Mitochondrial Genomes of Hemiarma marina and Leucocryptos marina Revised the Evolution of Cytochrome c Maturation in Cryptista

Abstract

Two evolutionarily distinct systems for cytochrome c maturation in mitochondria-Systems I and III-have been found among diverse aerobic eukaryotes. System I requires a set of proteins including mitochondrion-encoded CcmA, CcmB, CcmC, and CcmF (or a subset of the four proteins). On the other hand, System III is operated exclusively by nucleus-encoded proteins. The two systems are mutually exclusive among eukaryotes except a single organism possessing both. Recent advances in understanding both diversity and phylogeny of eukaryotes united cryptophytes, goniomonads, Hemiarma marina, kathablepharids and Palpitomonas bilix into one of the major taxonomic assemblages in eukaryotes (Cryptista). Among the lineages/species in Cryptista, the mitochondrial genomes (mtDNAs) have been completed for multiple cryptophytes, a goniomonad and P. bilix, and ccm genes were found solely in the P. bilix mtDNA. Nevertheless, we have been unsure whether H. marina and/or kathablepharids use System I for cytochrome c maturation, as no mtDNA was available for either of the two cryptist members. In this study, we determined the complete sequences of the mtDNAs of H. marina and a kathablepharid Leucocryptos marina, and found ccmA, ccmC, and ccmF in the former genome. Curiously, the ccm genes found in the H. marina mtDNA showed no phylogenetic affinity to the P. bilix homologs, unfavoring vertical inheritance of the ccm genes in the mtDNA evolution in Cryptista. Finally, we propose revised scenarios for the evolution of cytochrome c maturation systems in Cryptista by incorporating the mtDNA data obtained in this study.

On the bacterial ancestry of mitochondria: new insights with triangulated approaches

“…CcmF and other components of the Ccm system are encoded in the mtDNA of a variety of eukaryotic taxa including plants, Jakobida [13,15], Diphylleia [14], Palpitomons [51], Cryptista-related such as Hemiarma [52], Malawimonadida, Cyanidiales of Rhodophyta [53] and also Ciliophora such as Tetrahymena [54]. Ciliophora are at odds with the rest of the TSAR super-group to which they belong [50], which generally has System III for cytochrome c biogenesis [49,52]. System III consists of a single heme lyase protein without bacterial precedents, therefore constituting a eukaryotic innovation [49,52].…”

“…System III consists of a single heme lyase protein without bacterial precedents, therefore constituting a eukaryotic innovation [49,52]. For this reason, we have excluded the eukaryotic groups that have System III and its possible ancestor System V of Euglenozoa [55], except for lineages that are related to those containing the Ccm system (Cryptista, Haptista, Chlorophyta and Rhodophyta [52]). We additionally excluded Ciliophora for the highly derived nature of their genomes [16,54] and Malawimonadida because they lack nuclear genes.…”

“…The selection of the aerobic traits (Box 1) guided the choice of thes eukaryotic taxa, which were selected on the basis of the presence of at least one Ccm gene for cytochrome c biogenesis, because the Ccm system has been vertically inherited from alphaproteobacteria [13,14,49]. CcmF and other components of the Ccm system are encoded in the mtDNA of a variety of eukaryotic taxa including plants, Jakobida [13,15], Diphylleia [14], Palpitomons [51], Cryptista-related such as Hemiarma [52], Malawimonadida, Cyanidiales of Rhodophyta [53] and also Ciliophora such as Tetrahymena [54]. Ciliophora are at odds with the rest of the TSAR super-group to which they belong [50], which generally has System III for cytochrome c biogenesis [49,52].…”

A functional bacterial-derived restriction modification system in the mitochondrion of a heterotrophic protist

“…Our recent initiative to assess mitochondrial genome content using environmentally sampled protistan single-cell amplified genome (SAG) sequencing resulted in the complete mitochondrial sequence of multiple marine heterotrophic katablepharid protists [24]. The contemporary publication of the complete Leucocryptos marina mitochondrial genome confirmed the identity of the single-cell amplified genome (SAG)-derived mitochondrial DNAs as katablepharids [25]. The genomes from the SAG-generated mtDNA and Leucocryptos mtDNA were identical in their repertoires of canonical mitochondrial genes including tRNA genes ( Fig.…”

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“…Our recent initiative to assess mitochondrial genome content using environmentally sampled, protistan, single-cell amplified genome (SAG) sequences resulted in the complete mitochondrial sequence of multiple marine heterotrophic katablepharid protists [26]. The contemporary publication of the complete Leucocryptos marina mitochondrial genome confirmed the identity of the SAG-derived mtDNAs as katablepharid [30]. The genomes from the SAG-generated mtDNA and Leucocryptos mtDNA were identical in their repertoires of canonical mitochondrial genes, including those encoding tRNAs (Fig 1A).…”