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Variable Expression of Myoglobin Among the Hemoglobinless Antarctic Icefishes (Channichthyidae͞oxygen Transport͞phylogenetics)

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Variable Expression of Myoglobin Among the Hemoglobinless Antarctic Icefishes (Channichthyidae͞oxygen Transport͞phylogenetics) Proc. Natl. Acad. Sci. USA Vol. 94, pp. 3420–3424, April 1997 Physiology Variable expression of myoglobin among the hemoglobinless Antarctic icefishes (Channichthyidaeyoxygen transportyphylogenetics) BRUCE D. SIDELL*†‡,MICHAEL E. VAYDA*†,DEENA J. SMALL†,THOMAS J. MOYLAN*, RICHARD L. LONDRAVILLE*§, MENG-LAN YUAN†¶,KENNETH J. RODNICK*i,ZOE A. EPPLEY*, AND LORI COSTELLO† *School of Marine Sciences and Department of Zoology, †Department of Biochemistry, Microbiology and Molecular Biology, University of Maine, Orono, ME 04469 Communicated by George N. Somero, Stanford University, Pacific Grove, CA, January 13, 1997 (received for review October 24, 1996) ABSTRACT The important intracellular oxygen-binding Icefishes exhibit several unique physiological features. Car- protein, myoglobin (Mb), is thought to be absent from oxi- diovascular adaptations to compensate for lack of hemoglobin dative muscle tissues of the family of hemoglobinless Antarctic in the circulation include lower blood viscosity, increased heart icefishes, Channichthyidae. Within this family of fishes, which size, greater cardiac output, and increased blood volume is endemic to the Southern Ocean surrounding Antarctica, compared with their red-blooded notothenioid relatives (2, there exist 15 known species and 11 genera. To date, we have 14–16). Combined with the high aqueous solubility of oxygen examined eight species of icefish (representing seven genera) at severely cold body temperature, these cardiovascular fea- using immunoblot analyses. Results indicate that Mb is tures are considered necessary to ensure that tissues obtain present in heart ventricles from five of these species of icefish. adequate amounts of oxygen carried in physical solution by the Mb is absent from heart auricle and oxidative skeletal muscle plasma. Although enhancing circulatory delivery of oxygen, of all species. We have identified a 0.9-kb mRNA in Mb- these adaptations do not assist intracellular movement of expressing species that hybridizes with a Mb cDNA probe oxygen within tissues. Heart ventricle (7, 14) and aerobic from the closely related red-blooded Antarctic nototheniid skeletal muscle (17) of icefishes contain among the highest fish, Notothenia coriiceps. In confirmation that the 0.9-kb mitochondrial densities (.40% of cell volume) of any verte- mRNA encodes Mb, we report the full-length Mb cDNA brate tissues. Consistent with this robust mitochondrial pop- sequence of the ocellated icefish, Chionodraco rastrospinosus. ulation, energy metabolism of the icefishes is highly and Of the eight icefish species examined, three lack Mb polypep- obligately aerobic (2), exacerbating the challenges to both tide in heart ventricle, although one of these expresses the Mb circulatory and intracellular delivery of oxygen. mRNA. All species of icefish retain the Mb gene in their Pale coloration of icefish tissues has led most researchers to genomic DNA. Based on phylogeny of the icefishes, loss of Mb assume that Mb is not present in icefish oxidative muscles expression has occurred independently at least three times (3–7). However, we collected three channichthyid species off and by at least two distinct molecular mechanisms during the Antarctic Peninsula, Chionodraco rastrospinosus, speciation of the family. Pseudochaenichthys georgianus, and Chaenodraco wilsoni, that displayed distinctly rose-colored hearts. By contrast, hearts of Icefishes (family Channichthyidae) of the Southern Ocean two other icefish species common to Peninsular waters, surrounding Antarctica are unique among vertebrate animals; Chaenocephalus aceratus and Champsocephalus gunnari, were all 15 species lack hemoglobin (1, 2) and, despite their highly pale yellow. Absorption spectrum of a clarified supernatant aerobic mode of metabolism, are believed also to lack the (40,000 3 g) from P. georgianus ventricle exhibited maxima at intracellular respiratory pigment, myoglobin (Mb) (3–7). Mb 530 and 580 nm, characteristic of oxymyoglobin. Although not normally is present in high concentration in aerobic muscle conclusive, these observations prompted us to ascertain tissues of vertebrate animals, where it functions both as an whether Mb is expressed in aerobic muscle tissues of icefishes. intracellular oxygen reservoir and to facilitate the transcellular diffusion of oxygen (8). MATERIALS AND METHODS The Perciform suborder Notothenioidei (which includes the Animals and Tissues. Live specimens of icefishes C. acera- icefishes) arose and evolved in coastal Antarctic waters during tus, C. rastrospinosus, C. gunnari, P. georgianus, C. wilsoni, and the last 25 million