogen Serratia sp. ATCC 39006. Microbiology 158:648–658. https://doi.org/10.1099/mic.0.055780-0

    Article  CAS  PubMed  Google Scholar 

  8. Liu X, Wu Y, Chen Y, Xu F, Halliday N, Gao K et al (2016) RpoS differentially affects the general stress response and biofilm formation in the endophytic Serratia plymuthica G3. Res Microbiol 167:168–177. https://doi.org/10.1016/j.resmic.2015.11.003

    Article  CAS  PubMed  Google Scholar 

  9. Guan J, Xiao X, Xu S, Gao F, Wang J, Wang T et al (2015) Roles of RpoS in Yersinia pseudotuberculosis stress survival, motility, biofilm formation and type VI secretion system expression. J Microbiol 53:633–642. https://doi.org/10.1007/s12275-015-0099-6

    Article  CAS  PubMed  Google Scholar 

  10. Huerta AM, Collado-Vides J (2003) Sigma70 promoters in Escherichia coli: specific transcription in dense regions of overlapping promoter-like signals. J Mol Biol 333:261–278. https://doi.org/10.1016/j.jmb.2003.07.017

    Article  CAS  PubMed  Google Scholar 

  11. Typas A, Becker G, Hengge R (2007) The molecular basis of selective promoter activation by the sigmaS subunit of RNA polymerase. Mol Microbiol 63:1296–1306. https://doi.org/10.1111/j.1365-2958.2007.05601.x

    Article  CAS  PubMed  Google Scholar 

  12. Espinosa-Urgel M, Chamizo C, Tormo A (1996) A consensus structure for sigma S-dependent promoters. Mol Microbiol 21:657–659. https://doi.org/10.1111/j.1365-2958.1996.tb02573.x

    Article  CAS  PubMed  Google Scholar 

  13. Lee SJ, Gralla JD (2001) Sigma38 (rpoS) RNA polymerase promoter engagement via -10 region nucleotides. J Biol Chem 276:30064–30071. https://doi.org/10.1074/jbc.M102886200

    Article  CAS  PubMed  Google Scholar 

  14. Fenton MS, Gralla JD (2001) Function of the bacterial TATAAT -10 element as single-stranded DNA during RNA polymerase isomerization. Proc Natl Acad Sci USA 98:9020–9025. https://doi.org/10.1073/pnas.161085798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Schaumburg CS, Tan M (2003) Mutational analysis of the Chlamydia trachomatis dnaK promoter defines the optimal -35 promoter element. Nucleic Acids Res 31:551–555. https://doi.org/10.1093/nar/gkg150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Wise A, Brems R, Ramakrishnan V, Villarejo M (1996) Sequences in the -35 region of Escherichia coli rpoS-dependent genes promote transcription by E sigma S. J Bacteriol 178:2785–2793. https://doi.org/10.1128/jb.178.10.2785-2793.1996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Typas A, Hengge R (2006) Role of the spacer between the -35 and -10 regions in sigmas promoter selectivity in Escherichia coli. Mol Microbiol 59:1037–1051. https://doi.org/10.1111/j.1365-2958.2005.04998.x

    Article  CAS  PubMed  Google Scholar 

  18. Qin H, Liu Y, Cao X, Jiang J, Lian W, Qiao D et al (2020) RpoS is a pleiotropic regulator of motility, biofilm formation, exoenzymes, siderophore and prodigiosin production, and trade-off during prolonged stationary phase in Serratia marcescens. PLoS ONE. https://doi.org/10.1371/journal.pone.0232549

    Article  PubMed  PubMed Central  Google Scholar 

  19. Zhang X, Wu D, Guo T, Ran T, Wang W, Xu D (2018) Differential roles for ArcA and ArcB homologues in swarming motility in Serratia marcescens FS14. Antonie Van Leeuwenhoek 111:609–617. https://doi.org/10.1007/s10482-017-0981-9

    Article  CAS  PubMed  Google Scholar 

  20. Slater H, Crow M, Everson L, Salmond GP (2003) Phosphate availability regulates biosynthesis of two antibiotics, prodigiosin and carbapenem, in Serratia via both quorum-sensing-dependent and -independent pathways. Mol Microbiol 47:303–320. https://doi.org/10.1046/j.1365-2958.2003.03295.x

    Article  CAS  PubMed  Google Scholar 

  21. Ruff EF, Record MT Jr, Artsimovitch I (2015) Initial events in bacterial transcription initiation. Biomolecules 5:1035–1062. https://doi.org/10.3390/biom5021035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Bowers CW, Dombroski AJ (1999) A mutation in region 1.1 of sigma70 affects promoter DNA binding by Escherichia coli RNA polymerase holoenzyme. EMBO J 18:709–716. https://doi.org/10.1093/emboj/18.3.709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Li P, Kwok AH, Jiang J, Ran T, Xu D, Wang W et al (2015) Comparative genome analyses of Serratia marcescens FS14 reveals its high antagonistic potential. PLoS ONE 10:e0123061. https://doi.org/10.1371/journal.pone.0123061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Woodcock DM, Crowther PJ, Doherty J, Jefferson S, DeCruz E, Noyer-Weidner M et al (1989) Quantitative evaluation of Escherichia coli host strains for tolerance to cytosine methylation in plasmid and phage recombinants. Nucleic Acids Res 17:3469–3478. https://doi.org/10.1093/nar/17.9.3469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Herrero M, de Lorenzo V, Timmis KN (1990) Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J Bacteriol 172:6557–6567. https://doi.org/10.1128/jb.172.11.6557-6567.1990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by Grant Nos. 31770050, 31770074 from the National Natural Science Foundation of China.

Funding

This work was supported by Grant Nos. 31770050, 31770074 from the National Natural Science Foundation of China.

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BY: Investigation, Data Curation, Visualization, Writing-original draft; FC and HL: Investigation, Formal analysis; WW: Supervision, Funding acquisition, Writing-review & editing; TR: Formal analysis; DX: Conceptualization, Resources, Supervision, Project administration, Funding acquisition, Writing-review & editing.

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Correspondence to Dongqing Xu.

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Yang, B., Chu, F., Li, H. et al. RpoS Activates the Prodigionsin Production by Activating the Transcription of the RpoS-Dependent Pig Gene Cluster in Serratia marcescens FS14. Indian J Microbiol 61, 355–363 (2021). https://doi.org/10.1007/s12088-021-00952-4

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