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Evolution of the mitochondrial genome: protist connections to animals, fungi and plants Charles E Bullerwell and Michael W Grayà The past decade has seen the determination of complete DNA (mtDNA). For example, the first sequenced mito- mitochondrial genome sequences from a taxonomically chondrial genomes of animals, fungi and plants were diverse set of organisms. These data have allowed an found to have very dissimilar genome organizations that unprecedented understanding of the evolution of the did not immediately suggest common evolutionary ori- mitochondrial genome in terms of gene content and order, as gins. To address issues relating to mtDNA structural well as genome size and structure. In addition, phylogenetic diversity in the context of mitochondrial evolution, infor- reconstructions based on mitochondrial DNA (mtDNA)- mation was needed about mitochondrial genomes from encoded protein sequences have firmly established the representatives spanning the phylogenetic breadth and identities of protistan relatives of the animal, fungal and plant depth of eukaryotes (domain Eucarya). Of particular lineages. Analysis of the mtDNAs of these protists has provided importance in this regard were the protists, mainly uni- insight into the structure of the mitochondrial genome at the cellular organisms that encompass most of the evolution- origin of these three, mainly multicellular, eukaryotic groups. ary diversity of this domain. Further research into mtDNAs of taxa ancestral and intermediate to currently characterized organisms will help to Sequencing efforts over the past decade, particularly refine pathways and modes of mtDNA evolution, as well as those of the Organelle Genome Megasequencing Pro- provide valuable phylogenetic characters to assist in unraveling gram (OGMP; http://megasun.bch.umontreal.ca/ogmp) the deep branching order of all eukaryotes. [4,5] and the Fungal Mitochondrial Genome Project (FMGP; http://megasun.bch.umontreal.ca/People/lang/ Addresses FMGP/FMGP.html) [6,7] have greatly increased the Department of Biochemistry and Molecular Biology, Dalhousie number of complete mtDNA sequences, and also their University, Room 8F-2, Sir Charles Tupper Medical Building, 5850 College Street, Halifax, Nova Scotia B3H 1X5, Canada phylogenetic diversity. This research has revealed a vari- Ãe-mail: [email protected] ety of genome structures, from the several hundred small linear pieces found in the mitochondrion of the ichthyo- sporean Amoebidium parasiticum ([8], discussed below), Current Opinion in Microbiology 2004, 7:528–534 to the gene-rich eubacteria-like mitochondrial genome of This review comes from a themed issue on the jakobid flagellate Reclinomonas americana [9]. These Genomics data, in combination with phylogenies based on mito- Edited by Charles Boone and Philippe Glaser chondrial protein sequences, have strongly supported a Available online 11th September 2004 monophyletic origin for the mitochondrial genome, spe- cifically from within the a-Proteobacteria [5,10,11,12]. 1369-5274/$ – see front matter Despite enormous variations in genome size, ranging # 2004 Elsevier Ltd. All rights reserved. from the tiny apicomplexan mtDNAs (6 kbp) to the DOI 10.1016/j.mib.2004.08.008 expansive plant mtDNAs (>150 kbp), the coding func- tion of the mitochondrial genome has remained relatively stable. In general, mtDNAs code only for genes involved Abbreviations FMGP Fungal Mitochondrial Genome Project in the mitochondrial translation apparatus, electron trans- mtDNA mitochondrial DNA port and oxidative phosphorylation [12 ]. OGMP Organelle Genome Megasequencing Program A particular goal of the OGMP and the FMGP was to sequence the mitochondrial genomes of protists diverg- Introduction ing basally to the animal, fungal and plant lineages. These The first mitochondrial genome to be completely studies aimed to define the evolution of the mitochondrial sequenced (in 1981) was that of Homo sapiens [1]. Over genome from the presumed protist ancestors of these the following decade, mitochondrial genome sequencing groups by identifying evolutionary intermediates. Candi- focused on other members of the metazoan lineage, as dates for these early diverging groups, based on morpho- well as on ascomycete fungi (such as the yeast Saccharo- logical, ultrastructural and molecular evidence, included myces cerevisiae [2]) and land plants (such as the liverwort the choanoflagellates (believed to represent early diver- Marchantia polymorpha [3]). Although these data consti- ging unicellular ancestors of the animals), chytridiomy- tuted an important starting point in the definition of cetes (believed to be related to fungi), and green algae mitochondrial genomics, they were not sufficient for (believed to be specifically affiliated with the land