years (9, 10). Antarctica became isolated at red-blooded notothenioids Notothenia coriiceps and Gobiono- that time upon the opening of the Drake Passage and estab- tothen gibberifrons were collected by Otter Trawl off the south lishment of circumpolar currents that led to the rapid cooling shores of Low and Brabant Islands during the austral autumn of the Southern Ocean. At present, the ocean surrounding in 1991, 1993, and 1995. Pagetopsis macropterus was captured Antarctica is uniquely cold and thermally stable; water tem- off Brabant Island in March 1995. Cryodraco antarcticus tissues peratures around the Antarctic Peninsula fluctuate only be- were the kind gift of A. L. DeVries (University of Illinois) (the tween 10.3 and 21.878C annually (11, 12). Divergence of mitochondrial DNA sequences suggests that radiation of no- Abbreviations: Mb, myoglobin; PVDF, polyvinylidene difluoride. tothenioid families began 7 to 15 million years ago, but that Data deposition: The sequences reported in this paper have been speciation of channichthyid icefish began approximately 1 deposited in the GenBank database [accession no. U68350 (Notothenia coriiceps partial Mb cDNA sequence) and accession no. U70871 million years ago (13). (Chionodraco rastrospinosus full-length Mb cDNA sequence)]. ‡To whom reprint requests should be addressed. § The publication costs of this article were defrayed in part by page charge Present address: Department of Biology, University of Akron, Akron, payment. This article must therefore be hereby marked ‘‘advertisement’’ in OH 44325. ¶ accordance with 18 U.S.C. §1734 solely to indicate this fact. Present address: Department of Neurology, Harvard Medical School and Division of Neuroscience, The Children’s Hospital, Boston, MA Copyright q 1997 by THE NATIONAL ACADEMY OF SCIENCES OF THE USA 02115-5373. 0027-8424y97y943420-5$2.00y0 iPresent address: Department of Biological Sciences, Idaho State PNAS is available online at http:yywww.pnas.org. University, Pocatello, ID 83209. 3420 Downloaded by guest on September 26, 2021 Physiology: Sidell et al. Proc. Natl. Acad. Sci. USA 94 (1997) 3421 specimen was captured from McMurdo Sound). Chionodraco hamatus tissues, from animals captured at Terra Nova Bay, were the kind gift of G. di Prisco and R. Acierno (Italian National Antarctic Program). Heart ventricle, auricle, pectoral adductor profundus, testes, and spleen tissues were dissected immediately upon sacrifice of the animals. Samples were frozen in liquid nitrogen, transported to the United States on dry ice, and stored at 2708C until isolation of protein and nucleic acids. Protein Extraction and Immunoblot Analysis. Soluble polypeptides were liberated from heart ventricles by homog- enization in 20 mM Hepes (pH 7.8) at 48C and centrifuged at 10,000 3 g for 10 min. Protein in the supernatant was determined by BCA assay (Pierce). Polypeptides were dena- tured by boiling in the presence of 1% SDSy1 mM 2-mercap- toethanol, separated by electrophoresis through 17% Tricine– SDSyPAGE gels, and either electrophoretically transferred to polyvinylidene difluoride (PVDF) membranes (Micron Sepa- rations, Westboro, MA) or stained using Coomassie brilliant blue R-250. For slot blots, supernatants were diluted in 13 phosphate-buffered saline (PBS) (pH 7.4) and vacuum blotted onto PVDF membrane. Electroblot and slot-blot membranes were blocked by incubation overnight in 5% nonfat milk, washed in 13 PBS, and incubated with a 1:500 dilution of mouse anti-human Mb monoclonal antibody (Sigma). This antibody displayed strong cross-reactivity with Mb isolated from red-blooded notothenioid species known to express the pigment. Bound antibody was detected by a rabbit anti-mouse IgG secondary antibody (1:1000 dilution) conjugated to alka- line phosphatase (Bio-Rad), and visualized by subsequent incubation in stabilized Western blue substrate (Promega). RNA Gel Blot Hybridization and PCR Amplification. Total RNA was isolated from finely ground, frozen heart ventricles by acid guanidinium–thiocyanate–phenol chloroform extrac- tion (18). RNA concentrations were determined in triplicate by spectrophotometric analyses. Equal amounts (5 mg) of total RNA were resolved by electrophoresis through 1% agarosey formaldehyde gels (19) and blotted to GeneScreen Plus nylon membranes (DuPont). Blots were probed with a 329-bp seg- ment of N. coriiceps Mb cDNA corresponding to codons 5–114 that was 32P-labeled by the random primer method (Boehr- inger Mannheim). Blots received two successive 30-min washes in 0.13 SSCy0.1% SDS at 638C. The N. coriiceps partial Mb cDNA was obtained by reverse transcriptase-PCR (20); first- strand synthesis was primed by oligo(dT)–NotI primer adapter (Pharmacia), and amplification employed degenerate oligo- nucleotides based on conserved segments of tuna and carp Mb polypeptide sequences (Swiss-Prot accession nos. PO2205 and PO2204, respectively). Sequencing confirmed
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