Journal of Structural and Functional Genomics

, Volume 14, Issue 3, pp 119–126 | Cite as

Solution NMR structures provide first structural coverage of the large protein domain family PF08369 and complementary structural coverage of dark operative protochlorophyllide oxidoreductase complexes

  • Surya V. S. R. K. Pulavarti
  • Yunfen He
  • Erik A. Feldmann
  • Alexander Eletsky
  • Thomas B. Acton
  • Rong Xiao
  • John K. Everett
  • Gaetano T. Montelione
  • Michael A. Kennedy
  • Thomas Szyperski
Article
  • 169 Downloads

Abstract

High-quality NMR structures of the C-terminal domain comprising residues 484–537 of the 537-residue protein Bacterial chlorophyll subunit B (BchB) from Chlorobium tepidum and residues 9–61 of 61-residue Asr4154 from Nostoc sp. (strain PCC 7120) exhibit a mixed α/β fold comprised of three α-helices and a small β-sheet packed against second α-helix. These two proteins share 29 % sequence similarity and their structures are globally quite similar. The structures of BchB(484–537) and Asr4154(9–61) are the first representative structures for the large protein family (Pfam) PF08369, a family of unknown function currently containing 610 members in bacteria and eukaryotes. Furthermore, BchB(484–537) complements the structural coverage of the dark-operating protochlorophyllide oxidoreductase.

Keywords

BchB DPOR Asr4154 PF08369 PCP-red Structural genomics 

Abbreviations

BchB

Bacterial chlorophyll subunit B

BchN

Bacterial chlorophyll subunit N

ChlN

Chlorophyll subunit N

ChlB

Chlorophyll subunit B

DPOR

Dark-operative protochlorophyllide oxidoreductase

DSS

4,4-Dimethyl-4-silapentane-1-sulfonate sodium salt

DTT

Dithiothreitol

MES

2-(N-morpholino)ethanesulfonic acid

NESG

Northeast Structural Genomics Consortium

NOE

Nuclear overhauser effect

PCP-red

Protochlorophyllide reductase

PDB

Protein Data Bank

RMSD

Root mean square deviation

Supplementary material

10969_2013_9159_MOESM1_ESM.pdf (1 mb)
Supplementary material 1 (PDF 1,040 kb)

