1887

Abstract

cells utilize alkanesulphonates including taurine as the sulphur source. We previously reported that when cells carrying a double deletion in and were inoculated into a taurine-containing minimal medium, they started to grow only after long-term incubation (Nishikawa . 2018, 164: 1446–1456). We show here that cells that can induce -dependent alkanesulphonate–sulphur assimilation (SASSA) are essentially rare, but suppressors that can induce SASSA appear during long-term incubation. Mutant cells carrying and or generated suppressor cells that can induce SASSA at a frequency of about 10 in a population. Whereas cells without prior SASSA did not express even when necessary, the cells with prior SASSA properly expressed . Whole-genome DNA sequencing of a clone isolated from cells with prior SASSA revealed that the influx of sulphate or thiosulphate may be related to the regulation of SASSA. To clarify whether sulphate or thiosulphate affects the induction of SASSA, the effect of mutations in and , which are responsible for sulphate and thiosulphate uptake with different preferences for substrates, was examined. Only the mutant did not show repression of SASSA when no sulphate was added to the medium. When the concentration of the sulphate added was over 10 μM, the mutant showed repression of SASSA. Therefore, it was considered that the influx of extracellular sulphate resulted in repression of SASSA.

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2022-06-15
2024-12-09
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References

  1. Miao Z, Brusseau ML, Carroll KC, Carreón-Diazconti C, Johnson B. Sulfate reduction in groundwater: characterization and applications for remediation. Environ Geochem Health 2012; 34:539–550 [View Article] [PubMed]
    [Google Scholar]
  2. Grossman AR, Gonzalez-Ballester D, Shibagaki N, Pootakham W, Moseley J. Responses to macronutrient deprivation. In Pareek A, Sopory S, Bohnert H. eds Abiotic Stress Adaptation in Plants Dordrecht: Springer; 2009
    [Google Scholar]
  3. Sirko A, Hryniewicz M, Hulanicka D, Böck A. Sulfate and thiosulfate transport in Escherichia coli K-12: nucleotide sequence and expression of the cysTWAM gene cluster. J Bacteriol 1990; 172:3351–3357 [View Article] [PubMed]
    [Google Scholar]
  4. Hryniewicz M, Sirko A, Pałucha A, Böck A, Hulanicka D. Sulfate and thiosulfate transport in Escherichia coli K-12: identification of a gene encoding a novel protein involved in thiosulfate binding. J Bacteriol 1990; 172:3358–3366 [View Article] [PubMed]
    [Google Scholar]
  5. Sirko A, Zatyka M, Sadowy E, Hulanicka D. Sulfate and thiosulfate transport in Escherichia coli K-12: evidence for a functional overlapping of sulfate- and thiosulfate-binding proteins. J Bacteriol 1995; 177:4134–4136 [View Article] [PubMed]
    [Google Scholar]
  6. Parra F, Britton P, Castle C, Jones-Mortimer MC, Kornberg HL. Two separate genes involved in sulphate transport in Escherichia coli K12. J Gen Microbiol 1983; 129:357–358 [View Article] [PubMed]
    [Google Scholar]
  7. Zhang L, Jiang W, Nan J, Almqvist J, Huang Y. The Escherichia coli CysZ is a pH dependent sulfate transporter that can be inhibited by sulfite. Biochim Biophys Acta 2014; 1838:1809–1816 [View Article] [PubMed]
    [Google Scholar]
  8. Leyh TS, Taylor JC, Markham GD. The sulfate activation locus of Escherichia coli K12: cloning, genetic, and enzymatic characterization. J Biol Chem 1988; 263:2409–2416 [PubMed]
    [Google Scholar]
  9. Satishchandran C, Markham GD. Adenosine-5’-phosphosulfate kinase from Escherichia coli K12. Purification, characterization, and identification of a phosphorylated enzyme intermediate. J Biol Chem 1989; 264:15012–15021 [PubMed]
    [Google Scholar]
  10. Satishchandran C, Hickman YN, Markham GD. Characterization of the phosphorylated enzyme intermediate formed in the adenosine 5’-phosphosulfate kinase reaction. Biochemistry 1992; 31:11684–11688 [View Article] [PubMed]
    [Google Scholar]
  11. Satishchandran C, Markham GD. Mechanistic studies of Escherichia coli adenosine-5’-phosphosulfate kinase. Arch Biochem Biophys 2000; 378:210–215 [View Article] [PubMed]
