Extremophiles

, Volume 16, Issue 3, pp 437–446 | Cite as

Nmag_2608, an extracellular ubiquitin-like domain-containing protein from the haloalkaliphilic archaeon Natrialba magadii

  • María Victoria Ordóñez
  • Débora Nercessian
  • Rubén Danilo Conde
Original Paper

Abstract

Ubiquitin-like proteins (Ubls) and ubiquitin-like domain-containing proteins (Ulds) found in both eukaryotes and prokaryotes display an ubiquitin fold. We previously characterized a 124-amino acid polypeptide (P400) from the haloalkaliphilic archaeon Natrialba magadii having structural homology with ubiquitin family proteins. The reported N. magadii’s genome allowed the identification of the Nmag_2608 gene for the protein containing P400, which belongs to specific orthologs of halophilic organisms. It was found that Nmag_2608 has an N-terminal signal peptide with a lipobox motif characteristic of bacterial lipoproteins. Also, it presents partial identity with the ubiquitin-like domain-containing proteins, soluble ligand binding β-grasp proteins. Western blots and heterologous expression tests in E. coli evidenced that Nmag_2608 is processed and secreted outside the cell, where it could perform its function. The analysis of Nmag_2608 expression in N. magadii’s cells suggests a co-transcription with the adjoining Nmag_2609 gene encoding a protein of the cyclase family. Also, the transcript level decreased in cells grown in low salinity and starved. To conclude, this work reports for the first time an extracellular archaeal protein with an ubiquitin-like domain.

Keywords

Halophilic archaea Natrialba magadii Ubiquitin-like domains Extracellular proteins Protein–substrate interaction 

Supplementary material

792_2012_443_MOESM1_ESM.pdf (110 kb)
Supplementary material 1 (PDF 110 kb)

