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Antarctic fish hemoglobins: evidence for adaptive evolution at subzero temperature.

ABSTRACT: Notothenioids represent a large group of marine teleosts that are mostly endemic to the Antarctic Ocean. In this environment, the low metabolic demand and the high oxygen concentration reduce the need for hemoglobin(s) [Hb(s)]. The extreme condition is represented by the icefish (Channichthyidae, Notothenioidei), the only vertebrates that lack Hb. We obtained the nucleotide sequence coding for the beta-globin chain of the single major Hb form in six red-blooded notothenioids. These included Gymnodraco acuticeps, one of the closest species to the Hb-less icefish, which is also the only known fish having a single Hb without Bohr effect. This species shows a higher rate of nonsynonymous substitutions (KA), in contrast with the homogeneity of synonymous substitution (KS) rates, and KA/KS ratios significantly greater than one in the majority of comparisons. These results are suggestive of positive selection, diversifying the single major Hb toward specialized functions. A single Hb that is free to diversify means that its role in routine oxygen transport can be reduced in the presence of a combination of physiological, ecological, and environmental factors. Although a reduced "routine" function for Hb, as is apparent in G. acuticeps, might, indeed, evoke the lack of Hb in icefish, evidence of diversifying selection reported here is at variance with the hypothesis of a simple trend from a single Hb toward the Hb-less condition.

SUBMITTER: Bargelloni L

PROVIDER: S-EPMC21134 | biostudies-literature | 1998 Jul

REPOSITORIES: biostudies-literature

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Antarctic fish hemoglobins: evidence for adaptive evolution at subzero temperature.

Bargelloni L L Marcato S S Patarnello T T

Proceedings of the National Academy of Sciences of the United States of America 19980701 15

Notothenioids represent a large group of marine teleosts that are mostly endemic to the Antarctic Ocean. In this environment, the low metabolic demand and the high oxygen concentration reduce the need for hemoglobin(s) [Hb(s)]. The extreme condition is represented by the icefish (Channichthyidae, Notothenioidei), the only vertebrates that lack Hb. We obtained the nucleotide sequence coding for the beta-globin chain of the single major Hb form in six red-blooded notothenioids. These included Gymn ...[more]

PMID: 9671736

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Project description:The antifreeze glycoprotein-fortified Antarctic notothenioid fishes comprise the predominant fish suborder in the isolated frigid Southern Ocean. Their ecological success undoubtedly entailed evolutionary acquisition of a full suite of cold-stable functions besides antifreeze protection. Prior studies of adaptive changes in these teleost fishes generally examined a single genotype or phenotype. We report here the genome-wide investigations of transcriptional and genomic changes associated with Antarctic notothenioid cold adaptation. We sequenced and characterized 33,560 ESTs from four tissues of the Antarctic notothenioid Dissostichus mawsoni and derived 3,114 nonredundant protein gene families and their expression profiles. Through comparative analyses of same-tissue transcriptome profiles of D. mawsoni and temperate/tropical teleost fishes, we identified 177 notothenioid protein families that were expressed many fold over the latter, indicating cold-related up-regulation. These up-regulated gene families operate in protein biosynthesis, protein folding and degradation, lipid metabolism, antioxidation, antiapoptosis, innate immunity, choriongenesis, and others, all of recognizable functional importance in mitigating stresses in freezing temperatures during notothenioid life histories. We further examined the genomic and evolutionary bases for this expressional up-regulation by comparative genomic hybridization of DNA from four pairs of Antarctic and basal non-Antarctic notothenioids to 10,700 D. mawsoni cDNA probes and discovered significant to astounding (3- to >300-fold, P < 0.05) Antarctic-specific duplications of 118 protein-coding genes, many of which correspond to the up-regulated gene families. Results of our integrative tripartite study strongly suggest that evolution under constant cold has resulted in dramatic genomic expansions of specific protein gene families, augmenting gene expression and gene functions contributing to physiological fitness of Antarctic notothenioids in freezing polar conditions.

Project description:Subsequent to the two rounds of whole-genome duplication that occurred in the common ancestor of vertebrates, a third genome duplication occurred in the stem lineage of teleost fishes. This teleost-specific genome duplication (TGD) is thought to have provided genetic raw materials for the physiological, morphological, and behavioral diversification of this highly speciose group. The extreme physiological versatility of teleost fish is manifest in their diversity of blood-gas transport traits, which reflects the myriad solutions that have evolved to maintain tissue O(2) delivery in the face of changing metabolic demands and environmental O(2) availability during different ontogenetic stages. During the course of development, regulatory changes in blood-O(2) transport are mediated by the expression of multiple, functionally distinct hemoglobin (Hb) isoforms that meet the particular O(2)-transport challenges encountered by the developing embryo or fetus (in viviparous or oviparous species) and in free-swimming larvae and adults. The main objective of the present study was to assess the relative contributions of whole-genome duplication, large-scale segmental duplication, and small-scale gene duplication in producing the extraordinary functional diversity of teleost Hbs. To accomplish this, we integrated phylogenetic reconstructions with analyses of conserved synteny to characterize the genomic organization and evolutionary history of the globin gene clusters of teleosts. These results were then integrated with available experimental data on functional properties and developmental patterns of stage-specific gene expression. Our results indicate that multiple ?- and ?-globin genes were present in the common ancestor of gars (order Lepisoteiformes) and teleosts. The comparative genomic analysis revealed that teleosts possess a dual set of TGD-derived globin gene clusters, each of which has undergone lineage-specific changes in gene content via repeated duplication and deletion events. Phylogenetic reconstructions revealed that paralogous genes convergently evolved similar functional properties in different teleost lineages. Consistent with other recent studies of globin gene family evolution in vertebrates, our results revealed evidence for repeated evolutionary transitions in the developmental regulation of Hb synthesis.

Dataset Information

Antarctic fish hemoglobins: evidence for adaptive evolution at subzero temperature.

Publications

Antarctic fish hemoglobins: evidence for adaptive evolution at subzero temperature.

Similar Datasets

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