Evolutionary History of Mitochondrial Genomes in Discoba, Including the Extreme Halophile Pleurostomum flabellatum (Heterolobosea)

Abstract

Data from Discoba (Heterolobosea, Euglenozoa, Tsukubamonadida, and Jakobida) are essential to understand the evolution of mitochondrial genomes (mitogenomes), since this clade includes the most primitive-looking mitogenomes known, as well some extremely divergent genome information systems. Heterolobosea encompasses more than 150 described species, many of them from extreme habitats, but only six heterolobosean mitogenomes have been fully sequenced to date. Here we complete the mitogenome of the heterolobosean Pleurostomum flabellatum, which is extremely halophilic and reportedly also lacks classical mitochondrial cristae, hinting at reduction or loss of respiratory function. The mitogenome of P. flabellatum maps as a 57,829 bp long circular molecule, including 40 CDSs (19 tRNA, two rRNA, and 19 orfs). The gene content and gene arrangement are similar to Naegleria gruberi and N. fowleri, the closest relatives with sequenced mitogenomes. The P. flabellatum mitogenome contains genes that encode components of the electron transport chain similar to those of Naegleria mitogenomes. Homology searches against a draft nuclear genome showed that P. flabellatum has two homologs of the highly conserved Mic60 subunit of the MICOS complex, and likely lost Mic19 and Mic10. However, electron microscopy showed no cristae structures. We infer that P. flabellatum, which originates from high salinity (313‰) water where the dissolved-oxygen concentration is low, possesses a mitochondrion capable of aerobic respiration, but with reduced development of cristae structure reflecting limited use of this aerobic capacity (e.g., microaerophily).

The Diversity Patterns of Rare to Abundant Microbial Eukaryotes Across a Broad Range of Salinities in a Solar Saltern

“…Many halophilic or halotolerant microbial eukaryotes (e.g., Halocafeteria, Pleurostomum, Trimyema, Euplaesiobystra, Tulamoeba, and Aurem) were discovered in Korean solar salterns, suggesting that a diverse microbial eukaryote is present in these habitats [11,12,18,[21][22][23][24]. However, the overall biodiversity of the high-abundance (> 5% relative abundance (RA)) and rare (< 0.1% RA) [25] eukaryotic groups in Korean solar salterns has not yet been examined using the next-generation sequencing (NGS) approach, which has revealed extensive microbial eukaryote diversity in other systems [19,26,27].…”

Maturases and Group II Introns in the Mitochondrial Genomes of the Deepest Jakobid Branch

“…( B ) ML bootstrap values for the monophyly of Jakobida (without Ophirinina), Ophirinina, Ophirinina + Jakobida, and the competing hypothesis of Ophirinina sister to all Discoba (Ophirinina + Discoba) as a function of the proportion of fast-evolving sites removed from the phylogenomic dataset. ( C ) ML phylogenomic tree based on 14 conserved mitochondrion-encoded proteins from Ettahi et al (2021) . The tree was reconstructed using 25 species and 4,683 amino acid positions with the LG + C60 + F + R7 model using the PMSF approximation.…”

“…S5, Supplementary Material online). Second, we updated the dataset of mitochondrial markers from Ettahi et al (2021) by incorporating our ophirinid sequences and several outgroup taxa and excluding the very long-branching Euglenozoa. The ML tree based on these markers also supported the sister relation of ophirinids and jakobids with maximum bootstrap value (100%) ( fig.…”

“…First, a dataset based on the one described above but from which we removed all metamonads with the exception of the short-branched species Trimastix pyriformis (34 species were kept). Second, a dataset of 14 mitochondrion-encoded markers based on that from Ettahi et al (2021) . Both datasets were trimmed using trimAl v1.2 ( Capella-Gutiérrez et al 2009 ) by removing sites with gaps in more than 80% of the sequences (-gt 0.2) and similarity score below 0.001 (-st 0.001), and restricted minimum resulting length of 20% of the original alignment (-cons 20).…”

“…Among the atypical features are the mitochondrial cristae morphology (discoid-flattened cristae) and the presence of two flagellar vanes ( Yabuki et al 2018 ). More recently, an unrooted phylogeny reconstructed with a dataset of 14 mitochondrial genes placed Ophirina in an intermediate position between jakobids and other discobids ( Ettahi et al 2021 ). In this context, the inclusion of sequence data from new Ophirinina species might help to resolve the phylogenetic position of this group in the eukaryotic tree.…”