The Rhodomonas salina mitochondrial genome: bacteria-like operons, compact gene arrangement and complex repeat region

Abstract

To gain insight into the mitochondrial genome structure and gene content of a putatively ancestral group of eukaryotes, the cryptophytes, we sequenced the complete mitochondrial DNA of Rhodomonas salina. The 48 063 bp circular-mapping molecule codes for 2 rRNAs, 27 tRNAs and 40 proteins including 23 components of oxidative phosphorylation, 15 ribosomal proteins and two subunits of tat translocase. One potential protein (ORF161) is without assigned function. Only two introns occur in the genome; both are present within cox1 belong to group II and contain RT open reading frames. Primitive genome features include bacteria-like rRNAs and tRNAs, ribosomal protein genes organized in large clusters resembling bacterial operons and the presence of the otherwise rare genes such as rps1 and tatA. The highly compact gene organization contrasts with the presence of a 4.7 kb long, repeat-containing intergenic region. Repeat motifs ∼40–700 bp long occur up to 31 times, forming a complex repeat structure. Tandem repeats are the major arrangement but the region also includes a large, ∼3 kb, inverted repeat and several potentially stable ∼40–80 bp long hairpin structures. We provide evidence that the large repeat region is involved in replication and transcription initiation, predict a promoter motif that occurs in three locations and discuss two likely scenarios of how this highly structured repeat region might have evolved.

An unexpectedly large and loosely packed mitochondrial genome in the charophycean green alga Chlorokybus atmophyticus

“…Both genes are present in Ostreococcus tauri [32]; in addition, nad10 has been found in the prasinophyte Nephroselmis [30] and also in the cryptophyte alga Rhodomonas salina [33]. The gene repertoire of Chlorokybus is most similar to those of Mesostigma and Chaetosphaeridium (Table 2); in total, seven gene differences distinguish the latter two algae from Chlorokybus .…”

“…In the case of the ORF-containing cox1 intron at site 879, positional and structural homologues carrying a similar ORF have been identified exclusively outside the Streptophyta, i.e . in the chlorophyte Oltmannsiellopsis viridis [31], the brown alga Pylaiella littoralis [42] and the cryptophyte alga Rhodomonas salina [33]. Unlike the orf606 of its Oltmannsiellopis counterpart [31], the orf755 of the Chlorokybus cox1 intron can be aligned with the entire Rhodomonas cox1 intron ORF ( orf762 ).…”

Complex repeat structures and novel features in the mitochondrial genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana

“…It has atp4 but not atp8, but has the demethylase dam gene, shared only with the pelagophyte (heterokont) Aureococcus. The two sequenced cryptophyte genomes are also compact, but contain a few more protein-coding genes than stramenopiles (Hauth et al, 2005;Kim et al, 2008). They share only a few co-linear gene pairs with the stramenopiles.…”

“…Rhodomonas salina has a 4.7 kb block made up of several kinds of direct repeat sequences interspersed with six different types of palindrome (Hauth et al, 2005). Hemiselmis andersonii has an even larger repeat region of 20 kb (Kim et al, 2008).…”

Mitochondrial genomes from two red tide forming raphidophycean algae Heterosigma akashiwo and Chattonella marina var. marina

“…It is generally believed that partial duplication of an mt genome via either recombination or replication produced duplicated tRNA genes and/or non-functional tRNA-like sequences in metazoan mt genomes (Boore, 2000;Kurabayashi et al, 2008;Moritz and Brown, 1987), as well as protist mt genomes (Hauth et al, 2005;Kim et al, 2008;Oudot-Le Secq et al, 2006). This study clearly indicates that the same processes operated in the mt genome evolution in the C. marina var.…”