Skip to main content

The Phylogeny and Structural Properties of 2/2 Haemoglobins

  • Chapter
Dioxygen Binding and Sensing Proteins

Part of the book series: Protein Reviews ((PRON,volume 9))

Abstract

In 2002, Jonathan and Beatrice Wittenberg inspected the 42 protein sequences then known to belong to the lineage of truncated (two-on-two) globins. They pointed out that these proteins parted into three distinct phylogenetic groups. The classification allowed for the identification of essential residues surrounding the heme group and guided subsequent structural studies. It also provided clear targets for further experimental work and set the stage for analyses of gene history. In this chapter, the status of the two-on-two globin lineage is updated. It is shown that the 2002 observations withstand the test of additional sequences and structures. The two-on-two family, which has grown practically ten-fold since the original study, conforms to the group-specific mechanisms of ligand stabilisation and fold features anticipated in the seminal Wittenberg contribution.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Berenbrink, M. 2006. Evolution of vertebrate haemoglobins: Histidine side chains, specific buffer value and Bohr effect. Respir. Physiol. Neurobiol. 154:165–184.

    Article  PubMed  CAS  Google Scholar 

  • Bolognesi, M., Bordo, D., Rizzi, M., Tarricone, C., and Ascenzi, P. 1997. Nonvertebrate hemoglobins: structural bases for reactivity. Prog. Biophys. Mol. Biol. 68:29–68.

    Article  PubMed  CAS  Google Scholar 

  • Bolognesi, M., Rosano, C., Losso, R., Borassi, A., Rizzi, M., Wittenberg, J. B., Boffi, A., and Ascenzi, P. 1999. Cyanide binding to Lucina pectinata hemoglobin I and to sperm whale myoglobin: an x-ray crystallographic study. Biophys. J. 77:1093–1099.

    Article  PubMed  CAS  Google Scholar 

  • Bonamore, A., Ilari, A., Giangiacomo, L., Bellelli, A., Morea, V., and Boffi, A. 2005. A novel thermostable hemoglobin from the actinobacterium Thermobifida fusca. FEBS J. 272:4189–4201.

    Article  PubMed  CAS  Google Scholar 

  • Cole, S. T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., Gordon, S. V., Eiglmeier, K., Gas, S., Barry, C. E., 3rd, et al. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537–544.

    Article  PubMed  CAS  Google Scholar 

  • Couture, M., Chamberland, H., St-Pierre, B., Lafontaine, J., and Guertin, M. 1994. Nuclear genes encoding chloroplast hemoglobins in the unicellular green alga Chlamydomonas eugametos. Mol. Gen. Genet. 243:185–197.

    PubMed  CAS  Google Scholar 

  • Couture, M., Das, T. K., Lee, H. C., Peisach, J., Rousseau, D. L., Wittenberg, B. A., Wittenberg, J. B., and Guertin, M. 1999. Chlamydomonas chloroplast ferrous hemoglobin. Heme pocket structure and reactions with ligands. J. Biol. Chem. 274:6898–6910.

    Article  PubMed  CAS  Google Scholar 

  • Couture, M., Das, T. K., Savard, P. Y., Ouellet, Y., Wittenberg, J. B., Wittenberg, B. A., Rousseau, D. L., and Guertin, M. 2000. Structural investigations of the hemoglobin of the cyanobacterium Synechocystis PCC6803 reveal a unique distal heme pocket. Eur. J. Biochem. 267:4770–4780.

    Article  PubMed  CAS  Google Scholar 

  • Das, T. K., Weber, R. E., Dewilde, S., Wittenberg, J. B., Wittenberg, B. A., Yamauchi, K., Van Hauwaert, M. L., Moens, L., and Rousseau, D. L. 2000. Ligand binding in the ferric and ferrous states of Paramecium hemoglobin. Biochemistry 39:14330–14340.

