Origin and evolution of the unique tetra-domain hemoglobin from the hydrothermal vent scale worm branchipolynoe

Molecular Biology and Evolution

Volumn 27, Issue 1, 2010, Pages 143-152

  Projecto Garcia, J ^a,b   Zorn, N ^c   Jollivet, D ^a,b   Schaeffer, S W ^d   Lallier, F H ^a,b   Hourdez, S ^a,b  

^a STATION BIOLOGIQUE DE ROSCOFF   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c UNIVERSITÉ LOUIS PASTEUR   (France)

^d PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Annelids; Branchipolynoe; Evolution; Extracellular globins; Tandem duplication; Tetra domain

Indexed keywords

COMPLEMENTARY DNA; HEME; HEMOGLOBIN; OXYGEN;

AMINO ACID SEQUENCE; ARTICLE; ASCARIS SUUM; BRANCHIPOLYNOE; DNA SEQUENCE; EXON; GENE; GENE AMPLIFICATION; GENE DUPLICATION; GENE SEQUENCE; GENE STRUCTURE; GENETIC CODE; GLOBIN GENE; HYDROTHERMAL VENT; HYDROTHERMAL VENT SPECIES; INTRON; MOLECULAR CLONING; MOLECULAR EVOLUTION; NONHUMAN; PHYLOGENY; WORM;

AMINO ACID SEQUENCE; ANIMALS; CLONING, MOLECULAR; DNA, COMPLEMENTARY; EVOLUTION, MOLECULAR; GLOBINS; HEMOGLOBINS; INTRONS; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYCHAETA; PROMOTER REGIONS, GENETIC; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA;

ANNELIDA; ASCARIS SUUM; BRANCHIPOLYNOE; BRANCHIPOLYNOE SEEPENSIS; BRANCHIPOLYNOE SYMMYTILIDA; TETRA;

EID: 72649097302     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msp218     Document Type: Article

References (49)