plant determining the origin and evolution of mitochondrial lineage). Current Opinion in Microbiology 2004, 7:528–534 www.sciencedirect.com Evolution of the mitochondrial genome: protist connections to animals, fungi and plants Bullerwell and Gray 529 In this review, we focus on recent advances that have infer the structure of the mitochondrial genome before helped to bridge the gap between the well-established the emergence of multicellularity in this lineage. Of animal, fungal and plant lineages and their unicellular particular interest was the timing of the transition from protistan ancestors. the large, gene-rich mtDNAs seen in some protists to the small, gene-poor mitochondrial genomes seen in Clade Holozoa: choanoflagellates and animals. For example, R. americana contains the most ichthyosporeans are specific relatives ancestral (eubacteria-like) mtDNA identified to date: a of the animals 69 kbp genome that encodes almost 100 genes [9].By Choanocytes, the feeding cells of sponges, bear remark- contrast, animal mitochondrial genomes are much smal- able morphological similarity to members of the choano- ler (with sizes ranging from 13 to 22 kbp) and are highly flagellate protists. This resemblance, first recognized in compact [15], with open reading frames and tRNA the 19th century, prompted the long-standing view that genes often overlapping, and some stop codons created sponges represent an early form of multicellular animal, by the addition of a 30 oligo(A) tail to processed specifically related to choanoflagellates. However, in mRNAs. Metazoan mtDNAs generally encode fewer eukaryotic phylogenies based on molecular sequence than 40 genes, a set that includes no ribosomal protein data, the branching position of the choanoflagellates genes. has not been clear-cut (see [13] for discussion). Thus, it has been argued that choanoflagellates are specific The mitochondrial genome of Monosiga brevicollis, a choa- relatives of either animals or fungi, or that they branch noflagellate, is much larger than metazoan mtDNAs and before the divergence of animals and fungi. The specific encodes many more genes than the latter [8]. M. brevi- relationship of choanoflagellates to the metazoan lineage collis mtDNA is 76 568 bp long, circular mapping, and has only recently been firmly established through phylo- encodes 55 different genes, including 11 specifying ribo- genetic reconstructions based on mitochondrial protein somal proteins. This mtDNA is much more similar to sequence data [13] (Figure 1). This analysis also clearly those of protists such as R. americana than to those of confirms a sister group of the animal-choanoflagellate multicellular animals. Genome content and organization clade: the ichthyosporean protists. Ichthyosporeans, once indicate that the extreme reduction in mtDNA observed referred to as DRIPs (from the first initial of the four in metazoans occurred after the divergence of M. brevi- founding members of the group [14]), were similarly collis (and possibly all choanoflagellates) from the line believed to have diverged near the animal-fungal split. leading to metazoan animals (Figure 2). The mitochon- Based on these new data, Metazoa, Choanoflagellata and drial genome sequence from a member of the sponge Ichthyosporea can be considered a monophyletic group lineage, which is likely to have a branching position (Holozoa [13]) that branches as a sister group to Fungi between those of other multicellular animals and choano- (Figures 1 and 2). flagellates (Figure 1), would undoubtedly help to estab- lish more precisely the evolutionary timing of mtDNA With the identities of some relatively close protistan reduction in the animal lineage. relatives of the animals established, it was possible to In contrast to the mtDNA of M. brevicollis, the mtDNA of Amoebidium parasiticum (an ichthyosporean protist) Figure 1 has possibly the most unusual mitochondrial genome structure ever found [8]. A. parasiticum mtDNA is over animals (>460) 200 kbp in size and consists of hundreds of short (0.3– sponges (0) 8.3 kbp) linear fragments. Of the 80 ‘chromosomes’ that Holozoa have been partially or completely sequenced, three choanoflagellates (1) types have been described: i) small DNA molecules ichthyosporeans (1) without identified coding function, ii) medium-sized ascomycetes (16) DNA species carrying a single gene, and iii) larger basidiomycetes (2) Fungi molecules encoding multiple genes. All chromosomes zygomycetes (3) contain a virtually identical array of short terminal chytridiomycetes (7) repeats. Although other instances of linear mtDNAs land plants (6) and mtDNAs consisting of multiple linear or circular charophytes (2) Viridiplantae components have been described (e.g. [16 ]), no other chlorophytes (10) example is known with such

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