    Article  PubMed  CAS  Google Scholar 

  • di Prisco, G., Eastman, J. T., Giordano, D., Parisi, E., and Verde, C. 2007. Biogeography and adaptation of Notothenioid fish: hemoglobin function and globin-gene evolution. Gene 398:143–155.

    Article  PubMed  CAS  Google Scholar 

  • Egawa, T., and Yeh, S.R. 2005. Structural and functional properties of hemoglobins from unicellular organisms as revealed by resonance Raman spectroscopy. J. Inorg. Biochem. 99:72–96.

    Article  PubMed  CAS  Google Scholar 

  • Giangiacomo, L., Ilari, A., Boffi, A., Morea, V., and Chiancone, E. 2005. The truncated oxygen-avid hemoglobin from Bacillus subtilis. X-ray structure and ligand binding properties. J. Biol. Chem. 280:9192–9202.

    Article  PubMed  CAS  Google Scholar 

  • Hamdane, D., Kiger, L., Dewilde, S., Green, B. N., Pesce, A., Uzan, J., Burmester, T., Hankeln, T., Bolognesi, M., Moens, L., et al. 2003. The redox state of the cell regulates the ligand binding affinity of human neuroglobin and cytoglobin. J. Biol. Chem. 278:51713–51721.

    Article  PubMed  CAS  Google Scholar 

  • Hill, D. R., Belbin, T. J., Thorsteinsson, M. V., Bassam, D., Brass, S., Ernst, A., Boger, P., Paerl, H., Mulligan, M. E., and Potts, M. 1996. GlbN (cyanoglobin) is a peripheral membrane protein that is restricted to certain Nostoc spp. J. Bacteriol. 178:6587–6598.

    PubMed  CAS  Google Scholar 

  • Ilari, A., Kjelgaard, P., von Wachenfeldt, C., Catacchio, B., Chiancone, E., and Boffi, A. 2007. Crystal structure and ligand binding properties of the truncated hemoglobin from Geobacillus stearothermophilus. Arch. Biochem. Biophys. 457:85–94.

    Article  PubMed  CAS  Google Scholar 

  • Iwaasa, H., Takagi, T., and Shikama, K. 1989. Protozoan myoglobin from Paramecium caudatum. Its unusual amino acid sequence. J. Mol. Biol. 208:355–358.

    Article  PubMed  CAS  Google Scholar 

  • Iwaasa, H., Takagi, T., and Shikama, K. 1990. Protozoan hemoglobin from Tetrahymena pyriformis. Isolation, characterization, and amino acid sequence. J. Biol. Chem. 265:8603–8609.

    PubMed  CAS  Google Scholar 

  • Kapp, O. H., Moens, L., Vanfleteren, J., Trotman, C. N., Suzuki, T., and Vinogradov, S. N. 1995. Alignment of 700 globin sequences: extent of amino acid substitution and its correlation with variation in volume. Protein Sci. 4:2179–2190.

    PubMed  CAS  Google Scholar 

  • Keilin, D., and Ryley, J. F. 1953. Haemoglobin in Protozoa. Nature 172:451.

    Article  PubMed  CAS  Google Scholar 

  • Kendrew, J. C., Bodo, G., Dintzis, H. M., Parrish, R. G., Wyckoff, H., and Phillips, D. C. 1958. A three-dimensional model of the myoglobin molecule obtained by x-ray analysis. Nature 181:662–666.

    Article  PubMed  CAS  Google Scholar 

  • Kendrew, J. C., Dickerson, R. E., Stranberg, B. E., Hart, R. G., Davies, D. R., Phillips, D. C., and Shore, V. C. 1960. Structure of Myoglobin. Three-dimensional Fourier synthesis at 2Ã…. resolution. Nature 185:422–427.

    Article  PubMed  CAS  Google Scholar 

  • Kraulis, P. 1991. MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24:946–950.

