Diversification of mitochondrial genomes

Eukaryote supergroups and their mitochondrial genomes (consensus after Burki et al. 2020)

Cladogram of eukaryotic supergroups (topology after Burki et al. 2020, with Provora added after Tikhonenkov et al. 2022). The root of the eukaryote tree is unresolved; the tree is drawn with Discoba branching first only for convenience. Each tip carries a summary of what mitochondrial genomes look like in that lineage: size range, number of protein-coding genes, genetic code and notable peculiarities. Hover a tip for details. Sources: Burki et al. 2020; Roger et al. 2017; Gray 2012; Burger et al. 2013; Janouškovec et al. 2017; Tikhonenkov et al. 2022; Karnkowska et al. 2016; Smith & Keeling 2015.

Gene retention in representative mitochondrial genomes

Presence (filled) of the 36 tracked protein genes in representative complete mitogenomes, taken from the current RefSeq annotations by the pipeline (so this table updates too). Genes are ordered as in the marker table; taxa sorted by number of retained genes. Note that some absences reflect annotation vocabulary rather than biology (see the unmatched-products log in Methods).

Themes

• Gene loss is the rule, but rates differ enormously. Jakobids retain ~66 protein genes including a bacterial RNA polymerase (Lang et al. 1997; Burger et al. 2013); animals keep 13, apicomplexans 3; the direction is nearly always mtDNA → nucleus (Adams & Palmer 2003). Gene-rich mtDNAs are scattered across the tree (jakobids, malawimonads, Ancoracysta, cryptophytes, some CRuMs and stramenopiles), so LECA's mtDNA was itself gene-rich (Janouškovec et al. 2017; Roger et al. 2017).
• Size and gene content are decoupled. Land-plant mtDNAs reach megabases with only ~40 genes (Sloan et al. 2012); animal mtDNAs are compact; fungal genomes are inflated by introns and ORFs (Smith & Keeling 2015).
• Architecture varies wildly: linear and multichromosomal genomes, fragmented genes and rRNAs (Chlamydomonas, apicomplexans, dinoflagellates, diplonemids), RNA editing (kinetoplastids, plants, Physarum), and repeated changes of the genetic code (UGA = Trp in table 4 mtDNAs, reassignments in animals, ciliates, green algae).
• Complete loss of the mitochondrial genome occurred many times in anaerobes (mitosomes, hydrogenosomes) and, in Monocercomonoides, of the organelle itself (Karnkowska et al. 2016).

References

Burki F, Roger AJ, Brown MW, Simpson AGB (2020). The new tree of eukaryotes. Trends in Ecology & Evolution 35: 43–55. doi:10.1016/j.tree.2019.08.008

Lang BF, Burger G, O'Kelly CJ, Cedergren R, Golding GB, Lemieux C, Sankoff D, Turmel M, Gray MW (1997). An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature 387: 493–497. doi:10.1038/387493a0

Gray MW, Burger G, Lang BF (1999). Mitochondrial evolution. Science 283: 1476–1481. doi:10.1126/science.283.5407.1476

Gray MW, Lang BF, Burger G (2004). Mitochondria of protists. Annual Review of Genetics 38: 477–524. doi:10.1146/annurev.genet.37.110801.142526

Gray MW (2012). Mitochondrial evolution. Cold Spring Harbor Perspectives in Biology 4: a011403. doi:10.1101/cshperspect.a011403

Burger G, Gray MW, Forget L, Lang BF (2013). Strikingly bacteria-like and gene-rich mitochondrial genomes throughout jakobid protists. Genome Biology and Evolution 5: 418–438. doi:10.1093/gbe/evt008

Janouškovec J, Tikhonenkov DV, Burki F, Howe AT, Rohwer FL, Mylnikov AP, Keeling PJ (2017). A new lineage of eukaryotes illuminates early mitochondrial genome reduction. Current Biology 27: 3717–3724. doi:10.1016/j.cub.2017.10.051

Tikhonenkov DV, Mikhailov KV, Gawryluk RMR, Belyaev AO, Mathur V, Karpov SA, Zagumyonnyi DG, Borodina AS, Prokina KI, Mylnikov AP, Aleoshin VV, Keeling PJ (2022). Microbial predators form a new supergroup of eukaryotes. Nature 612: 714–719. doi:10.1038/s41586-022-05511-5

Adams KL, Palmer JD (2003). Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Molecular Phylogenetics and Evolution 29: 380–395. doi:10.1016/S1055-7903(03)00194-5

Sloan DB, Alverson AJ, Chuckalovcak JP, Wu M, McCauley DE, Palmer JD, Taylor DR (2012). Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biology 10: e1001241. doi:10.1371/journal.pbio.1001241

Smith DR, Keeling PJ (2015). Mitochondrial and plastid genome architecture: reoccurring themes, but significant differences at the extremes. Proceedings of the National Academy of Sciences USA 112: 10177–10184. doi:10.1073/pnas.1422049112

Boore JL (1999). Animal mitochondrial genomes. Nucleic Acids Research 27: 1767–1780. doi:10.1093/nar/27.8.1767

Lavrov DV, Pett W (2016). Animal mitochondrial DNA as we do not know it: mt-genome organization and evolution in nonbilaterian lineages. Genome Biology and Evolution 8: 2896–2913. doi:10.1093/gbe/evw195

Feagin JE, Harrell MI, Lee JC, Coe KJ, Sands BH, Cannone JJ, Tami G, Schnare MN, Gutell RR (2012). The fragmented mitochondrial ribosomal RNAs of Plasmodium falciparum. PLoS ONE 7: e38320. doi:10.1371/journal.pone.0038320

Waller RF, Jackson CJ (2009). Dinoflagellate mitochondrial genomes: stretching the rules of molecular biology. BioEssays 31: 237–245. doi:10.1002/bies.200800164

Zíhala D, Eliáš M (2019). Evolution and unprecedented variants of the mitochondrial genetic code in a lineage of green algae. Genome Biology and Evolution 11: 2992–3007. doi:10.1093/gbe/evz210

Karnkowska A, Vacek V, Zubáčová Z, Treitli SC, Petrželková R, Eme L, Novák L, Žárský V, Barlow LD, Herman EK, Soukal P, Hroudová M, Doležal P, Stairs CW, Roger AJ, Eliáš M, Dacks JB, Vlček Č, Hampl V (2016). A eukaryote without a mitochondrial organelle. Current Biology 26: 1274–1284. doi:10.1016/j.cub.2016.03.053

Roger AJ, Muñoz-Gómez SA, Kamikawa R (2017). The origin and diversification of mitochondria. Current Biology 27: R1177–R1192. doi:10.1016/j.cub.2017.09.015

Automated tree of RefSeq mitochondrial genomes

Groups are collapsed initially — click a triangle or a legend entry to expand; use the search box to find a species.

Statistics over all complete RefSeq mitogenomes

Sampled genomes