Home LiteratureArticle Details
PMID: 18849444 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Synthesis and uptake of the compatible solutes ectoine and 5-hydroxyectoine by Streptomyces coelicolor A3(2) in response to salt and heat stresses.

Applied and environmental microbiology ·Vol. 74 ·No. 23 ·2008-12-00 ·Pages 7286-96

Bursy J, Kuhlmann AU, Pittelkow M, Hartmann H, Jebbar M, Pierik AJ, Bremer E

Abstract

Streptomyces coelicolor A3(2) synthesizes ectoine and 5-hydroxyectoine upon the imposition of either salt (0.5 M NaCl) or heat stress (39 degrees C). The cells produced the highest cellular levels of these compatible solutes when both stress conditions were simultaneously imposed. Protection against either severe salt (1.2 M NaCl) or heat stress (39 degrees C) or a combination of both environmental cues could be accomplished by adding low concentrations (1 mM) of either ectoine or 5-hydroxyectoine to S. coelicolor A3(2) cultures. The best salt and heat stress protection was observed when a mixture of ectoine and 5-hydroxyectoine (0.5 mM each) was provided to the growth medium. Transport assays with radiolabeled ectoine demonstrated that uptake was triggered by either salt or heat stress. The most effective transport and accumulation of [(14)C]ectoine by S. coelicolor A3(2) were achieved when both environmental cues were simultaneously applied. Our results demonstrate that the accumulation of the compatible solutes ectoine and 5-hydroxyectoine allows S. coelicolor A3(2) to fend off the detrimental effects of both high salinity and high temperature on cell physiology. We also characterized the enzyme (EctD) required for the synthesis of 5-hydroxyectoine from ectoine, a hydroxylase of the superfamily of the non-heme-containing iron(II)- and 2-oxoglutarate-dependent dioxygenases (EC 1.14.11). The gene cluster (ectABCD) encoding the enzymes for ectoine and 5-hydroxyectoine biosynthesis can be found in the genome of S. coelicolor A3(2), Streptomyces avermitilis, Streptomyces griseus, Streptomyces scabiei, and Streptomyces chrysomallus, suggesting that these compatible solutes play an important role as stress protectants in the genus Streptomyces.

MeSH Terms
Amino Acids, Diamino/metabolism Bacterial Proteins/genetics,metabolism Carbon Radioisotopes/metabolism Hot Temperature Hydrolases/genetics,isolation & purification,metabolism Metabolic Networks and Pathways Multigene Family Salts/metabolism Streptomyces coelicolor/drug effects,genetics,metabolism,radiation effects
Chemicals
Amino Acids, Diamino Bacterial Proteins Carbon Radioisotopes Salts hydroxyectoine ectoine Hydrolases
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Bursy Jan
Laboratory for Microbiology, Department of Biology, Philipps University Marburg, Marburg, Germany.
Kuhlmann Anne U
Pittelkow Marco
Hartmann Holger
Jebbar Mohamed
Pierik Antonio J
Bremer Erhard
References (73)
73 references, click to expand
  1. Osmosensing and osmoregulatory compatible solute accumulation by bacteria.
    Comp Biochem Physiol A Mol Integr Physiol. 2001 Oct;130(3):437-60 PMID: 11913457
  2. Inhibition of protein aggregation in vitro and in vivo by a natural osmoprotectant.
    Proc Natl Acad Sci U S A. 2006 Sep 5;103(36):13357-61 PMID: 16899544
  3. Enhanced trehalose production improves growth of Escherichia coli under osmotic stress.
    Appl Environ Microbiol. 2005 Jul;71(7):3761-9 PMID: 16000787
  4. Niche-specificity factors of a marine oil-degrading bacterium Alcanivorax borkumensis SK2.
    FEMS Microbiol Lett. 2008 Aug;285(1):89-96 PMID: 18557784
  5. Functional expression of the ectoine hydroxylase gene (thpD) from Streptomyces chrysomallus in Halomonas elongata.
    Appl Environ Microbiol. 2004 May;70(5):3130-2 PMID: 15128576
  6. Stabilization of Enzymes against Thermal Stress and Freeze-Drying by Mannosylglycerate.
    Appl Environ Microbiol. 1997 Oct;63(10):4020-5 PMID: 16535713
  7. Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate.
    FEMS Microbiol Rev. 2000 Jul;24(3):263-90 PMID: 10841973
  8. Role of Ngamma-acetyldiaminobutyrate as an enzyme stabilizer and an intermediate in the biosynthesis of hydroxyectoine.
