Red blood with blue-blood ancestry: Intriguing structure of a snail hemoglobin

doi:10.1073/pnas.0601861103

Red blood with blue-blood ancestry: Intriguing structure of a snail hemoglobin

*Institute of Zoology, Johannes Gutenberg University, D-55099 Mainz, Germany; and
^‡Biology Department, University of New Mexico, 269 Castetter Hall, Albuquerque, NM 87131

Edited by Francisco J. Ayala, University of California, Irvine, CA, and approved June 15, 2006 (received for review March 7, 2006)

Abstract

The phylogenetic enigma of snail hemoglobin, its isolated occurrence in a single gastropod family, the Planorbidae, and the lack of sequence data, stimulated the present study. We present here the complete cDNA and predicted amino acid sequence of two hemoglobin polypeptides from the planorbid Biomphalaria glabrata (intermediate host snail for the human parasite Schistosoma mansoni). Both isoforms contain 13 different, cysteine-free globin domains, plus a small N-terminal nonglobin “plug” domain with three cysteines for subunit dimerization (total M _r ≈ 238 kDa). We also identified the native hemoglobin molecule and present here a preliminary 3D reconstruction from electron microscopical images (3 nm resolution); it suggests a 3 × 2-mer quaternary structure (M _r ≈ 1.43 MDa). Moreover, we identified a previously undescribed rosette-like hemolymph protein that has been mistaken for hemoglobin. We also detected expression of an incomplete hemocyanin as trace component. The combined data show that B. glabrata hemoglobin evolved from pulmonate myoglobin, possibly to replace a less-efficient hemocyanin, and reveals a surprisingly simple evolutionary mechanism to create a high molecular mass respiratory protein from 78 similar globin domains.

Footnotes

^†To whom correspondence may be addressed. E-mail: lieb{at}uni-mainz.de or markl{at}uni-mainz.de
Author contributions: B.L., W.G., C.M.A. and J.M. designed research; B.L., K.D., H.-S.K., S.B., W.G., A.M., B.H., S.A.S., C.M.A., and J.M. performed research and analyzed data; and B.L., W.G., C.M.A., and J.M. wrote the paper.
Conflict of interest statement: No conflicts declared.
This paper was submitted directly (Track II) to the PNAS office.
Data deposition: The B. glabrata hemoglobin sequences have been deposited in the GenBank database [accession nos. AM167926 (BgHb1), AM167927 (BgHb2), and AM167928 (BgHb3)].
Abbreviations:

BgHb,

Biomphalaria glabrata hemoglobin;

BgRp,

B. glabrata rosette protein;

BgHc,

B. glabrata hemocyanin.