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The Hemoglobins of Sub-Antarctic Fishes of the Suborder Notothenioidei

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The Hemoglobins of Sub-Antarctic Fishes of the Suborder Notothenioidei View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Available online at www.sciencedirect.com Polar Science 4 (2010) 295e308 http://ees.elsevier.com/polar/ The hemoglobins of sub-Antarctic fishes of the suborder Notothenioidei Daniela Coppola a, Daniela Giordano a, Alessandro Vergara b, Lelio Mazzarella b, Guido di Prisco a, Cinzia Verde a, Roberta Russo a,* a Institute of Protein Biochemistry, CNR, Via Pietro Castellino 111, I-80131 Naples, Italy b Department of Chemistry, University of Naples ‘Federico II’, Complesso Universitario Monte S. Angelo, Via Cinthia, I-80126 Naples, Italy Received 16 December 2009; revised 19 April 2010; accepted 19 April 2010 Available online 12 May 2010 Abstract Fishes of the perciform suborder Notothenioidei provide an excellent opportunity for studying the evolution and functional importance of evolutionary adaptations to temperature. To understand the unique biochemical features of high-Antarctic noto- thenioids, it is important to improve our knowledge of these highly cold-adapted stenotherms with new information on their sub- Antarctic relatives. This paper focuses on the oxygen-transport system of two non-Antarctic species, Eleginops maclovinus and Bovichtus diac- anthus. Unlike most Antarctic notothenioids, the blood of E. maclovinus and B. diacanthus displays high hemoglobin (Hb) multiplicity. E. maclovinus, the sister group of Antarctic notothenioids, has one cathodal (Hb C) and two anodal components (Hb 1, Hb 2). B. diacanthus, one of the most northern notothenioids, has three major Hbs. The multiple Hbs may have been maintained as a response to temperature differences and fluctuations of temperate waters, much larger than in the Antarctic. Although non- Antarctic notothenioids have never developed cold adaptation, the amino-acid sequence reveals high identity with the globins of Antarctic notothenioids. Hbs of sub-Antarctic notothenioids are characterised by high oxygen affinity and Root effect. Phylogenetic analyses are consistent with the hypothesis that Bovichtidae and Eleginopidae diverged after they became established in more temperate waters north of the Antarctic Polar Front. Ó 2010 Elsevier B.V. and NIPR. All rights reserved. Keywords: Hemoglobin; Fish; Hemoglobin multiplicity; Root effect 1. Introduction of water, uniquely cold and thermally stable. The opening of the Drake Passage, occurred approximately The formation of the Southern Ocean, which 41 million years ago, and the formation of the Tas- surrounds Antarctica and includes the Weddell and manian Gateway few millions years after, are the two Ross Seas, was marked by the creation of a large mass key events (Scher and Martin, 2006). The separation of the southern landmasses led to the development of the * Corresponding author. Antarctic Circumpolar Current (ACC), and this in turn E-mail address: [email protected] (R. Russo). was at least partially responsible for cooling of 1873-9652/$ - see front matter Ó 2010 Elsevier B.V. and NIPR. All rights reserved. doi:10.1016/j.polar.2010.04.007 296 D. Coppola et al. / Polar Science 4 (2010) 295e308 Antarctic waters from w20 C to the present extreme AFGPs in non-Antarctic notothenioids from South values near À1.8 C(Clarke, 1983). Ocean changes America and New Zealand waters has been examined played a crucial role in establishing the thermal in several studies (Cheng et al., 2003; Cheng and conditions that have driven evolution of the Antarctic Detrich, 2007). The copy numbers of AFGP genes biota (Eastman, 1993). The cold and oxygen-rich and the numbers of AFGPs reflect the harshness of the waters south of the Antarctic Polar Front (APF; the freezing threat that Antarctic notothenioids have to northern boundary of the ACC, a well-defined roughly face, in comparison with temperate notothenioids, circular oceanic system, running between 50S and which reached temperate waters before the production 60S) serve as important effectors of evolution of the of the high levels of AFGPs found in current Antarctic Antarctic marine biota. The APF acts as a cold “wall” notothenioids (Cheng et al., 2003). that hinders mixing of the waters of the Southern In Notothenia angustata and Notothenia micro- Ocean with those of the Indian, Pacific and Atlantic lepidota, living in cool-temperate waters, the AFGP Oceans and limits migration of the fauna of the system is reduced, with very low blood AFGP temperate ocean to the south, and vice versa (Coppes concentration and only two to three genes showing and Somero, 2007). Because of this, the APF acts as some replacements in the functional repeat a barrier for gene flow, causing evolutionary processes ThreAlaeAla (Cheng et al., 2003). Dissostichus ele- to occur in isolation. ginoides, a non-Antarctic notothenioid of the family Diversification of the major group of Antarctic fishes Nototheniidae, appears to have no functional AFGP of the perciform suborder Notothenioidei, largely sequences, consistent with its non-Antarctic distribu- confined within Antarctic and sub-Antarctic waters, has tion. The hypothesis is that this species had the occurred in parallel with the climatic changes. This primordial AFGP genotype, lost or mutated following suborder comprises eight families and 122 species. Five its migration to non-Antarctic habitats (Cheng et al., families and 96 species are Antarctic, whereas three 2003). families and 26 species are non-Antarctic (Eastman, Another remarkable example of adaptation to 2005). Among the five notothenioid families, Notothe- extreme cold found in Antarctic notothenioid fishes is niidae, Harpagiferidae, Artedidraconidae, Bathy- the apparent loss of inducible heat-shock response draconidae and Channichthyidae, 15 species occur (HSR) at constantly cold temperatures (Hofmann et al., along the cool-temperate southern coast of South 2000). Interesting results showed that Bovichtus vari- America and New Zealand (Eastman and Eakin, 2000). egatus (family Bovichtidae) expresses heat-shock These cold-temperate species encounter water temper- proteins (hsp) in response to heat stress, whereas atures of approximately 5e15 C. Three small basal N. angustata, a non-Antarctic notothenioid living in families, 10 of 11 species in the family Bovichtidae, New Zealand waters, does not display the stress- monotypic Pseudaphritidae and Eleginopidae are non- inducible hsp synthesis at the protein-level (Hofmann Antarctic and presumably diverged during the Eocene et al., 2005). These results suggest that HSR, the up- and became established in waters around areas corre- regulation of heat-stress sensitive genes, was lost after sponding to New Zealand, Australia and high-latitude evolution in the subzero, stenothermic environment of South America. They essentially never experienced Antarctic waters during the divergence of Bovichtidae near-freezing water temperatures, and absence of from the other Antarctic notothenioid families. detectable antifreeze-glycoprotein (AFGP) coding Red-blooded high-Antarctic notothenioid families sequence in Bovichtidae, Pseudaphritidae and Ele- have evolved a suite of physiological and molecular ginopidae supports this scenario for the basal notothe- adaptations, accompanied by a decrease in Hb oxygen nioid lineages (Cheng et al., 2003). affinity and concentration (Verde et al., 2006b). Hb- To understand the unique biochemical features of less Channichthyidae represent the extreme of this high-Antarctic notothenioids, it is important to enrich trend (Ruud, 1954). our knowledge of these highly cold-adapted steno- This paper provides preliminary data on the oxygen- therms with new information on their sub-Antarctic transport system of two non-Antarctic species, Ele- relatives. ginops maclovinus and B. diacanthus. The survival of polar fish depends on the presence E. maclovinus, locally known as mullet or ro´balo, of AFGPs because they avoid freezing by binding is a notothenioid belonging to the family Ele- water to AFGPs, thus preventing growth of ice crystals ginopidae and is the only species of its genus. It is an in their blood and other body fluids (DeVries, 1988; important component of the ichthyofauna in the Cheng and DeVries, 1991). The occurrence of coastal temperate and sub-Antarctic waters of South D. Coppola et al. / Polar Science 4 (2010) 295e308 297 America; it is also found in coastal waters around the 2.3. Amino-acid sequencing Falkland Islands (Falkland Islands Government, 2003; Brickle et al., 2005). E. maclovinus is the sister group Globins of E. maclovinus and B. diacanthus were of Antarctic notothenioids that dominate the cold purified by reverse-phase HPLC on C4 Vydac shelf waters of Antarctica and it is of interest to (4.6 Â 250 mm) columns. Before loading, samples understand notothenioid diversification representing were incubated in a denaturating solution of 5% the “starting point” for the notothenioid radiation b-mercaptoethanol and 1% TFA at room temperature. (Eastman and Lannoo, 2008). The status of Eleginops Fractionation of tryptic peptides and subsequent as sister group of Antarctic notothenioids is supported amino-acid sequencing were carried out as previously by phylogenetic analyses employing both morpho- described (Verde et al., 2002). Nucleotide sequences logical (Balushkin, 2000) and molecular data, were established by cloning and sequence analysis of including partial (Bargelloni et al., 2000) and globin cDNAs: complete 16S rRNA (Near et al., 2004) mtDNA gene sequences. a) B. diacanthus: total RNA was isolated from the South
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