Adaptation of the Mitochondrial Genome in Cephalopods: Enhancing Proton Translocation Channels and the Subunit Interactions

Abstract

Mitochondrial protein-coding genes (mt genes) encode subunits forming complexes of crucial cellular pathways, including those involved in the vital process of oxidative phosphorylation (OXPHOS). Despite the vital role of the mitochondrial genome (mt genome) in the survival of organisms, little is known with respect to its adaptive implications within marine invertebrates. The molluscan Class Cephalopoda is represented by a marine group of species known to occupy contrasting environments ranging from the intertidal to the deep sea, having distinct metabolic requirements, varied body shapes and highly advanced visual and nervous systems that make them highly competitive and successful worldwide predators. Thus, cephalopods are valuable models for testing natural selection acting on their mitochondrial subunits (mt subunits). Here, we used concatenated mt genes from 17 fully sequenced mt genomes of diverse cephalopod species to generate a robust mitochondrial phylogeny for the Class Cephalopoda. We followed an integrative approach considering several branches of interest–covering cephalopods with distinct morphologies, metabolic rates and habitats–to identify sites under positive selection and localize them in the respective protein alignment and/or tridimensional structure of the mt subunits. Our results revealed significant adaptive variation in several mt subunits involved in the energy production pathway of cephalopods: ND5 and ND6 from Complex I, CYTB from Complex III, COX2 and COX3 from Complex IV, and in ATP8 from Complex V. Furthermore, we identified relevant sites involved in protein-interactions, lining proton translocation channels, as well as disease/deficiencies related sites in the aforementioned complexes. A particular case, revealed by this study, is the involvement of some positively selected sites, found in Octopoda lineage in lining proton translocation channels (site 74 from ND5) and in interactions between subunits (site 507 from ND5) of Complex I.

Signals of positive selection in mitochondrial protein‐coding genes of woolly mammoth: Adaptation to extreme environments?

“…ND5 16 mutation is suggested to have a role in functional metabolic differences in Tachycineta swallow species inhabiting environments with latitudinal variations (Stager et al, 2014 (Almeida et al, 2015), while in rodents, ND6 5 and ND6 6 mutations are linked with adaptation to hypoxic conditions (Tomasco & Lessa, 2011). This evidence points to adaptive variations to oxygen availability and metabolic processes, which may be associated with possible metabolic adaptation of woolly mammoths clades in cold high-latitude environments that are characterized with high oxygen pressure.…”

“…Finch et al (2014) in their study on African savanna and forest elephants also proposed that positive selection in complex I residues including ND5 20 is indicative of ecological adaptations. With respect to site ND6 4 , mutations in residues adjacent to this site have been linked to adaptive selection, where amino acid replacements in ND6 6 is suggested to influence efficiency of electron transfer under cold and hypoxic conditions in cephalopods (Almeida et al, 2015), while in rodents, ND6 5 and ND6 6 mutations are linked with adaptation to hypoxic conditions (Tomasco & Lessa, 2011). This evidence points to adaptive variations to oxygen availability and metabolic processes, which may be associated with possible metabolic adaptation of woolly mammoths clades in cold high-latitude environments that are characterized with high oxygen pressure.…”

Mitogenome evolution in ladybirds: Potential association with dietary adaptation

“…Complex I (NADH dehydrogenase) is the first and largest of the five enzyme complexes that constitute the OXPHOS pathway (Ballard & Whitlock, 2004). ND5 is a conserved and highly hydrophobic protein, and positive selection at nad5 has been suggested in several animals, such as the Tibetan wild ass (Equus kiang) (Luo et al, 2013), the plateau pika (O. curzoniae) (Luo et al, 2013), and various cephalopods (Almeida et al, 2015). Despite the importance of their function, ND3 and ND4L are components of the most smallest subunit of Complex I.…”

“…Numerous studies have shown that non-neutral mutations in mitochondrial-encoded protein-coding genes (PCGs) are associated with adaptations of animals to different environments (Almeida, Maldonado, Vasconcelos, & Antunes, 2015;da Fonseca et al, 2008;Luo, Yang, & Gao, 2013;Pfenninger et al, 2014;Scott et al, 2018Scott et al, , 2011Yuan et al, 2018;Zhang, Yang, & Zhang, 2019).…”

Understanding the adaptive evolution of mitochondrial genomes in intertidal chitons

“…All the events resulting to the impairment of mitochondrial functions have adverse effects on the amino acid constituency of the OXPHOS proteins. Changes in these amino acid residues do not alter protein structure rather can have an impact on the functional domains, such as regions lining the proton translocation channel and subunit interacting sites, and thereby succour animals to adapt to challenging environments [12,13]. Therefore, estimation of selection pressures acting on mt In spite of possessing significant roles as a global food resource and marine bioindicator, only a small percentage of molluscs possess completely sequenced and annotated genomes, rendering the phylum with the lowest ratio between fraction of sequenced genomes and number of described species [26].…”