Mitochondrial Genomes in Unicellular Relatives of

Authors: Dennis V Lavrov B Franz Lang

Publish Date: 2014

Volume: , Issue: , Pages: 1-4

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Abstract

Mitochondrial genomes of unicellular relatives of animals a Phylogenetic relationships among animals fungi and their unicellular relatives as inferred in several recent multigene studies ShalchianTabrizi et al 2008 Torruella et al 2011 and references therein Species names for which mtDNA sequences have been described previously are shown in blue Two species for which mitochondrial genome data are newly reported in this entry are in red b Genetic map comparison of M vibrans and C owczarzaki mtDNAs The linear mitochondrial genome of M vibrans is depicted as a circle with linear ends marked by red filled circles The genome architecture of C owczarzaki is unknown potentially also linear Standard genes in black are atp6 and atp89 subunits 6 8 and 9 of Fo adenosine triphosphate ATP synthase cox13 cytochrome c oxidase subunits 1–3 cob apocytochrome b nad16 and nad4L NADH dehydrogenase subunits 1–6 and 4 L rns and rnl small and large subunit rRNAs tRNA genes are identified by the oneletter code for their corresponding amino acid subscripts denote different genes for isoacceptor tRNAs Genes that do not occur in the standard fungal/animal mtDNA blue are ccmC ccmF cytochrome c maturation protein CcmC and heme lyase rpsN and rplN small and large subunit ribosomal proteins tatC twinarginine translocase component C ORFs in M vibrans green Genes shown on the outer and inner circumference are transcribed in clockwise and counterclockwise direction respectively The gray region within C owczarzaki cox1 indicates a group IB intron that comprises a trnA gene colored red Because of the high number of ORFs in C owczarzaki these are not named instead respective arcs are colored greenMitochondrial genomes of two holozoan protists the marine choanoflagellate Monosiga brevicollis and the freshwater ichthyosporean Amoebidium parasiticum have been described previously Burger et al 2003 Mitochondrial DNA sequences of Capsaspora owczarzaki GenBank accession KC573038 a symbiont of a tropical freshwater snail and of Ministeria vibrans GenBank accession KC573040 a freeliving protist with slender radiating tentacles are published as part of this review Fig 1b Additional sequences are expected to become available through the Origins of Multicellularity Project at the Broad Institute http//wwwbroadinstituteorg/ This review begins with a brief description of the four mitochondrial genomes of holozoan protists followed by a summary of similarities and differences in mtDNA organization in this groupMitochondrial DNA of the choanoflagellate Monosiga brevicollis is a circular mapping molecule 76568 bp in size with 86 A+T content It contains a total of 53 identified genes that specify 26 proteins including tatC a gene for the subunit C of the twinarginine translocase and 11 ribosomal proteins two rRNAs and 25 tRNAs In addition two large open reading frames ORFs are present in the genome Intergenic regions of M brevicollis mtDNA are unusually large several hundred to several thousand bp long and A+Trich 93 They encompass multiple arrays of sequence repeats that consist nearly exclusively of A + T and constitute more than half 53 of the genome Four group I introns are present in M brevicollis mitochondrial genes three in cox1 and one in nad5The mitochondrial genome of Ministeria vibrans is a linear molecule ~56 kb in size having an A+T content of 75 and with large ~1 kb inverted terminal repeats that encompass the gene for aspartate tRNA trnD Fig 1b A total of 50 genes encode 24 proteins including nine ribosomal proteins two rRNAs and 24 tRNAs In addition ten large ORFs are present in the genome three of them exceeding a surprising 1000 codons in length The genes with opposite transcriptional polarities are arranged in two clusters which are subdivided by the largest 1351 bp noncoding region in the genome No introns are found in M vibrans mitochondrial genesThe mitochondrial genome of Capsaspora owczarzaki is ~200 kb in size nearly four times larger than that of its closest relative M vibrans but it has a similar A+T composition 72 It contains 49 identified genes coding for 21 proteins two rRNAs 26 tRNAs plus 52 ORFs greater than 100 codons ORFs that contain long arrays of short sequence repeats that are very common in this mtDNA are not counted Among the protein genes that are unusual for opisthokonts are ccmC and ccmF involved in heme maturation and delivery and six ribosomal protein genes The otherwise common atp8 is lacking Note however that this genome proved difficult to assemble due to a very high content of sequence repeats and therefore it is only tentatively complete and linear in architecture as depicted in Fig 1b Only one intron inside cox1 is present in C owczarzaki mitochondrial genes and it contains a gene for alanine tRNA trnA Accordingly the large size of the genome is due to the large repeatcontaining noncoding regionsFinally the mitochondrial genome of Amoebidium parasiticum consists of several hundred linear chromosomes and has a total estimated size of approximately 300 kb and A+T content of ~62 Burger et al 2003 Three different types of chromosomes have been described an abundant class of small molecules without identified coding function mediumsized molecules carrying a single gene and a few large molecules harboring several genes separated by relatively short 80–200 bp intergenic spacers All chromosomes share a common terminal repeat structure About half of A parasiticum mtDNA has been sequenced and a total of 44 genes have been identified including three for ribosomal proteins In addition 30 ORFs are present in the characterized part of the genome Many tRNA genes in the A parasiticum mtgenome are duplicated with up to four copies and numerous gene fragments are present The genome also contains the largest number of introns in Holozoa even though not all genes have been identified yet at least 21 group I and two group II introns Among individual genes cox1 has eight group I and one group II and rnl has five group I and one group II intronsGene complement of mitochondrial genomes in Holozoa shown as a Venn diagram For comparison the gene content of the homoscleromorph demosponge Oscarella carmela the largest among animals is shown Each oval corresponds to one organism genes included within an oval are present in the mtDNA of the given organism Only proteincoding genes are shown Gene names are abbreviated as in Fig 1At the same time characterized mitochondrial genomes of holozoan protists share several features in common They encode a nearly identical set of proteins involved in oxidative phosphorylation the only variation being the absence atp8 in C owczarzaki mtDNA Fig 2 some ribosomal protein genes and an apparently complete set of tRNAs required for mitochondrial protein synthesis In addition all these organisms use the same “minimally derived” mitochondrial genetic code which differs from the standard genetic code in that UGA codons specify tryptophan rather than termination Finally positions of some cox1 and nad5 introns are conserved between A parasiticum M brevicollis and several nonbilaterian animals Data from additional mitochondrial genomes of unicellular relatives of animals are needed to clarify whether these shared features represent synapomorphies for Holozoa traits shared with a common ancestor and to better understand the evolution of mtDNA in this important group of eukaryotes

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