ND6 gene “lost” and found: evolution of mitochondrial gene rearrangement in Antarctic notothenioids

• Main Authors: Xuan Zhuang, C.-H Christina Cheng
• Other Authors: The Pennsylvania State University CiteSeerX Archives
• Format: Text
• Language: English
• Subjects: Antarctic; Southern Ocean; The Antarctic; Antarc*; Icefish
• Online Access: http://citeseerx.ist.psu.edu/viewdoc/summary?doi=10.1.1.1077.7990; http://www.life.illinois.edu/ccheng/Zhuang%20%26%20Cheng_MBE_2010.pdf

Abstract Evolution of Antarctic notothenioids in the frigid and oxygen-rich Southern Ocean had led to remarkable genomic changes, most notably the gain of novel antifreeze glycoproteins and the loss of oxygen-binding hemoproteins in the icefish family. Recently, the mitochondrial (mt) NADH dehydrogenase subunit 6 (ND6) gene and the adjacent transfer RNA Glu (tRNA Glu ) were also reportedly lost. ND6 protein is crucial for the assembly and function of Complex I of the mt electron transport chain that produces adenosine triphosphate (ATP) essential for life; thus, ND6 absence would be irreconcilable with Antarctic notothenioids being thriving species. Here we report our discovery that the ND6 gene and tRNA Glu were not lost but had been translocated to the control region (CR) from their canonical location between ND5 and cytochrome b genes. We characterized the CR and adjacent sequences of 22 notothenioid species representing all eight families of Notothenioidei to elucidate the mechanism and evolutionary history of this mtDNA rearrangement. Species of the three basal non-Antarctic families have the canonical vertebrate mt gene order, whereas species of all five Antarctic families have a rearranged CR bearing the embedded ND6 (ND6 CR ) and tRNA Glu , with additional copies of tRNA Thr , tRNA Pro , and noncoding region in various lineages. We hypothesized that an initial duplication of the canonical mt region from ND6 through CR occurred in the common ancestor to the Antarctic clade, and we deduced the succession of loss or modification of the duplicated region leading to the extant patterns of mt DNA reorganization that is consistent with notothenioid evolutionary history. We verified that the ND6 CR gene in Antarctic notothenioids is transcribed and therefore functional. However, ND6 CRencoded protein sequences differ substantially from basal non-Antarctic notothenioid ND6, and we detected lineage-specific positive selection on the branch leading to the Antarctic clade of ND6 CR under the branch-site model. ...