A tale of two genes: Divergent evolutionary fate of haptoglobin and hemopexin in hemoglobinless Antarctic icefishes

Kevin T. Bilyk, Xuan Zhuang, Katherine R. Murphy, Chi-Hing C Cheng-De Vries

Research output: Contribution to journalArticle

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.

Original languageEnglish (US)
Article numberjeb188573
JournalJournal of Experimental Biology
Volume222
Issue number6
DOIs
StatePublished - Jan 1 2019

Fingerprint

Hemopexin
Haptoglobins
haptoglobins
hemoglobin
Hemoglobins
gene
Genes
recycling
genes
Recycling
Heme
genotype
transcription (genetics)
Genotype
nonsense mutation
heme iron
Polyadenylation
protein
Nonsense Codon
Gene Regulatory Networks

Keywords

  • Channichthyidae
  • Notothenioid
  • Relaxed selection

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Physiology
  • Aquatic Science
  • Animal Science and Zoology
  • Molecular Biology
  • Insect Science

Cite this

A tale of two genes : Divergent evolutionary fate of haptoglobin and hemopexin in hemoglobinless Antarctic icefishes. / Bilyk, Kevin T.; Zhuang, Xuan; Murphy, Katherine R.; Cheng-De Vries, Chi-Hing C.

In: Journal of Experimental Biology, Vol. 222, No. 6, jeb188573, 01.01.2019.

Research output: Contribution to journalArticle

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