Abstract

BackgroundDinoflagellates comprise an ecologically significant and diverse eukaryotic phylum that is sister to the phylum containing apicomplexan endoparasites. The mitochondrial genome of apicomplexans is uniquely reduced in gene content and size, encoding only three proteins and two ribosomal RNAs (rRNAs) within a highly compacted 6 kb DNA. Dinoflagellate mitochondrial genomes have been comparatively poorly studied: limited available data suggest some similarities with apicomplexan mitochondrial genomes but an even more radical type of genomic organization. Here, we investigate structure, content and expression of dinoflagellate mitochondrial genomes.ResultsFrom two dinoflagellates, Crypthecodinium cohnii and Karlodinium micrum, we generated over 42 kb of mitochondrial genomic data that indicate a reduced gene content paralleling that of mitochondrial genomes in apicomplexans, i.e., only three protein-encoding genes and at least eight conserved components of the highly fragmented large and small subunit rRNAs. Unlike in apicomplexans, dinoflagellate mitochondrial genes occur in multiple copies, often as gene fragments, and in numerous genomic contexts. Analysis of cDNAs suggests several novel aspects of dinoflagellate mitochondrial gene expression. Polycistronic transcripts were found, standard start codons are absent, and oligoadenylation occurs upstream of stop codons, resulting in the absence of termination codons. Transcripts of at least one gene, cox3, are apparently trans-spliced to generate full-length mRNAs. RNA substitutional editing, a process previously identified for mRNAs in dinoflagellate mitochondria, is also implicated in rRNA expression.ConclusionThe dinoflagellate mitochondrial genome shares the same gene complement and fragmentation of rRNA genes with its apicomplexan counterpart. However, it also exhibits several unique characteristics. Most notable are the expansion of gene copy numbers and their arrangements within the genome, RNA editing, loss of stop codons, and use of trans-splicing.

Highlights

  • Dinoflagellates comprise an ecologically significant and diverse eukaryotic phylum that is sister to the phylum containing apicomplexan endoparasites

  • Genomic sequence reveals a complex mitochondrial genome Crypthecodinium cohnii Previously reported C. cohnii cox1 sequences indicated multiple copies of the gene with different flanking sequences [15]. To test if this genomic complexity extends to other C. cohnii mitochondrial genes, we sequenced multiple genomic clones containing cob and/or cox3

  • A library of EcoRI restriction fragments constructed from a fraction enriched in mitochondrial DNA (mtDNA) was screened using a C. cohnii cob gene probe, obtained by polymerase chain reaction (PCR)

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Summary

Introduction

Dinoflagellates comprise an ecologically significant and diverse eukaryotic phylum that is sister to the phylum containing apicomplexan endoparasites. More typically mitochondrial genomes have been reduced to 40–50 genes arranged on either circular- or linear-mapping chromosomes of 15–60 kb ( many plant mitochondrial genomes have been secondarily expanded to several hundreds to thousands of kb) [4]. Diplonemid mitochondria contain multiple circular mtDNA molecules, each encoding gene fragments that are trans-spliced to generate functional transcripts [6]. Another example is the mtDNA in the ichthyosporean, Amoebidium parasiticum: in this case, mitochondrial genes are fragmented and dispersed over several hundred linear chromosomes, totaling > 200 kb [7]. Over the diversity of eukaryotes, mitochondrial genomes exhibit other interesting characteristics, including the use of a number of different non-standard genetic codes, many of which involve alterations in start and, more rarely, stop codons [8,9]

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