References

  1. 1.
    Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer ELL, Eddy SR, Bateman A (2010) The Pfam protein families database. Nucleic Acids Res 38:D211–D222PubMedCrossRefGoogle Scholar
  2. 2.
    Reinbothe C, Bakkouri ME, Buhr F, Muraki N, Nomata J, Kurisu G, Fujita Y, Reinbothe S (2010) Chlorophyll biosynthesis: spotlight on protochlorophyllide reduction. Trends Plant Sci 15:614–624PubMedCrossRefGoogle Scholar
  3. 3.
    Bröcker MJ, Virus S, Ganskow S, Heathcote P, Heinz DW, Schubert WD, Jahn D, Moser J (2008) ATP-driven reduction by dark-operative protochlorophyllide oxidoreductase from Chlorobium tepidum mechanistically resembles nitrogenase catalysis. J Biol Chem 283:10559–10567PubMedCrossRefGoogle Scholar
  4. 4.
    Sarma R, Barney BM, Hamilton TL, Jones A, Seefeldt LC, Peters JW (2008) Crystal structure of the L protein of Rhodobacter sphaeroides light-independent protochlorophyllide reductase with MgADP bound: a homologue of the nitrogenase Fe protein. Biochemistry 47:13004–13015PubMedCrossRefGoogle Scholar
  5. 5.
    Bröcker MJ, Schomburg S, Heinz DW, Jahn D, Schubert WD, Moser J (2010) Crystal structure of the nitrogenase-like dark operative protochlorophyllide oxidoreductase catalytic complex (ChlN/ChlB)2. J Biol Chem 285:27336–27345PubMedCrossRefGoogle Scholar
  6. 6.
    Muraki N, Nomata J, Ebata K, Mizoguchi T, Shiba T, Tamiaki H, Kurisu G, Fujita Y (2010) X-ray crystal structure of the light-independent protochlorophyllide reductase. Nature 465:110–114PubMedCrossRefGoogle Scholar
  7. 7.
    Moser J, Lange C, Krausze J, Rebelein J, Schubert WD, Ribbe MW, Heinz DW, Jahn D (2013) Structure of ADP-aluminium fluoride-stabilized protochlorophyllide oxidoreductase complex. Proc Natl Acad Sci USA 110:2094–2098PubMedCrossRefGoogle Scholar
  8. 8.
    Dessailly BH, Nair R, Jaroszewski L, Fajardo JE, Kouranov A, Lee D, Fiser A, Godzik A, Rost B, Orengo C (2009) PSI-2: structural genomics to cover protein domain family space. Structure 17:869–881PubMedCrossRefGoogle Scholar
  9. 9.
    Liu JF, Montelione GT, Rost B (2007) Novel leverage of structural genomics. Nat Biotechnol 25:850–853Google Scholar
  10. 10.
    Acton TB, Gunsalus KC, Xiao R, Ma LC, Aramini J, Baran MC, Chiang YW, Climent T, Cooper B, Denissova NG, Douglas SM, Everett JK, Ho CK, Macapagal D, Rajan PK, Shastry R, Shih LY, Swapna GVT, Wilson M, Wu M, Gerstein M, Inouye M, Hunt JF, Montelione GT (2005) Robotic cloning and protein production platform of the Northeast Structural Genomics Consortium. Methods Enzymol 394:210–243PubMedCrossRefGoogle Scholar
  11. 11.
    Acton TB, Xiao R, Anderson S, Aramini J, Buchwald WA, Ciccosanti C, Conover K, Everett J, Hamilton K, Huang YJ, Janjua H, Kornhaber G, Lau J, Lee DY, Liu GH, Maglaqui M, Ma LC, Mao L, Patel D, Rossi P, Sahdev S, Shastry R, Swapna GVT, Tang YF, Tong SC, Wang DY, Wang H, Zhao L, Montelione GT (2011) Preparation of protein samples for NMR structure, function, and small-molecule screening studies. Methods Enzymol 493:21–60PubMedCrossRefGoogle Scholar
  12. 12.
    Xiao R, Anderson S, Aramini J, Belote R, Buchwald WA, Ciccosanti C, Conover K, Everett JK, Hamilton K, Huang YJ, Janjua H, Jiang M, Kornhaber GJ, Lee DY, Locke JY, Ma LC, Maglaqui M, Mao L, Mitra S, Patel D, Rossi P, Sahdev S, Sharma S, Shastry R, Swapna GVT, Tong SN, Wang D, Wang H, Zhao L, Montelione GT, Acton TB (2010) The high-throughput protein sample production platform of the Northeast Structural Genomics Consortium. J Struct Biol 172:21–33PubMedCrossRefGoogle Scholar
  13. 13.
    Neri D, Szyperski T, Otting G, Senn H, Wuethrich K (1989) Stereospecific nuclear magnetic resonance assignments of the methyl groups of valine and leucine in the DNA-binding domain of the 434 repressor by biosynthetically directed fractional 13C labeling. Biochemistry 28:7510–7516PubMedCrossRefGoogle Scholar
  14. 14.
    Moseley HNB, Monleon D, Montelione GT (2001) Automatic determination of protein backbone resonance assignments from triple resonance nuclear magnetic resonance data. Methods Enzymol 339:91–108PubMedCrossRefGoogle Scholar
  15. 15.
    Zimmerman DE, Kulikowski CA, Huang YP, Feng WQ, Tashiro M, Shimotakahara S, Chien CY, Powers R, Montelione GT (1997) Automated analysis of protein NMR assignments using methods from artificial intelligence. J Mol Biol 269:592–610PubMedCrossRefGoogle Scholar
  16. 16.
    Bahrami A, Assadi AH, Markley JL, Eghbalnia HR (2009) Probabilistic interaction network of evidence algorithm and its application to complete labeling of peak lists from protein NMR spectroscopy. PLoS Comput Biol 5:e1000307PubMedCrossRefGoogle Scholar
  17. 17.