    Article  Google Scholar 

  • Kumar, S., Tamura, K., Jakobsen, I. B., and Nei, M. 2001. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245.

    Article  PubMed  CAS  Google Scholar 

  • Milani, M., Pesce, A., Nardini, M., Ouellet, H., Ouellet, Y., Dewilde, S., Bocedi, A., Ascenzi, P., Guertin, M., Moens, L., Friedman, J. M., Wittenberg, J.B., and Bolognesi, M. 2005. Structural bases for heme binding and diatomic ligand recognition in truncated hemoglobins. J. Inorg. Biochem. 99:97–109.

    Article  PubMed  CAS  Google Scholar 

  • Milani, M., Savard, P. Y., Ouellet, H., Ascenzi, P., Guertin, M., and Bolognesi, M. 2003. A TyrCDl/TrpG8 hydrogen bond network and a TyrB10TyrCD1 covalent link shape the heme distal site of Mycobacterium tuberculosis hemoglobin O. Proc. Natl. Acad. Sci. U.S.A. 100:5766–5771.

    Article  PubMed  CAS  Google Scholar 

  • Moens, L., Vanfleteren, J., Van de Peer, Y., Peeters, K., Kapp, O., Czeluzniak, J., Goodman, M., Blaxter, M., and Vinogradov, S. 1996. Globins in nonvertebrate species: dispersal by horizontal gene transfer and evolution of the structure-function relationships. Mol. Biol. Evol. 13:324–333.

    PubMed  CAS  Google Scholar 

  • Nardini, M., Pesce, A., Labarre, M., Richard, C., Bolli, A., Ascenzi, P., Guertin, M., and Bolognesi, M. 2006. Structural determinants in the group III truncated hemoglobin from Campylobacter jejuni. J. Biol. Chem. 281:37803–37812.

    Article  PubMed  CAS  Google Scholar 

  • Nicolis, S., Monzani, E., Ciaccio, C., Ascenzi, P., Moens, L., and Casella, L. 2007. Reactivity and endogenous modification by nitrite and hydrogen peroxide: does human neuroglobin act only as a scavenger? Biochem. J. 407:89–99.

    Article  PubMed  CAS  Google Scholar 

  • Ouellet, H., Juszczak, L., Dantsker, D., Samuni, U., Ouellet, Y. H., Savard, P. Y., Wittenberg, J. B., Wittenberg, B. A., Friedman, J. M., and Guertin, M. 2003. Reactions of Mycobacterium tuberculosis truncated hemoglobin O with ligands reveal a novel lig-and-inclusive hydrogen bond network. Biochemistry 42:5764–5774.

    Article  PubMed  CAS  Google Scholar 

  • Perutz, M. F. 1960. Structure of hemoglobin. Brookhaven Symp. Biol. 13:165–183.

    PubMed  CAS  Google Scholar 

  • Pesce, A., Couture, M., Dewilde, S., Guertin, M., Yamauchi, K., Ascenzi, P., Moens, L., and Bolognesi, M. 2000. A novel two-over-two α-helical sandwich fold is characteristic of the truncated hemoglobin family. EMBO J. 19:2424–2434.

    Article  PubMed  CAS  Google Scholar 

  • Pesce, A., Dewilde, S., Kiger, L., Milani, M., Ascenzi, P., Marden, M. C., Van Hauwaert, M. L., Vanfleteren, J., Moens, L., and Bolognesi, M. 2001. Very high resolution structure of a trematode hemoglobin displaying a TyrB10-TyrE7 heme distal residue pair and high oxygen affinity. J. Mol. Biol. 309:1153–1164.

    Article  PubMed  CAS  Google Scholar 

  • Potts, M., Angeloni, S. V., Ebel, R. E., and Bassam, D. 1992. Myoglobin in a Cyanobacterium. Science 256:1690–1691.