1. Bailly X, Chabasse C, Hourdez S, Dewilde S, Moens L, Zal F. 2007. Globin gene family evolution and functional diversification in annelids. FEBS J. 274:2641-2652.
2. Bailly X, Leroy R, Carney S, Collin O, Zal F, Toulmond A, Jollivet D. 2003. The loss of the hemoglobin H2S-binding function in annelids from sulfide-free habitats reveals molecular adaptation driven by Darwinian positive selection. Proc Natl Acad Sci USA. 100:5885-5890.
3. Chae JH, Kim CG. 2003. CP2 binding to the promoter is essential for the enhanced transcription of globin genes in erythroid cells. Mol Cells. 15:40-47.
4. Darawshe S, Tsafadyah Y, Daniel E. 1987. Quaternary structure of erythrocruorin from the nematode Ascaris suum. Biochem J. 242:689-694.
5. De Baere I, Liu L, Moens L, Van Beeumen J, Gielens C, Richelle J, Trotman C, Finch J, Gerstein M, Perutz M. 1992. Polar zipper sequence in the high-affinity hemoglobin of Ascaris suum: amino acid sequence and structural interpretation. Proc Natl Acad Sci USA. 89:4638-4642.
6. De Baere I, Perutz MF, Kiger L, Marden MC, Poyart C. 1994. Formation of two hydrogen bonds from the globin to the heme-linked oxygen molecule in Ascaris hemoglobin. Proc Natl Acad Sci USA. 91:1594-1597.
7. De Maria R, Zeuner A, Eramo A, Domenichelli C, Bonci D, Grignani F, Srinivasula SM, Alnemri ES, Testa U, Peschle C. 1999. Negative regulation of erythropoiesis by caspase-mediated cleavage of GATA-1. Nature. 401:489-493.
8. Dewilde S, Blaxter M, Van Hauwaert M-L, Vanfleteren J, Esmans EL, Marden M, Griffon N, Moens L. 1996. Globin and globin structure of the nerve myoglobin of Aphrodite aculeata. J Biol Chem. 271:19865-19870.
9. Dewilde S, Van Hauwaert M-L, Peeters K, Vanfleteren J, Moens L. 1999. Daphnia pulex didomain hemoglobin: structure and evolution of polymeric hemoglobins and their coding genes. Mol Biol Evol. 16:1208-1218.
10. Dixon B, Walker B, Kimmins W, Pohajdak B. 1992. A nematode gene contains an intron previously thought to be unique to plants. J Mol Evol. 35:131-136.
11. Flores JF, Fisher CR, Carney SL, Green BN, Freytag JK, Schaeffer SW, Royer Jr WE. 2005. Sulfide binding is mediated by zinc ions discovered in the crystal structure of a hydrothermal vent tubeworm hemoglobin. Proc Natl Acad Sci USA. 102: 2713-2718.
12. Flores JF, Hourdez S. 2006. The zinc-mediated sulfide-binding mechanism of hydrothermal vent tubeworm 400-kDa hemoglobin. Cah Biol Mar. 47:371-377.
13. Goldman N, Yang Z. 1994. A codon based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol. 11:725-736.
14. Goodman M, Pedwaydon J, Czelusniak J, Suzuki T, Gotoh T, Moens L, Shishikura F, Walz D, Vinogradov SN. 1988. An evolutionary tree for invertebrate globin sequences. J Mol Evol. 27:236-249.
15. Grinich NP, Terwilliger RC. 1980. The quaternary structure of an unusual high-molecular-weight intracellular hemoglobin from the bivalve mollusc Barbatia reeveana. Biochem J. 189:1-8.
16. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 52:696-704.
17. Guindon S, Lethiec F, Duroux P, Gascuel O. 2005. PHYML Online-a web server for fast maximum likelihood-based phylogenetic inference. Nucl Acids Res. 33:W557-W559.
18. Hourdez S, Lallier FH. 2007. Adaptations to hypoxia in hydrothermal vent and cold-seep invertebrates. Rev Env Sci Biotech. 6:143-159.
19. Hourdez S, Lallier FH, Green BN, Toulmond A. 1999. Hemoglobins from deep-sea hydrothermal vent scale-worms of the genus Branchipolynoe: a new type of quaternary structure. Proteins. 34:427-434.
20. Hourdez S, Lallier FH, Martin-Jézéquel V, Weber RE, Toulmond A. 1999. Characterization and functional properties of the extracellular coelomic hemoglobins from the deep-sea, hydro-thermal vent scale-worm Branchipolynoe symmytilida. Proteins. 34:435-442.
21. Hourdez S, Weber RE. 2005. Molecular and functional adaptations in deep-sea hemoglobins. J Inorg Biochem. 99(1):130-141.
22. Huelsenbeck JP, Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 17:754-755.
23. Kato K, Tokishita S-i, Mandokoro Y, Kimura S, Ohta T, Kobayashi M, Yamagata H. 2001. Two-domain hemoglobin gene of the water flea Moina macrocopa: duplication in the ancestral Cladocera, diversification, and loss of a bridge intron. Gene. 273:41-50.
24. Krantz SB. 1991. Erythropoietin. Blood. 77(3):419-434.
25. Larkin MA, Blackshields G, Brown NP, et al. (13 co-authors). 2007. Clustal W and Clustal X version 2.0. Bioinformatics. 23: 2947-2948.
26. Lieb B, Todt C. 2008. Hemocyanin in mollusks-a molecular survey and new data on hemocyanin genes in Solenogastres and Caudofoveata. Mol Phylogenet Evol. 49:382-385.
27. Manning A, Trotman C, Tate W. 1990. Evolution of a polymeric globin in the brine shrimp Artemia. Nature. 348:653-656.
28. Mansfield BC, Krissansen GW, Smith MG, Tate WP. 1980. Isolation of intact larval haemoglobin from the brine shrimp Artemia salina. Prevention of degradation in vitro by proteases induced during larval development. Biochem Biophys Acta. 623:163-170.
29. Mishra RN, Singla-Pareek SL, Nair S, Sopory SK, Reddy MK. 2002. Directional genome walking using PCR. BioTechniques. 33:830-834.
30. Naito Y, Riggs C, Vandergon T, Riggs A. 1991. Origin of a "bridge" intron in the gene for two domain globin. Proc Natl Acad Sci USA. 88:6672-6676.
31. Posada D. 2008. jModelTest: phylogenetic averaging. Mol Biol Evol. 25:1253-1256.
32. Riggs AF. 1991. Aspects of the origin and evolution of non-vertebrate hemoglobins. Am Zool. 31:535-545.
33. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 19:1572-1574.
34. Saitou N, Nei M. 1987. The neighbor-joining method: a nem method for reconstructing phylogenetic trees. Mol Biol Evol. 4:406-425.
35. Sambrook J, Fritsch EF, Maniatis T. 1989. In: Nolan C, editor. Molecular cloning: a laboratory manual. Cold Springs Harbor Press, Cold Spring Harbour, NY.
36. Sherman DR, Kloek AP, Krishnan BR, Guinn B. 1992. Ascaris hemoglobin gene: plant-like structure reflects the ancestral globin gene. Proc Natl Acad Sci USA. 89:11696-11700.
37. Shi X, Karkut T, Chahmanhkah M, Alting-Mees M, Hemmingsen SM, Hegedus D. 2002. 5#-RACEing across a bridging oligonucleotide. Biotechniques. 32:480-482.
38. Suzuki T, Arita T. 1995. Two-domain hemoglobin from the blood clam, Barbatia lima. The cDNA-derived amino acid sequence. J Protein Chem. 14(7):499-502.
39. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol. 24:1596-1599.
40. Terwilliger NB. 1992. Molecular structure of the extracellular heme proteins. Vol.13. In: Mangum CP, editor. Advances in comparative and environmental physiology. blood and tissue oxygen carriers. Spriger-Verlag, Berlin, Heidelberg (Germany).p. 459.
41. Terwilliger NB. 1998. Functional adaptations of oxygen-transport proteins. J Exp Biol. 201:1085-1098.
42. Trotman C, Manning A, Bray J, Jellie A, Moens L, Tate W. 1994. Interdomain linkage in the polymeric hemoglobin molecule of Artemia. J Mol Evol. 38:628-636.
43. Tunnicliffe V. 1991. The biology of hydrothermal vents: ecology and evolution. Oceanogr Mar Biol. 29:319-407.
44. Weber RE. 1978. Respiratory pigments. Physiology of Annelids Mill PJ London: Academic Press Inc.
45. Weber RE, Vinogradov SN. 2001. Nonvertebrate hemoglobins: functions and molecular adaptations. Physiol Rev. 81:569-628.
46. Yang J, Kloek A, Goldberg D, Mathews F. 1995. The structure of ° Ascaris hemoglobin domain I at 2.2 A resolution: molecular features of oxygen avidity. Proc Natl Acad Sci USA. 92: 4224-4228.
47. Yang Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput App BioSci. 13: 555-556.
48. Zal F, Leize E, Lallier FH, Toulmond A, Van Dorsselaer A, Childress J. 1998. S-Sulfohemoglobin and disulfide exchange: the mecha-nisms of sulfide binding by Riftia pachyptila hemoglobins. Proc Natl Acad Sci USA. 95:8997-9002.
49. Zon LI, Youssoufian H, Mather C, Lodish HF, Orkin S. 1991. Activation of the erythropoietin receptor promoter by transcription factor GATA-1. Proc Natl Acad Sci USA. 88:10638-10641.