References

  1. Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–795PubMedCrossRefGoogle Scholar
  2. Burroughs AM, Balaji S, Iyer LM, Aravind L (2007a) Small but versatile: the extraordinary functional and structural diversity of the beta-grasp fold. Biol Direct 2:18. doi:10.1186/1745-6150-2-18 PubMedCrossRefGoogle Scholar
  3. Burroughs AM, Balaji S, Iyer LM, Aravind L (2007b) A novel superfamily containing the β-grasp fold involved in binding diverse soluble ligands. Biol Direct 2:4. doi:10.1186/1745-6150-2-4 PubMedCrossRefGoogle Scholar
  4. Ciechanover A (1994) The ubiquitin-proteasome proteolytic pathway. Cell 79:13–21PubMedCrossRefGoogle Scholar
  5. Ciechanover A, Iwai K (2004) The ubiquitin system: from basic mechanisms to the patient bed. IUBMB Life 56:193–201PubMedCrossRefGoogle Scholar
  6. Coker JA, DasSarma P, Kumar J, Müller JA, DasSarma S (2007) Transcriptional profiling of the model Archaeon Halobacterium sp. NRC-1: responses to changes in salinity and temperature. Saline Systems 3:6. doi:10.1186/1746-1448-3-6 PubMedCrossRefGoogle Scholar
  7. Cole C, Barber JD, Barton GJ (2008) The Jpred 3 secondary structure prediction server. Nucl Acids Res 36(Web Server issue):W197–W201. doi:10.1093/nar/gkn238
  8. Dobrovolskya VN, Bowyerb JF, Pabarcusc MK, Heflicha RH, Williamsd LD, Doerged DR, Arvidssone B, Bergquiste J, Casidac JE (2005) Effect of arylformamidase (kynurenine formamidase) gene inactivation in mice on enzymatic activity, kynurenine pathway metabolites and phenotype. Biochim Biophys Acta 1724:163–172CrossRefGoogle Scholar
  9. Downes BP, Saracco SA, Lee SS, Crowell DN, Vierstra RD (2006) MUBs, a family of ubiquitin-fold proteins that are plasma membrane-anchored by prenylation. J Biol Chem 281:27145–27157PubMedCrossRefGoogle Scholar
  10. Dye BT, Schulman BA (2007) Structural mechanisms underlying posttranslational modification by ubiquitin-like proteins. Annu Rev Biophys Biomol Struct 36:131–150PubMedCrossRefGoogle Scholar
  11. Giménez MI, Dilks K, Pohischröder M (2007) Haloferax volcanii twin-arginine translocation substates include secreted soluble, c-terminally anchored and lipoproteins. Mol Microbiol 66:1597–1606PubMedCrossRefGoogle Scholar
  12. Grabbe C, Dikic I (2009) Functional roles of ubiquitin-like domain (ULD) and ubiquitin-binding domain (UBD) containing proteins. Chem Rev 109:1481–1494PubMedCrossRefGoogle Scholar
  13. Hartmann-Petersen R, Gordon C (2004) Integral UBL domain proteins: a family of proteasome interacting proteins. Semin Cell Dev Biol 15:247–259PubMedCrossRefGoogle Scholar
  14. Hayashi S, Wu HC (1990) Lipoproteins in bacteria. J Bioenerg Biomembr 22:451–471PubMedCrossRefGoogle Scholar
  15. Helland R, Fjellbirkeland A, Karlsen OA, Ve T, Lillehaug JR, Jensen HB (2008) An oxidized tryptophan facilitates copper binding in Methylococcus capsulatus-secreted protein MopE. J Biol Chem 283:13897–13904PubMedCrossRefGoogle Scholar
  16. Hochstrasser M (2000) Evolution and function of ubiquitin-like protein-conjugation systems. Nat Cell Biol 2:53–157CrossRefGoogle Scholar
  17. Hochstrasser M (2009) Origin and function of ubiquitin-like proteins. Nature 458:422–429PubMedCrossRefGoogle Scholar
  18. Hulo N, Bairoch A, Bulliard V, Cerutti L, Cuche BA, de Castro E, Lachaize C, Langendijk-Genevaux PS, Sigrist CJA (2007) The 20 years of PROSITE. Nucl Acids Res 36:D245–D249PubMedCrossRefGoogle Scholar
  19. Humbard MA, Miranda HV, Lim J, Krause DJ, Pritz JR, Zhou G, Chen S, Wells L, Maupin-Furlow JA (2010) Ubiquitin-like small archaeal modifier proteins (SAMPs) in Haloferax volcanii. Nature 463:54–60PubMedCrossRefGoogle Scholar
  20. Iyer LM, Burroughs AM, Aravind L (2006) The prokaryotic antecedents of the ubiquitin-signaling system and the early evolution of ubiquitin-like beta-grasp domains. Genome Biol 7:R60. doi:10.1186/gb-2006-7-7-r60 PubMedCrossRefGoogle Scholar
  21. Jeong YJ, Jeong BC, Song HK (2011) Crystal structure of ubiquitin-like small archaeal modifier protein 1 (SAMP1) from Haloferax volcanii. Biochem Biophys Res Commun 405:112–117PubMedCrossRefGoogle Scholar
  22. Jones DT (1999) Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292:195–202PubMedCrossRefGoogle Scholar
  23. Keller U, Lang M, Crnovcic I, Pfennig F, Schauwecker F (2010) The actinomycin biosynthetic gene cluster of Streptomyces chrysomallus: a genetic hall of mirrors for synthesis of a molecule with mirror symmetry. J Bacteriol 192:2583–2595PubMedCrossRefGoogle Scholar
  24. Kerscher O, Felberbaum R, Hochstrasser M (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 22:159–180PubMedCrossRefGoogle Scholar
  25. Kiel C, Serrano L (2006) The ubiquitin domain superfold: structure-based sequence alignments and characterization of binding epitopes. J Mol Biol 355:821–844PubMedCrossRefGoogle Scholar
  26. Kurnasov O, Goral V, Colabroy K, Gerdes S, Anantha S, Osterman A, Begley TP (2003) NAD biosynthesis: identification of the tryptophan to quinolinate pathway in bacteria. Chem Biol 10:1195–1204PubMedCrossRefGoogle Scholar