    Moseley HNB, Sahota G, Montelione GT (2004) Assignment validation software suite for the evaluation and presentation of protein resonance assignment data. J Biomol NMR 28:341–355PubMedCrossRefGoogle Scholar
  18. 18.
    Huang YJ, Powers R, Montelione GT (2005) Protein NMR recall, precision, and F-measure scores (RPF scores): structure quality assessment measures based on information retrieval statistics. J Am Chem Soc 127:1665–1674PubMedCrossRefGoogle Scholar
  19. 19.
    Liu G, Shen Y, Atreya HS, Parish D, Shao Y, Sukumaran DK, Xiao R, Yee A, Lemak A, Bhattacharya A, Acton TA, Arrowsmith CH, Montelione GT, Szyperski T (2005) NMR data collection and analysis protocol for high-throughput protein structure determination. Proc Natl Acad Sci USA 102:10487–10492PubMedCrossRefGoogle Scholar
  20. 20.
    Güntert P, Mumenthaler C, Wüthrich K (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J Mol Biol 273:283–298PubMedCrossRefGoogle Scholar
  21. 21.
    Herrmann T, Güntert P, Wüthrich K (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J Mol Biol 319:209–227PubMedCrossRefGoogle Scholar
  22. 22.
    Huang YJ, Tejero R, Powers R, Montelione GT (2006) A topology-constrained distance network algorithm for protein structure determination from NOESY data. Proteins 62:587–603PubMedCrossRefGoogle Scholar
  23. 23.
    Cornilescu G, Delaglio F, Bax A (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J Biomol NMR 13:289–302PubMedCrossRefGoogle Scholar
  24. 24.
    Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr Sect D: Biol Crystallogr 54:905–921CrossRefGoogle Scholar
  25. 25.
    Bhattacharya A, Tejero R, Montelione GT (2007) Evaluating protein structures determined by structural genomics consortia. Proteins 66:778–795PubMedCrossRefGoogle Scholar
  26. 26.
    Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
  27. 27.
    Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE (2000) The Protein Data Bank. Nucleic Acids Res 28:235–242PubMedCrossRefGoogle Scholar
  28. 28.
    Holm L, Sander C (1995) Dali: a network tool for protein structure comparison. Trends Biochem Sci 20:478–480PubMedCrossRefGoogle Scholar
  29. 29.
    Neuwald AF, Aravind L, Spouge JL, Koonin EV (1999) AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 9:27–43PubMedGoogle Scholar
  30. 30.
    Putnam CD, Clancy SB, Tsuruta H, Gonzalez S, Wetmur JG, Tainer JA (2001) Structure and mechanism of the RuvB holliday junction branch migration motor. J Mol Biol 311:297–310PubMedCrossRefGoogle Scholar
  31. 31.
    Petukhov M, Dagkessamanskaja A, Bommer M, Barrett T, Tsaneva I, Yakimov A, Quéval R, Shvetsov A, Khodorkovskiy M, Käs E, Grigoriev M (2012) Large-scale conformational flexibility determines the properties of AAA + TIP49 ATPases. Structure 20:1321–1331PubMedCrossRefGoogle Scholar
  32. 32.
    Nayal M, Honig B (2006) On the nature of cavities on protein surfaces: application to the identification of drug-binding sites. Proteins 63:892–906PubMedCrossRefGoogle Scholar
  33. 33.
    Petrey D, Fischer M, Honig B (2009) Structural relationships among proteins with different global topologies and their implications for function annotation strategies. Proc Natl Acad Sci USA 106:17377–17382PubMedCrossRefGoogle Scholar
  34. 34.
    Zhang QC, Deng L, Fisher M, Guan J, Honig B, Petrey D (2011) PredUs: a web server for predicting protein interfaces using structural neighbors. Nucleic Acids Res 39:W283–W287PubMedCrossRefGoogle Scholar
  35. 35.
    Zhang QC, Petrey D, Norel R, Honig BH (2010) Protein interface conservation across structure space. Proc Natl Acad Sci USA 107:10896–10901PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Surya V. S. R. K. Pulavarti
    • 1
    • 2
  • Yunfen He
    • 1
    • 2
  • Erik A. Feldmann
    • 3
    • 4
  • Alexander Eletsky
    • 1
    • 2
  • Thomas B. Acton
    • 5
    • 6
  • Rong Xiao
    • 5
    • 6
  • John K. Everett
    • 5
    • 6
  • Gaetano T. Montelione
    • 5
    • 6
    • 7
  • Michael A. Kennedy
    • 3
    • 4
  • Thomas Szyperski
    • 1
    • 2
  1. 1.Department of ChemistryThe State University of New York at BuffaloBuffaloUSA
  2. 2.Northeast Structural Genomics ConsortiumBuffaloUSA
  3. 3.Department of Chemistry and BiochemistryMiami UniversityOxfordUSA
  4. 4.Northeast Structural Genomics ConsortiumOxfordUSA
  5. 5.Center of Advanced Biotechnology and Medicine and Department of Molecular Biology and Biochemistry, RutgersThe State University of New JerseyPiscatawayUSA
  6. 6.Northeast Structural Genomics ConsortiumPiscatawayUSA
  7. 7.Department of Biochemistry and Molecular Biology, Robert Wood Johnson Medical SchoolUMDNJPiscatawayUSA

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