    Article  PubMed  CAS  Google Scholar 

  • Ptitsyn, O. B., and Ting, K. L. 1999. Non-functional conserved residues in globins and their possible role as a folding nucleus. J. Mol. Biol. 291:671–682.

    Article  PubMed  CAS  Google Scholar 

  • Sato, T., and Tamiya, H. 1937. Ueber die Atmungsfarbstoffe von Paramecium. Cytologia (Tokyo) Fujii-Jubilaei Volume: 1133–1138.

    Google Scholar 

  • Scott, N. L., Falzone, C. J., Vuletich, D. A., Zhao, J., Bryant, D. A., and Lecomte, J. T. J. 2002. Truncated hemoglobin from the cyanobacterium Synechococcus sp. PCC 7002: evidence for hexacoordination and covalent adduct formation in the ferric recombinant protein. Biochemistry 41:6902–6910.

    Article  PubMed  CAS  Google Scholar 

  • Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., and Higgins, D. G. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876–4882.

    Article  PubMed  CAS  Google Scholar 

  • Vinogradov, S. N., Hoogewijs, D., Bailly, X., Arredondo-Peter, R., Guertin, M., Gough, J., Dewilde, S., Moens, L., and Vanfleteren, J. R. 2005. Three globin lineages belonging to two structural classes in genomes from the three kingdoms of life. Proc. Natl. Acad. Sci. U.S.A. 102:11385–11389.

    Article  PubMed  CAS  Google Scholar 

  • Vinogradov, S. N., Hoogewijs, D., Bailly, X., Mizuguchi, K., Dewilde, S., Moens, L., and Vanfleteren, J.R. 2007. A model of globin evolution. Gene 398:132–142.

    Article  PubMed  CAS  Google Scholar 

  • Vuletich, D. A., and Lecomte, J. T. J. 2006. A phylogenetic and structural analysis of truncated hemoglobins. J. Mol. Evol. 62:196–210.

    Article  PubMed  CAS  Google Scholar 

  • Wainwright, L. M., Wang, Y., Park, S. F., Yeh, S. R., and Poole, R. K. 2006. Purification and spectroscopic characterization of Ctb, a group III truncated hemoglobin implicated in oxygen metabolism in the food-borne pathogen Campylobacter jejuni. Biochemistry 45:6003–6011.

    Article  PubMed  CAS  Google Scholar 

  • Weber, R. E., and Fago, A. 2004. Functional adaptation and its molecular basis in vertebrate hemoglobins, neuroglobins and cytoglobins. Respir. Physiol. Neurobiol. 144:141–159.

    Article  PubMed  CAS  Google Scholar 

  • Weber, R. E., and Vinogradov, S. N. 2001. Nonvertebrate hemoglobins: functions and molecular adaptations. Physiol. Rev. 81:569–628.

    PubMed  CAS  Google Scholar 

  • Wittenberg, J. B. 2007. On optima: the case of myoglobin-facilitated oxygen diffusion. Gene 398:156–161.

    Article  PubMed  CAS  Google Scholar 

  • Wittenberg, J. B., Bolognesi, M., Wittenberg, B. A., and Guertin, M. 2002. Truncated hemoglobins: a new family of hemoglobins widely distributed in bacteria, unicellular eukaryotes, and plants. J. Biol. Chem. 277:871–874.

    Article  PubMed  CAS  Google Scholar 

  • Wittenberg, J. B., and Wittenberg, B. A. 2003. Myoglobin function reassessed. J. Exp. Biol. 206:2011–2020.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer-Verlag Italia

About this chapter

Cite this chapter

Vuletich, D.A., Lecomte, J.T.J. (2008). The Phylogeny and Structural Properties of 2/2 Haemoglobins. In: Bolognesi, M., di Prisco, G., Verde, C. (eds) Dioxygen Binding and Sensing Proteins. Protein Reviews, vol 9. Springer, Milano. https://doi.org/10.1007/978-88-470-0807-6_5

Download citation

Publish with us

Policies and ethics