  27. Lomovskaya N, Doi-katayama Y, Filippins S, Nastro C, Fonstein L, Gallo M, Colombo AL, Hutchinson CR (1998) The Streptomyces peucetius dpsY and dnrX genes govern early and late steps of daunorubicin and doxorubicin biosynthesis. J Bacteriol 180:2379–2386PubMedGoogle Scholar
  28. Madern D, Ebel C, Zaccai G (2000) Halophilic adaptation of enzymes. Extremophiles 4:91–98PubMedCrossRefGoogle Scholar
  29. Makarova KS, Koonin EV (2003) Comparative genomics of archaea: how much have we learned in six years, and what’s next? Genome Biol 4:115PubMedCrossRefGoogle Scholar
  30. Marquet A (2001) Enzymology of carbon-sulfur bond formation. Curr Opin Chem Biol 5:541–549PubMedCrossRefGoogle Scholar
  31. Mattar S, Scharf B, Kent SBH, Rodewald K, Oesterhelt D, Engelhard M (1994) The primary structure of halocyanin, an archaeal blue copper protein, predicts a lipid anchor for membrane fixation. J Biol Chem 269:14939–14945PubMedGoogle Scholar
  32. Matthijs S, Baysse C, Koedam N, Tehrani KA, Verheyden L, Budzikiewicz H, Schäfer M, Hoorelbeke B, Meyer JM, De Greve H, Cornelis P (2004) The Pseudomonas siderophore quinolobactin is synthesized from xanthurenic acid, an intermediate of the kynurenine pathway. Mol Microbiol 52:371–384PubMedCrossRefGoogle Scholar
  33. Mavromatis K, Chu K, Ivanova N, Hooper SD, Markowitz VM, Kyrpides NC (2009) Gene context analysis in the Integrated Microbial Genomes (IMG) data management system. PLoS One 4:e7979PubMedCrossRefGoogle Scholar
  34. Ming YZ, Di X, Gomez-Sanchez EP, Gomez-Sanchez CE (1994) Improved downward capillary transfer for blotting of DNA and RNA. Biotechniques 16:58–59PubMedGoogle Scholar
  35. Narui K, Noguchi N, Saito A, Kakimi K, Motomura N, Kubo K, Takamoto S, Sasatsu M (2009) Anti-infectious activity of tryptophan metabolites in the l-tryptophan–l-kynurenine pathway. Biol Pharm Bull 32:41–44PubMedCrossRefGoogle Scholar
  36. Nercessian D, Marino Buslje C, Ordóñez MV, De Castro RE, Conde RD (2009) Presence of structural homologs of ubiquitin in haloalkaliphilic Archaea. Int Microbiol 12:167–173PubMedGoogle Scholar
  37. Ng SYM, Chaban B, VanDyke DJ, Jarrell KF (2007) Archaeal signal peptidases. Microbiology 153:305–314PubMedCrossRefGoogle Scholar
  38. Ordóñez MV, Guillén J, Nercessian D, Villalain J, Conde RD (2011) Secondary structure determination by FTIR of an archaeal ubiquitin-like polypeptide from Natrialba magadii. Eur Biophys J 40:1101–1107PubMedCrossRefGoogle Scholar
  39. Pabarcus MK, Casida JE (2005) Cloning, expression, and catalytic triad of recombinant Arylformamidase. Protein Expr Purif 44:39–44PubMedCrossRefGoogle Scholar
  40. Pickart CM (2001) Mechanisms underlying ubiquitination. Ann Rev Biochem 70:503–533PubMedCrossRefGoogle Scholar
  41. Ranjan N, Damberger FF, Sutter M, Allain FHT, Weber-Ban E (2011) Solution structure and activation mechanism of ubiquitin-like small archaeal modifier proteins. J Mol Biol 405:1040–1055PubMedCrossRefGoogle Scholar
  42. Rudolph MJ, Wuebbens MM, Rajagopalan KV, Schindelin H (2001) Crystal structure of molybdopterin synthase and its evolutionary relationship to ubiquitin activation. Nat Struct Biol 8:42–46PubMedCrossRefGoogle Scholar
  43. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1987) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85CrossRefGoogle Scholar
  44. Soppa J (2006) From genomes to function: haloarchaea as model organisms. Microbiology 152:585–590PubMedCrossRefGoogle Scholar
  45. Storf S, Pfeiffer F, Dilks K, Chen ZQ, Imam S, Pohlschröder M (2010) Mutational and bioinformatic analysis of haloarchaeal lipobox-containing proteins. Archaea. doi:10.1155/2010/410975 PubMedGoogle Scholar
  46. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680PubMedCrossRefGoogle Scholar
  47. Tindall BJ, Ross HN, Grant WD (1984) Natronobacterium gen. nov. and Natronococcus gen. nov., two new genera of the haloalkaliphilic archaebacteria. Syst Appl Microbiol 5:41–57CrossRefGoogle Scholar
  48. Tokuda H, Matsuyama S (2004) Sorting of lipoproteins of the outer membrane in E. coli. Biochim Biophys Acta 1693:5–13PubMedCrossRefGoogle Scholar
  49. Wang C, Xi J, Begley TP, Nicholson LK (2001) Solution structure of ThiS and implications for the evolutionary roots of ubiquitin. Nat Struct Biol 8:47–51PubMedCrossRefGoogle Scholar
  50. Wang Z, Potter BM, Gray AM, Sacksteder KA, Geisbrecht BV, Laity JH (2007) The solution structure of antigen MPT64 from Mycobacterium tuberculosis defines a new family of beta-grasp proteins. J Mol Biol 366:375–381PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2012

Authors and Affiliations

  • María Victoria Ordóñez
    • 1
  • Débora Nercessian
    • 1
  • Rubén Danilo Conde
    • 1
  1. 1.Degradación de Proteínas, Instituto de Investigaciones Biológicas, Facultad de Ciencias Exactas y NaturalesUniversidad Nacional de Mar del Plata, CONICETMar del PlataArgentina

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