    Appl Environ Microbiol. 1999 Sep;65(9):3774-9 PMID: 10473374
  9. Osmotically induced synthesis of the compatible solute hydroxyectoine is mediated by an evolutionarily conserved ectoine hydroxylase.
    J Biol Chem. 2007 Oct 26;282(43):31147-55 PMID: 17636255
  10. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2).
    Nature. 2002 May 9;417(6885):141-7 PMID: 12000953
  11. The chemical chaperone proline relieves the thermosensitivity of a dnaK deletion mutant at 42 degrees C.
    J Bacteriol. 2004 Dec;186(23):8149-52 PMID: 15547289
  12. Thermoprotection of Bacillus subtilis by exogenously provided glycine betaine and structurally related compatible solutes: involvement of Opu transporters.
    J Bacteriol. 2004 Mar;186(6):1683-93 PMID: 14996799
  13. Synthesis of the compatible solute ectoine in Virgibacillus pantothenticus is triggered by high salinity and low growth temperature.
    Appl Environ Microbiol. 2008 Jul;74(14):4560-3 PMID: 18487398
  14. Extrinsic protein stabilization by the naturally occurring osmolytes beta-hydroxyectoine and betaine.
    Extremophiles. 1999 Aug;3(3):191-8 PMID: 10484175
  15. The osmophobic effect: natural selection of a thermodynamic force in protein folding.
    J Mol Biol. 2001 Jul 27;310(5):955-63 PMID: 11502004
  16. Construction and characterization of an NaCl-sensitive mutant of Halomonas elongata impaired in ectoine biosynthesis.
    FEMS Microbiol Lett. 1998 Apr 15;161(2):293-300 PMID: 9570121
  17. Role of the glycine betaine and carnitine transporters in adaptation of Listeria monocytogenes to chill stress in defined medium.
    Appl Environ Microbiol. 2003 Dec;69(12):7492-8 PMID: 14660402
  18. Corynebacterium glutamicum is equipped with four secondary carriers for compatible solutes: identification, sequencing, and characterization of the proline/ectoine uptake system, ProP, and the ectoine/proline/glycine betaine carrier, EctP.
    J Bacteriol. 1998 Nov;180(22):6005-12 PMID: 9811661
  19. The Hsp70 and Hsp60 chaperone machines.
    Cell. 1998 Feb 6;92(3):351-66 PMID: 9476895
  20. The structure and biosynthesis of new tetrahydropyrimidine derivatives in actinomycin D producer Streptomyces parvulus. Use of 13C- and 15N-labeled L-glutamate and 13C and 15N NMR spectroscopy.
    J Biol Chem. 1988 Nov 5;263(31):16014-22 PMID: 2903148
  21. Characterization of the ectoine biosynthesis genes of haloalkalotolerant obligate methanotroph "Methylomicrobium alcaliphilum 20Z".
    Arch Microbiol. 2006 Jan;184(5):286-97 PMID: 16283251
  22. Induction of synthesis of tetrahydropyrimidine derivatives in Streptomyces strains and their effect on Escherichia coli in response to osmotic and heat stress.
    J Bacteriol. 1996 Jan;178(2):385-95 PMID: 8550457
  23. High survival and stability rates of Escherichia coli dried in hydroxyectoine.
    FEMS Microbiol Lett. 2004 Apr 15;233(2):347-52 PMID: 15063506
  24. Responses of Bacillus subtilis to hypotonic challenges: physiological contributions of mechanosensitive channels to cellular survival.
    Appl Environ Microbiol. 2008 Apr;74(8):2454-60 PMID: 18310427
  25. Glycine betaine-assisted protein folding in a lysA mutant of Escherichia coli.
    J Biol Chem. 2000 Jan 14;275(2):1050-6 PMID: 10625645
  26. DNA helix destabilization by proline and betaine: possible role in the salinity tolerance process.
    FEBS Lett. 1997 Jun 30;410(2-3):201-5 PMID: 9237629
  27. The role of LRP and H-NS in transcription regulation: involvement of synergism, allostery and macromolecular crowding.