    [Google Scholar]
  12. Berendt U, Haverkamp T, Prior A, Schwenn JD. Reaction mechanism of thioredoxin: 3’-phospho-adenylylsulfate reductase investigated by site-directed mutagenesis. Eur J Biochem 1995; 233:347–356 [View Article] [PubMed]
    [Google Scholar]
  13. Savage H, Montoya G, Svensson C, Schwenn JD, Sinning I. Crystal structure of phosphoadenylyl sulphate (PAPS) reductase: a new family of adenine nucleotide alpha hydrolases. Structure 1997; 5:895–906 [View Article] [PubMed]
    [Google Scholar]
  14. Lillig CH, Prior A, Schwenn JD, Aslund F, Ritz D et al. New thioredoxins and glutaredoxins as electron donors of 3’-phosphoadenylylsulfate reductase. J Biol Chem 1999; 274:7695–7698 [View Article] [PubMed]
    [Google Scholar]
  15. Siegel LM, Davis PS. Reduced nicotinamide adenine dinucleotide phosphate-sulfite reductase of enterobacteria. IV. The Escherichia coli hemoflavoprotein: subunit structure and dissociation into hemoprotein and flavoprotein components. J Biol Chem 1974; 249:1587–1598 [PubMed]
    [Google Scholar]
  16. Tanaka Y, Yoshikaie K, Takeuchi A, Ichikawa M, Mori T et al. Crystal structure of a YeeE/YedE family protein engaged in thiosulfate uptake. Sci Adv 2020; 6:eaba7637 [View Article] [PubMed]
    [Google Scholar]
  17. Sirko AE, Zatyka M, Hulanicka MD. Identification of the Escherichia coli cysM gene encoding O-acetylserine sulphydrylase B by cloning with mini-Mu-lac containing a plasmid replicon. J Gen Microbiol 1987; 133:2719–2725 [View Article] [PubMed]
    [Google Scholar]
  18. Maier THP. Semisynthetic production of unnatural L-alpha-amino acids by metabolic engineering of the cysteine-biosynthetic pathway. Nat Biotechnol 2003; 21:422–427 [View Article] [PubMed]
    [Google Scholar]
  19. Nakatani T, Ohtsu I, Nonaka G, Wiriyathanawudhiwong N, Morigasaki S et al. Enhancement of thioredoxin/glutaredoxin-mediated L-cysteine synthesis from S-sulfocysteine increases L-cysteine production in Escherichia coli. Microb Cell Fact 2012; 11:62 [View Article] [PubMed]
    [Google Scholar]
  20. Keseler IM, Mackie A, Santos-Zavaleta A, Billington R, Bonavides-Martínez C et al. The EcoCyc database: reflecting new knowledge about Escherichia coli K-12. Nucleic Acids Res 2017; 45:D543–D550 [View Article] [PubMed]
    [Google Scholar]
  21. Kawano Y, Suzuki K, Ohtsu I. Current understanding of sulfur assimilation metabolism to biosynthesize L-cysteine and recent progress of its fermentative overproduction in microorganisms. Appl Microbiol Biotechnol 2018; 102:8203–8211 [View Article] [PubMed]
    [Google Scholar]
  22. Kredich NM, Tomkins GM. The enzymic synthesis of L-cysteine in Escherichia coli and Salmonella typhimurium. J Biol Chem 1966; 241:4955–4965 [View Article] [PubMed]
    [Google Scholar]
  23. Denk D, Böck A. L-cysteine biosynthesis in Escherichia coli: nucleotide sequence and expression of the serine acetyltransferase (cysE) gene from the wild-type and a cysteine-excreting mutant. J Gen Microbiol 1987; 133:515–525 [View Article] [PubMed]
    [Google Scholar]
  24. Kredich NM. The molecular basis for positive regulation of cys promoters in Salmonella typhimurium and Escherichia coli. Mol Microbiol 1992; 6:2747–2753 [View Article] [PubMed]
    [Google Scholar]
  25. Hryniewicz MM, Kredich NM. The cysP promoter of Salmonella typhimurium: characterization of two binding sites for CysB protein, studies of in vivo transcription initiation, and demonstration of the anti-inducer effects of thiosulfate. J Bacteriol 1991; 173:5876–5886 [View Article] [PubMed]
    [Google Scholar]
  26. Eichhorn E, van der Ploeg JR, Leisinger T. Deletion analysis of the Escherichia coli taurine and alkanesulfonate transport systems. J Bacteriol 2000; 182:2687–2695 [View Article] [PubMed]
    [Google Scholar]
  27. Eichhorn E, van der Ploeg JR, Leisinger T. Characterization of a two-component alkanesulfonate monooxygenase from Escherichia coli. J Biol Chem 1999; 274:26639–26646 [View Article] [PubMed]
    [Google Scholar]
  28. Eichhorn E, van der Ploeg JR, Kertesz MA, Leisinger T. Characterization of alpha-ketoglutarate-dependent taurine dioxygenase from Escherichia coli. J Biol Chem 1997; 272:23031–23036 [View Article] [PubMed]
