Department of Biology, Western Kentucky University, 1906 College Heights Blvd, #11080, Bowling Green, KY 42101-1080, USA
Department of Animal Biology, University of Illinois at Urbana-Champaign, 515 Morrill Hall, 505 S. Goodwin Avenue, Urbana, IL 61801, USA.
J Exp Biol. 2019 Mar 21;222(Pt 6):jeb188573. doi: 10.1242/jeb.188573.
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.
南极鳕鱼在孤立寒冷的南大洋中的进化导致了显著的特征获得和丧失。其中最引人注目的是冰鱼（Channichthyidae 科）失去了主要的氧气载体血红蛋白（Hb）。尽管这种丧失的机制及其导致的代偿性变化已经得到了很好的研究，但 Hb 丧失对曾经支持其回收和处理的基因网络的影响仍未得到探索。在这里，我们报告了横跨冰鱼科的两种关键 Hb 支持蛋白 - 触珠蛋白（Hp）和血红素结合蛋白（Hx）的功能命运和潜在的分子变化 - 在去除细胞毒性游离 Hb 和血红素方面分别起着至关重要的作用。Hp 在结合游离 Hb 进行细胞内回收方面起着关键作用，由于其主要客户（冰鱼 Hp）不存在，冰鱼的 Hp 转录现在几乎消失，翻译为功能性蛋白质几乎沉默。Hp 基因型退化已经在冰鱼系统发育的不同谱系中表现出来，有三个不同的无意义突变和一个缺失移码突变，以及突变的多聚腺苷酸化信号序列。因此，Hb 的丧失似乎降低了对 Hp 维持的选择压力，导致其随机、共同进化漂移走向灭绝。Hx 结合游离血红素在肝细胞中进行铁回收。与 Hp 相反，Hx 的基因型完整性在冰鱼中得以保留，转录水平与红血细胞的 notothenioids 相当。Hx 的持续存在可能归因于其功能对线粒体和非 Hb 细胞血红素蛋白的持续选择压力。