    J Mol Biol. 2007 Feb 23;366(3):900-15 PMID: 17196617
  28. Genome sequence of the streptomycin-producing microorganism Streptomyces griseus IFO 13350.
    J Bacteriol. 2008 Jun;190(11):4050-60 PMID: 18375553
  29. Salt stress control of intracellular solutes in streptomycetes indigenous to saline soils.
    Appl Environ Microbiol. 1984 Feb;47(2):301-6 PMID: 16346472
  30. Structure of human phytanoyl-CoA 2-hydroxylase identifies molecular mechanisms of Refsum disease.
    J Biol Chem. 2005 Dec 9;280(49):41101-10 PMID: 16186124
  31. An overview of the role and diversity of compatible solutes in Bacteria and Archaea.
    Adv Biochem Eng Biotechnol. 1998;61:117-53 PMID: 9670799
  32. Compatible solute influence on nucleic acids: many questions but few answers.
    Saline Systems. 2008 Jun 03;4:6 PMID: 18522725
  33. Role of trehalose in growth at high temperature of Salmonella enterica serovar Typhimurium.
    J Bacteriol. 2001 Jun;183(11):3365-71 PMID: 11344144
  34. Characterization of genes for the biosynthesis of the compatible solute ectoine from Marinococcus halophilus and osmoregulated expression in Escherichia coli.
    Microbiology. 1997 Apr;143 ( Pt 4):1141-9 PMID: 9141677
  35. Growth phase-dependent switch in osmolyte strategy in a moderate halophile: ectoine is a minor osmolyte but major stationary phase solute in Halobacillus halophilus.
    Environ Microbiol. 2008 Mar;10(3):716-26 PMID: 18093162
  36. A molecular mechanism for osmolyte-induced protein stability.
    Proc Natl Acad Sci U S A. 2006 Sep 19;103(38):13997-4002 PMID: 16968772
  37. Ectoine and hydroxyectoine inhibit aggregation and neurotoxicity of Alzheimer's beta-amyloid.
    FEBS Lett. 2005 Aug 29;579(21):4775-80 PMID: 16098972
  38. Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments.
    Arch Microbiol. 1998 Oct;170(5):319-30 PMID: 9818351
  39. The stabilization of proteins by osmolytes.
    Biophys J. 1985 Mar;47(3):411-4 PMID: 3978211
  40. Small stress molecules inhibit aggregation and neurotoxicity of prion peptide 106-126.
    Biochem Biophys Res Commun. 2008 Jan 25;365(4):808-13 PMID: 18039468
  41. Inhibition of insulin amyloid formation by small stress molecules.
    FEBS Lett. 2004 Apr 23;564(1-2):121-5 PMID: 15094052
  42. Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis.
    Nat Biotechnol. 2003 May;21(5):526-31 PMID: 12692562
  43. Osmotically regulated synthesis of the compatible solute ectoine in Bacillus pasteurii and related Bacillus spp.
    Appl Environ Microbiol. 2002 Feb;68(2):772-83 PMID: 11823218
  44. Complex regulation of the synthesis of the compatible solute ectoine in the halophilic bacterium Chromohalobacter salexigens DSM 3043T.
    Microbiology. 2004 Sep;150(Pt 9):3051-63 PMID: 15347763
  45. Isolation and characterization of salt-sensitive mutants of the moderate halophile Halomonas elongata and cloning of the ectoine synthesis genes.
    J Biol Chem. 1997 Oct 10;272(41):25794-801 PMID: 9325308
  46. Thermostabilization of proteins by diglycerol phosphate, a new compatible solute from the hyperthermophile Archaeoglobus fulgidus.
    Appl Environ Microbiol. 2000 May;66(5):1974-9 PMID: 10788369
  47. Role of ectoine in Vibrio cholerae osmoadaptation.
    Appl Environ Microbiol. 2003 Oct;69(10):5919-27 PMID: 14532045
  48. Dicarboxylic amino acids and glycine-betaine regulate chaperone-mediated protein-disaggregation under stress.
    Mol Microbiol. 2003 Jul;49(2):401-10 PMID: 12828638
  49. Marinococcus halophilus DSM 20408T encodes two transporters for compatible solutes belonging to the betaine-carnitine-choline transporter family: identification and characterization of ectoine transporter EctM and glycine betaine transporter BetM.
    Extremophiles. 2004 Jun;8(3):175-84 PMID: 14872322
  50. Osmoprotection of Escherichia coli by ectoine: uptake and accumulation characteristics.
    J Bacteriol. 1992 Aug;174(15):5027-35 PMID: 1629159
  51. Characterization of the genes for the biosynthesis of the compatible solute ectoine in the moderately halophilic bacterium Halomonas elongata DSM 3043.
