Evidence for Recombination of mtDNA in the Marine Mussel Mytilus trossulus from the Baltic

Abstract

A number of studies have claimed that recombination occurs in animal mtDNA, although this evidence is controversial. Ladoukakis and Zouros (2001) provided strong evidence for mtDNA recombination in the COIII gene in gonadal tissue in the marine mussel Mytilus galloprovincialis from the Black Sea. The recombinant molecules they reported had not however become established in the population from which experimental animals were sampled. In the present study, we provide further evidence of the generality of mtDNA recombination in Mytilus by reporting recombinant mtDNA molecules in a related mussel species, Mytilus trossulus, from the Baltic. The mtDNA region studied begins in the 16S rRNA gene and terminates in the cytochrome b gene and includes a major noncoding region that may be analogous to the D-loop region observed in other animals. Many bivalve species, including some Mytilus species, are unusual in that they have two mtDNA genomes, one of which is inherited maternally (F genome) the other inherited paternally (M genome). Two recombinant variants reported in the present study have population frequencies of 5% and 36% and appear to be mosaic for F-like and M-like sequences. However, both variants have the noncoding region from the M genome, and both are transmitted to sperm like the M genome. We speculate that acquisition of the noncoding region by the recombinant molecules has conferred a paternal role on mtDNA genomes that otherwise resemble the F genome in sequence.

Comparative Mitochondrial Genomics of Freshwater Mussels (Bivalvia: Unionoida) With Doubly Uniparental Inheritance of mtDNA: Gender-Specific Open Reading Frames and Putative Origins of Replication

“…Overall, these studies have shown (i) a high level of nucleotide sequence divergence but nearly identical gene content between F and M genomes within each species, (ii) an accelerated rate of molecular evolution of both the M and the F genomes compared to other animal mitochondrial genomes, (iii) an accelerated rate of molecular evolution of M genomes compared to F genomes, (iv) an absence of atp8 in mytiloid mussels, (v) the presence of a second trnM (i.e., transfer RNA gene for methionine) in mytiloid and veneroid bivalves, (vi) recombination between M and F genomes in mytiloid mussels, (vii) periodic ''role reversals'' (masculinization) of female-transmitted mtDNA in mytiloid mussels that are subsequently transmitted through sperm, (viii) different gene order between F and M genomes in unionoids, and (ix) the presence of a unique extension of the cytochrome c oxidase subunit II gene in the M (but not the F) genome in unionoids (reviewed in Breton et al 2007; see also Chapman et al 2008). An important hypothesis that has emerged from sequencing studies of species with DUI is that genderspecific sequences and/or sequences that exhibit the highest level of nucleotide divergence between the F and M genomes (i.e., regions that are under different, potentially gender-specific selective constraints and could, therefore, have different roles in either genome) are the most likely candidates for determining whether a mitochondrial genome will be transmitted maternally or paternally (Zouros 2000;Burzyń ski et al 2003;Cao et al 2004a;Breton et al 2006Breton et al , 2007Theologidis et al 2007;Venetis et al 2007;Cao et al 2009). For example, it has been demonstrated in marine mussels that masculinized type genomes (i.e., an F genome that ''masculinizes'' and takes on the role of the previous M genome) are essentially recombinants composed of an F genome's coding and control regions, with an additional standard M-type control region (Burzyń ski et al 2003;Breton et al 2006;Venetis et al 2007).…”

“…An important hypothesis that has emerged from sequencing studies of species with DUI is that genderspecific sequences and/or sequences that exhibit the highest level of nucleotide divergence between the F and M genomes (i.e., regions that are under different, potentially gender-specific selective constraints and could, therefore, have different roles in either genome) are the most likely candidates for determining whether a mitochondrial genome will be transmitted maternally or paternally (Zouros 2000;Burzyń ski et al 2003;Cao et al 2004a;Breton et al 2006Breton et al , 2007Theologidis et al 2007;Venetis et al 2007;Cao et al 2009). For example, it has been demonstrated in marine mussels that masculinized type genomes (i.e., an F genome that ''masculinizes'' and takes on the role of the previous M genome) are essentially recombinants composed of an F genome's coding and control regions, with an additional standard M-type control region (Burzyń ski et al 2003;Breton et al 2006;Venetis et al 2007). This has led to the proposition that an M-type control region, particularly its most variable domain called VD1 by Cao et al (2004a), might be necessary to confer the paternal role on genomes that are otherwise F-like (Burzyń ski et al 2003;Breton et al 2006;Venetis et al 2007).…”

“…For example, it has been demonstrated in marine mussels that masculinized type genomes (i.e., an F genome that ''masculinizes'' and takes on the role of the previous M genome) are essentially recombinants composed of an F genome's coding and control regions, with an additional standard M-type control region (Burzyń ski et al 2003;Breton et al 2006;Venetis et al 2007). This has led to the proposition that an M-type control region, particularly its most variable domain called VD1 by Cao et al (2004a), might be necessary to confer the paternal role on genomes that are otherwise F-like (Burzyń ski et al 2003;Breton et al 2006;Venetis et al 2007). Alternatively, the absence of masculinization or role-reversal events in freshwater bivalves coincides with the presence of a unique M genome-specific 39 extension of the cytochrome c oxidase subunit 2 gene (Mcox2e; Curole and Kocher 2002) that could facilitate the transmission of the M genomes in freshwater bivalves (Breton et al 2007;Chakrabarti et al 2007;Chapman et al 2008).…”

Characteristics of mitochondrial DNA of unionid bivalves (Mollusca: Bivalvia: Unionidae). I. Detection and characteristics of doubly uniparental inheritance (DUI) of unionid mitochondrial DNA

“…Till 2000 it was believed that, contrary to nuclear DNA, mtDNA did not undergo recombination. However recently, the body of evidence supporting this phenomenon in animal mtDNA has been increasing (LADOUKAKIS & ZOUROS 2001, PIGANEAU et al 2004, SHAO et al 2005, TSAOUSIS et al 2005, CIBOROWSKI et al 2007), including marine bivalves (LADOUKAKIS & ZOUROS 2001, BURZYÑSKI et al 2003.…”

“…The frequency of heteroplasmy in M. trossulus from the Gulf of Gdañsk, Poland is 32.7% of males and 3.5% of females, and the phenomenon is not a result of hybridisation (WENNE 1993). In the case of marine bivalves there is also evidence for recombination, and reversal or masculinisation events between these molecules of mtDNA, hence in phylogenetic analyses the two mtDNA molecules may not form separate clades (HOEH et al 1996b, 2002a, QUESADA et al 1999, BURZYÑSKI et al 2003, BRETON et al 2007.…”