An Unexpectedly Complex Mitoribosome in Andalucia godoyi, a Protist with the Most Bacteria-like Mitochondrial Genome

Abstract

The mitoribosome, as known from studies in model organisms, deviates considerably from its ancestor, the bacterial ribosome. Deviations include substantial reduction of the mitochondrial ribosomal RNA (mt-rRNA) structure and acquisition of numerous mitochondrion-specific (M) mitoribosomal proteins (mtRPs). A broadly accepted view assumes that M-mtRPs compensate for structural destabilization of mt-rRNA resulting from its evolutionary remodeling. Since most experimental information on mitoribosome makeup comes from eukaryotes having derived mitochondrial genomes and mt-rRNAs, we tested this assumption by investigating the mitochondrial translation machinery of jakobids, a lineage of unicellular protists with the most bacteria-like mitochondrial genomes. We report here proteomics analyses of the Andalucia godoyi small mitoribosomal subunit and in silico transcriptomic and comparative genome analyses of four additional jakobids. Jakobids have mt-rRNA structures that minimally differ from their bacterial counterparts. Yet, with at least 31 small subunit (SSU) and 44 large subunit (LSU) mtRPs, the mitoriboproteome of Andalucia is essentially as complex as that in animals or fungi. Further, the relatively high conservation of jakobid sequences has helped to clarify the identity of several mtRPs, previously considered to be lineage-specific, as divergent homologs of conserved M-mtRPs, notably mS22 and mL61. The coexistence of bacteria-like mt-rRNAs and a complex mitoriboproteome refutes the view that M-mtRPs were ancestrally recruited to stabilize deviations of mt-rRNA structural elements. We postulate instead that the numerous M-mtRPs acquired in the last eukaryotic common ancestor allowed mt-rRNAs to pursue a broad range of evolutionary trajectories across lineages: from dramatic reduction to acquisition of novel elements to structural conservatism.

How to build a ribosome from RNA fragments in Chlamydomonas mitochondria

“…As a result, very few rRNAs are exposed to the solvent, with proteins coating the entire mitoribosome and stabilizing the fragmented rRNAs (Supplementary Movie 1 ). Proteins follow the classical r-protein nomenclature 21 , and newly identified proteins are numbered according to the last inventory of mitoribosomal r-proteins 22 .

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The Chlamydomonas mitochondrial ribosome: how to build a ribosome from RNA fragments

“…The body protuberance could be assigned to a large insertion in the mitoribosome-specific protein mS45 (Fig. S4B), which shows high structural variability between mitoribosomes in different species despite the conservation of its core domain (Valach et al, 2021). The head protuberance was poorly resolved in our density map but is most likely composed of long extensions of the head's conserved rproteins (uS3m, uS10m, mS35).…”

“…As a result, very few rRNAs are exposed to the solvent, with proteins coating the entire mitoribosome and stabilizing the fragmented rRNAs (Movie 1). Proteins follow the classical r-protein nomenclature (Ban et al, 2014), and newly identified proteins are numbered according to the last inventory of mitoribosomal r-proteins (Valach et al, 2021).…”

“…The body protuberance, located close to the mRNA entrance, is mainly formed by a specific extension of more than 400 aa in the mitochondria-specific rprotein mS45 (Fig. S4), a highly variable r-protein (Valach et al, 2021). The head protuberance density could not be assigned due to the low resolution of this area.…”

Estimating global variation in the maximum growth rates of eukaryotic microbes from cultures and metagenomes via codon usage patterns

“…One trait of particular interest is the maximal growth rate of an organism, a fundamental parameter of microbial lifestyle that can tell us a great deal about an organism's ecology [20][21][22]. Among microbial eukaryotes, minimal doubling times range over two orders of magnitude, from hours (e.g., [23,24]) to days (e.g., [25]), and potentially even weeks (e.g., [26,27]).…”