    Syst Appl Microbiol. 1998 Dec;21(4):487-97 PMID: 9924816
  52. Specialized roles of the two pathways for the synthesis of mannosylglycerate in osmoadaptation and thermoadaptation of Rhodothermus marinus.
    J Biol Chem. 2004 Mar 12;279(11):9892-8 PMID: 14701859
  53. Characterization of biosynthetic enzymes for ectoine as a compatible solute in a moderately halophilic eubacterium, Halomonas elongata.
    J Bacteriol. 1999 Jan;181(1):91-9 PMID: 9864317
  54. New type of osmoregulated solute transporter identified in halophilic members of the bacteria domain: TRAP transporter TeaABC mediates uptake of ectoine and hydroxyectoine in Halomonas elongata DSM 2581(T).
    J Bacteriol. 2002 Jun;184(11):3078-85 PMID: 12003950
  55. Hydroxyectoine is superior to trehalose for anhydrobiotic engineering of Pseudomonas putida KT2440.
    Appl Environ Microbiol. 2002 Sep;68(9):4328-33 PMID: 12200283
  56. Chemical chaperones regulate molecular chaperones in vitro and in cells under combined salt and heat stresses.
    J Biol Chem. 2001 Oct 26;276(43):39586-91 PMID: 11517217
  57. Comparative study of the thermostabilizing properties of mannosylglycerate and other compatible solutes on model enzymes.
    Extremophiles. 2002 Jun;6(3):209-16 PMID: 12072956
  58. Three transport systems for the osmoprotectant glycine betaine operate in Bacillus subtilis: characterization of OpuD.
    J Bacteriol. 1996 Sep;178(17):5071-9 PMID: 8752321
  59. Isolation and characterization of salt-sensitive mutants of the moderately halophilic bacterium Salinivibrio costicola subsp. yaniae.
    Biosci Biotechnol Biochem. 2008 Aug;72(8):1977-82 PMID: 18685202
  60. Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures.
    Proc Natl Acad Sci U S A. 2002 Jul 23;99(15):9727-32 PMID: 12105274
  61. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  62. Compatible-solute-supported periplasmic expression of functional recombinant proteins under stress conditions.
    Appl Environ Microbiol. 2000 Apr;66(4):1572-9 PMID: 10742244
  63. Thermoprotection by glycine betaine and choline.
    Microbiology. 1999 Sep;145 ( Pt 9):2543-8 PMID: 10517607
  64. Glycine betaine confers enhanced osmotolerance and cryotolerance on Listeria monocytogenes.
    J Bacteriol. 1994 Jan;176(2):426-31 PMID: 8288538
  65. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  66. Responses of E. coli to osmotic stress: large changes in amounts of cytoplasmic solutes and water.
    Trends Biochem Sci. 1998 Apr;23(4):143-8 PMID: 9584618
  67. The conformation of new tetrahydropyrimidine derivatives in solution and in the crystal.
    Eur J Biochem. 1993 Jun 15;214(3):897-906 PMID: 8319696
  68. Chill induction of the SigB-dependent general stress response in Bacillus subtilis and its contribution to low-temperature adaptation.
    J Bacteriol. 2003 Aug;185(15):4305-14 PMID: 12867438
  69. The ectD gene, which is involved in the synthesis of the compatible solute hydroxyectoine, is essential for thermoprotection of the halophilic bacterium Chromohalobacter salexigens.
    J Bacteriol. 2006 Jun;188(11):3774-84 PMID: 16707670
  70. Characterization of the synthetic compatible solute homoectoine as a potent PCR enhancer.
    Biochem Biophys Res Commun. 2004 Sep 24;322(3):867-72 PMID: 15336543
  71. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  72. Trehalose synthesis genes are controlled by the putative sigma factor encoded by rpoS and are involved in stationary-phase thermotolerance in Escherichia coli.
    J Bacteriol. 1991 Dec;173(24):7918-24 PMID: 1744047
  73. FeII/alpha-ketoglutarate-dependent hydroxylases and related enzymes.
    Crit Rev Biochem Mol Biol. 2004 Jan-Feb;39(1):21-68 PMID: 15121720
Article Info
Journal
Applied and environmental microbiology
Abbr.
Appl Environ Microbiol
ISSN
1098-5336
Published
2008-12-00
Epub
2008-00-10
Pages
7286-96
Language
English
Region
United States
NLM ID
7605801
PMCID
PMC2592907
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com