    [Google Scholar]
  29. van der Ploeg JR, Weiss MA, Saller E, Nashimoto H, Saito N et al. Identification of sulfate starvation-regulated genes in Escherichia coli: a gene cluster involved in the utilization of taurine as a sulfur source. J Bacteriol 1996; 178:5438–5446 [View Article] [PubMed]
    [Google Scholar]
  30. Nishikawa M, Shen L, Ogawa K. Taurine dioxygenase (tauD)-independent taurine assimilation in Escherichia coli. Microbiology (Reading) 2018; 164:1446–1456 [View Article] [PubMed]
    [Google Scholar]
  31. Iwanicka-Nowicka R, Hryniewicz MM. A new gene, cbl, encoding A member of the LysR family of transcriptional regulators belongs to Escherichia coli cys regulon. Gene 1995; 166:11–17 [View Article] [PubMed]
    [Google Scholar]
  32. van der Ploeg JR, Iwanicka-Nowicka R, Kertesz MA, Leisinger T, Hryniewicz MM. Involvement of CysB and Cbl regulatory proteins in expression of the tauABCD operon and other sulfate starvation-inducible genes in Escherichia coli. J Bacteriol 1997; 179:7671–7678 [View Article] [PubMed]
    [Google Scholar]
  33. van Der Ploeg JR, Iwanicka-Nowicka R, Bykowski T, Hryniewicz MM, Leisinger T. The Escherichia coli ssuEADCB gene cluster is required for the utilization of sulfur from aliphatic sulfonates and is regulated by the transcriptional activator Cbl. J Biol Chem 1999; 274:29358–29365 [View Article] [PubMed]
    [Google Scholar]
  34. Bykowski T, van der Ploeg JR, Iwanicka-Nowicka R, Hryniewicz MM. The switch from inorganic to organic sulphur assimilation in Escherichia coli: adenosine 5’-phosphosulphate (APS) as a signalling molecule for sulphate excess. Mol Microbiol 2002; 43:1347–1358 [View Article] [PubMed]
    [Google Scholar]
  35. Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 2000; 97:6640–6645 [View Article] [PubMed]
    [Google Scholar]
  36. Datta S, Costantino N, Court DL. A set of recombineering plasmids for gram-negative bacteria. Gene 2006; 379:109–115 [View Article]
    [Google Scholar]
  37. Cherepanov PP, Wackernagel W. Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 1995; 158:9–14 [View Article]
    [Google Scholar]
  38. Miller JH. Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 1972
    [Google Scholar]
  39. Jacobson BL, He JJ, Vermersch PS, Lemon DD, Quiocho FA. Engineered interdomain disulfide in the periplasmic receptor for sulfate transport reduces flexibility. Site-directed mutagenesis and ligand-binding studies. J Biol Chem 1991; 266:5220–5225 [View Article]
    [Google Scholar]
  40. Stec E, Witkowska-Zimny M, Hryniewicz MM, Neumann P, Wilkinson AJ et al. Structural basis of the sulphate starvation response in E. coli: crystal structure and mutational analysis of the cofactor-binding domain of the Cbl transcriptional regulator. J Mol Biol 2006; 364:309–322 [View Article]
    [Google Scholar]
  41. Tyrrell R, Verschueren KH, Dodson EJ, Murshudov GN, Addy C et al. The structure of the cofactor-binding fragment of the LysR family member, CysB: a familiar fold with a surprising subunit arrangement. Structure 1997; 5:1017–1032 [View Article] [PubMed]
    [Google Scholar]
  42. Mittal M, Singh AK, Kumaran S. Structural and biochemical characterization of ligand recognition by CysB, the master regulator of sulfate metabolism. Biochimie 2017; 142:112–124 [View Article] [PubMed]
    [Google Scholar]
  43. Quan JA, Schneider BL, Paulsen IT, Yamada M, Kredich NM et al. Regulation of carbon utilization by sulfur availability in Escherichia coli and Salmonella typhimurium. Microbiology (Reading) 2002; 148:123–131 [View Article] [PubMed]
    [Google Scholar]
  44. Zimmer DP, Soupene E, Lee HL, Wendisch VF, Khodursky AB et al. Nitrogen regulatory protein C-controlled genes of Escherichia coli: scavenging as a defense against nitrogen limitation. Proc Natl Acad Sci U S A 2000; 97:14674–14679 [View Article] [PubMed]
    [Google Scholar]
  45. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2006; 2:1–11 [View Article] [PubMed]
    [Google Scholar]
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