Comparative analysis of the superoxide dismutase gene family in Cetartiodactyla

Abstract

Cetacea, whales, dolphins and porpoises form an order of mammals adapted to aquatic life. Their transition to an aquatic habitat resulted in exceptional protection against cellular insults, including oxidative and osmotic stress. Here, we considered the structure and molecular evolution of the superoxide dismutase (SOD) gene family, which encodes essential enzymes in the mammalian antioxidant system, in the superorder Cetartiodactyla. To this end, we juxtaposed cetaceans and their closest extant relatives (order Artiodactyla). We identified 94 genes in 23 species, of which 70 are bona fide intact genes. Although the SOD gene family is conserved in Cetartiodactyla, lineage‐specific gene duplications and deletions were observed. Phylogenetic analyses show that the SOD2 subfamily diverged from a clade containing SOD1 and SOD3, suggesting that cytoplasmic, extracellular and mitochondrial SODs have started down independent evolutionary paths. Specific‐amino acid changes (e.g. K130N in SOD2) that may enhance ROS elimination were identified in cetaceans. In silico analysis suggests that the core transcription factor repertoire of cetartiodactyl SOD genes may include Sp1, NF‐κB, Nrf2 and AHR. Putative transcription factors binding sites responding to hypoxia were (e.g. Suppressor of Hairless; Su(H)) found in the cetacean SOD1 gene. We found significant evidence for positive selection in cetaceans using codon models. Cetaceans with different diving abilities also show divergent evolution of SOD1 and SOD2. Our genome‐wide analysis of SOD genes helps clarify their relationship and evolutionary trajectory and identify putative functional changes in cetaceans.

Adaptive evolution of antioxidase-related genes in hypoxia-tolerant mammals

“…As an important defense barrier, the antioxidant enzyme system plays a key role in resisting oxidative damage caused by low oxygen levels. Higher SOD activity has been observed in diving species ( Miller, 2012 ), and a significantly higher evolutionary rate of SOD was also identified in cetaceans ( Tian et al, 2021a ). In addition, positive selection affects several GST genes in divergent taxonomic groups, which is indicative of pervasive adaptive evolution ( Tian et al, 2019 ).…”

“…ROS play key roles in the body, such as signaling between cells, immunity, and participation in normal physiological reactions ( Nose, 2000 ; Dröge, 2002 ), but excessive ROS produce certain oxidative damage pressure on the body ( Kaelin, 2005 ). Consequently, numerous species have evolved various antioxidant mechanisms, including non-enzymatic and endogenous antioxidants, to adapt to peroxidative damage in hypoxic environments ( Tian et al, 2021a ). Among these mechanisms, the antioxidant system is crucial for counteracting the effects of hypoxic environments in hypoxia-tolerant animals.…”

“… Tian et al (2021b) found that the SOD gene family has undergone adaptive evolution in cetaceans. Additionally, gene duplication of GPX s occurred, and peroxidase gene families ( PRDX1 and PRDX3 ) expanded in the cetacean lineage ( Yim et al, 2014 ; Zhou et al, 2018 ; Tian et al, 2021a ). In addition, the genomes of the Tibetan antelope ( Pantholops hodgsonii ) showed that 247 positively selected genes are related to hypoxia tolerance, and some of them are connected with antioxidant pathways ( Ge et al, 2013 ).…”

Distribution and diversity of ROS-generating enzymes across the animal kingdom, with a focus on sponges (Porifera)

“…•− production via timing their daily migrations. Indeed, [59] show that antioxidant protection in cetaceans differs between shallow-diving and deep-diving habitats, as reflected by their O 2…”