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A tale of two genes: divergent evolutionary fate of haptoglobin and hemopexin in hemoglobinless Antarctic icefishes.
J Exp Biol. 2019 03 21; 222(Pt 6)JE

Abstract

The evolution of Antarctic notothenioid fishes in the isolated freezing Southern Ocean has led to remarkable trait gains and losses. One of the most extraordinary was the loss of the major oxygen carrier hemoglobin (Hb) in the icefishes (family Channichthyidae). Although the mechanisms of this loss and the resulting compensatory changes have been well studied, the impact of Hb loss on the network of genes that once supported its recycling and disposal has remained unexplored. Here, we report the functional fate and underlying molecular changes of two such key Hb-supporting proteins across the icefish family - haptoglobin (Hp) and hemopexin (Hx), crucial in removing cytotoxic free Hb and heme, respectively. Hp plays a critical role in binding free Hb for intracellular recycling and absent its primary client, icefish Hp transcription is now vanishingly little, and translation into a functional protein is nearly silenced. Hp genotype degeneration has manifested in separate lineages of the icefish phylogeny with three distinct nonsense mutations and a deletion frame shift, as well as mutated polyadenylation signal sequences. Thus, Hb loss appears to have diminished selective constraint on Hp maintenance, resulting in its stochastic, co-evolutionary drift towards extinction. Hx binds free heme for iron recycling in hepatocytes. In contrast to Hp, Hx genotype integrity is preserved in the icefishes and transcription occurs at levels comparable to those in the red-blooded notothenioids. The persistence of Hx likely owes to continued selective pressure for its function from mitochondrial and non-Hb cellular hemoproteins.

Authors+Show Affiliations

Department of Biology, Western Kentucky University, 1906 College Heights Blvd, #11080, Bowling Green, KY 42101-1080, USA kevin.bilyk@wku.edu. Department of Animal Biology, University of Illinois at Urbana-Champaign, 515 Morrill Hall, 505 S. Goodwin Avenue, Urbana, IL 61801, USA.Department of Animal Biology, University of Illinois at Urbana-Champaign, 515 Morrill Hall, 505 S. Goodwin Avenue, Urbana, IL 61801, USA. Department of Ecology & Evolution, University of Chicago, 1101 E. 57th Street, Chicago, IL 60637, USA.Department of Animal Biology, University of Illinois at Urbana-Champaign, 515 Morrill Hall, 505 S. Goodwin Avenue, Urbana, IL 61801, USA. Laboratories of Analytical Biology, National Museum of Natural History, Smithsonian Institution, P.O. Box 37012, MRC 183, Washington, DC 20013-7012, USA.Department of Animal Biology, University of Illinois at Urbana-Champaign, 515 Morrill Hall, 505 S. Goodwin Avenue, Urbana, IL 61801, USA.

Pub Type(s)

Journal Article
Research Support, U.S. Gov't, Non-P.H.S.

Language

eng

PubMed ID

30765469

Citation

Bilyk, Kevin T., et al. "A Tale of Two Genes: Divergent Evolutionary Fate of Haptoglobin and Hemopexin in Hemoglobinless Antarctic Icefishes." The Journal of Experimental Biology, vol. 222, no. Pt 6, 2019.
Bilyk KT, Zhuang X, Murphy KR, et al. A tale of two genes: divergent evolutionary fate of haptoglobin and hemopexin in hemoglobinless Antarctic icefishes. J Exp Biol. 2019;222(Pt 6).
Bilyk, K. T., Zhuang, X., Murphy, K. R., & Cheng, C. C. (2019). A tale of two genes: divergent evolutionary fate of haptoglobin and hemopexin in hemoglobinless Antarctic icefishes. The Journal of Experimental Biology, 222(Pt 6). https://doi.org/10.1242/jeb.188573
Bilyk KT, et al. A Tale of Two Genes: Divergent Evolutionary Fate of Haptoglobin and Hemopexin in Hemoglobinless Antarctic Icefishes. J Exp Biol. 2019 03 21;222(Pt 6) PubMed PMID: 30765469.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - A tale of two genes: divergent evolutionary fate of haptoglobin and hemopexin in hemoglobinless Antarctic icefishes. AU - Bilyk,Kevin T, AU - Zhuang,Xuan, AU - Murphy,Katherine R, AU - Cheng,C-H Christina, Y1 - 2019/03/21/ PY - 2018/07/11/received PY - 2019/02/06/accepted PY - 2019/2/16/pubmed PY - 2020/5/23/medline PY - 2019/2/16/entrez KW - Channichthyidae KW - Notothenioid KW - Relaxed selection JF - The Journal of experimental biology JO - J. Exp. Biol. VL - 222 IS - Pt 6 N2 - The evolution of Antarctic notothenioid fishes in the isolated freezing Southern Ocean has led to remarkable trait gains and losses. One of the most extraordinary was the loss of the major oxygen carrier hemoglobin (Hb) in the icefishes (family Channichthyidae). Although the mechanisms of this loss and the resulting compensatory changes have been well studied, the impact of Hb loss on the network of genes that once supported its recycling and disposal has remained unexplored. Here, we report the functional fate and underlying molecular changes of two such key Hb-supporting proteins across the icefish family - haptoglobin (Hp) and hemopexin (Hx), crucial in removing cytotoxic free Hb and heme, respectively. Hp plays a critical role in binding free Hb for intracellular recycling and absent its primary client, icefish Hp transcription is now vanishingly little, and translation into a functional protein is nearly silenced. Hp genotype degeneration has manifested in separate lineages of the icefish phylogeny with three distinct nonsense mutations and a deletion frame shift, as well as mutated polyadenylation signal sequences. Thus, Hb loss appears to have diminished selective constraint on Hp maintenance, resulting in its stochastic, co-evolutionary drift towards extinction. Hx binds free heme for iron recycling in hepatocytes. In contrast to Hp, Hx genotype integrity is preserved in the icefishes and transcription occurs at levels comparable to those in the red-blooded notothenioids. The persistence of Hx likely owes to continued selective pressure for its function from mitochondrial and non-Hb cellular hemoproteins. SN - 1477-9145 UR - https://www.unboundmedicine.com/medline/citation/30765469/A_tale_of_two_genes:_divergent_evolutionary_fate_of_haptoglobin_and_hemopexin_in_hemoglobinless_Antarctic_icefishes_ DB - PRIME DP - Unbound Medicine ER -