Evolution of Linear Mitochondrial Genomes in Medusozoan Cnidarians

Abstract

In nearly all animals, mitochondrial DNA (mtDNA) consists of a single circular molecule that encodes several subunits of the protein complexes involved in oxidative phosphorylation as well as part of the machinery for their expression. By contrast, mtDNA in species belonging to Medusozoa (one of the two major lineages in the phylum Cnidaria) comprises one to several linear molecules. Many questions remain on the ubiquity of linear mtDNA in medusozoans and the mechanisms responsible for its evolution, replication, and transcription. To address some of these questions, we determined the sequences of nearly complete linear mtDNA from 24 species representing all four medusozoan classes: Cubozoa, Hydrozoa, Scyphozoa, and Staurozoa. All newly determined medusozoan mitochondrial genomes harbor the 17 genes typical for cnidarians and map as linear molecules with a high degree of gene order conservation relative to the anthozoans. In addition, two open reading frames (ORFs), polB and ORF314, are identified in cubozoan, schyphozoan, staurozoan, and trachyline hydrozoan mtDNA. polB belongs to the B-type DNA polymerase gene family, while the product of ORF314 may act as a terminal protein that binds telomeres. We posit that these two ORFs are remnants of a linear plasmid that invaded the mitochondrial genomes of the last common ancestor of Medusozoa and are responsible for its linearity. Hydroidolinan hydrozoans have lost the two ORFs and instead have duplicated cox1 at each end of their mitochondrial chromosome(s). Fragmentation of mtDNA occurred independently in Cubozoa and Hydridae (Hydrozoa, Hydroidolina). Our broad sampling allows us to reconstruct the evolutionary history of linear mtDNA in medusozoans.

Genetic aspects of mitochondrial genome evolution

“…Medusozoa (Cnidaria excluding Anthozoa) feature linear chromosomes that are split into two or more different molecules (Voigt et al, 2008;Kayal et al, 2012). hjoismäki and Goffart, 2011, and references therein).…”

“…Only the basal Anthozoa harbour circular mitochondrial genomes with a size of up to 21kb (Medina et al, 2006), while the other cnidarian classes display linear chromosomes. In Hydrozoa and Cubozoa they are in addition fragmented into several pieces (Voigt et al, 2008;Kayal et al, 2012). The largest number so far, eight chromosomes, has been found in the the cubozoan Alatina moseri.…”

“…Putative genomic regions involved in replication have been identified for Hydra, although several plausible mechanisms known for other genetic systems have been ruled out for this species (Voigt et al, 2008), see also (Kayal et al, 2012). It seems to be promising to evaluate alternative mechanisms for mitogenome replication known for nonmetazoans with linear or multipartite mitogenomes (see e.g.…”

The mitochondrial gene order and CYTB gene evolution in insects

“…Митогеном многоклеточных животных, за исключением представи телей типа Knidaria, в большинстве случаев содержит 37 генов: 13 белоккодирующих генов, 22 гена тРНК и два гена рибосомальной РНК (Castellana et al, 2011;Kayal et al, 2012).…”

Conformação gonadal, caracterização histoquímica e ultraestrutural da gônada masculina e espermatozoides em espécies de águas-vivas (Cubozoa e Scyphozoa, Medusozoa, Cnidaria)

“…Os problemas classificatórios em Cnidaria têm atraído o interesse de zoólogos (Werner 1973a) e são diversos os trabalhos que apresentam teorias e hipóteses filogenéticas tentativas para classificar o grupo. As principais divergências concernem na problemática sobre: a diversificação dos ciclos de vida e qual dos dois estágios ou formas corporais (pólipo ou medusa) seria o mais basal (Werner 1973a;Werner 1973b;Bridge et al 1992;Schuchert 1993;Bridge et al 1995;Odorico and Miller 1997); na relação entre as quatro das atuais classes de Medusozoa (Hydrozoa, Scyphozoa, Cubozoa e Staurozoa); e entre os subgrupos de Hydrozoa e ordens de Scyphozoa (Marques and Collins 2004;Dawson 2004;Collins et al 2006;Daly et al 2007;Kayal et al 2012;Kayal et al 2013;Zapata et al 2015). Kayal et al (2013) ampliaram a amostragem dos genomas mitocondriais já apresentados para Cnidaria a fim de reavaliar as relações filogenéticas dentro do filo.…”