Abstract
The degree of conservation and evolution of cytoplasmic mRNA metabolism pathways across the eukaryotes remains incompletely resolved. In this study, we describe a comprehensive genome and transcriptome-wide analysis of proteins involved in mRNA maturation, translation, and mRNA decay across representative organisms from the six eukaryotic super-groups. We demonstrate that eukaryotes share common pathways for mRNA metabolism that were almost certainly present in the last eukaryotic common ancestor, and show for the first time a correlation between intron density and a selective absence of some Exon Junction Complex (EJC) components in eukaryotes. In addition, we identify pathways that have diversified in individual lineages, with a specific focus on the unique gene gains and losses in members of the Excavata and SAR groups that contribute to their unique gene expression pathways compared to other organisms.
Highlights
The eukaryotic tree of life is a complex, elaborate, and beautiful structure
We produced a set of 1655 non-redundant eukaryotic protein sequences involved in mRNA metabolism from the Saccharomyces cerevisiae, Ensembl and other genome databases ([20, 35]; Table A in S1 Table) and transcriptome datasets from the Marine Microeukaryote Transcriptome Sequencing Project (MMETSP) transcriptome reference database [46, 47]
Homologues to the core components of the Exon Junction Complex (EJC); eIF4AIII, Magoh and Y14 were identified from genome sequences of 58 species including members of the six super-groups of eukaryotes (Archaeplastida, Amoebozoa, Opisthokonta, SAR, CCTH, and Excavata; Tables A-D in S2 Table). eIF4AIII, Magoh and Y14 were found to be present in all major eukaryotic super-groups but Magoh and Y14 are selectively absent in organisms with low intron densities such as Saccharomyces cerevisiae; 0.003 introns per gene [25] and Cyanidioschyzon merolae; 0.005 introns per gene [49] (Fig 1)
Summary
The eukaryotic tree of life is a complex, elaborate, and beautiful structure Multicellular lineages such as animals and plants, and model microorganisms such as yeast, only form a small minority of its branches, with the majority of the eukaryotic tree consisting of protists [1]. These other eukaryotic branches are highly diverse in terms of cell organisation, fundamental biochemistry, and life strategy. These distantly related parasitic lineages perhaps most notably, in terms of human impact, include: the pathogenic apicomplexans such as Plasmodium, the causative agent of malaria [2]; the kinetoplastids including Trypanosoma brucei, the causative agent of sleeping sickness [3]; and the oomycetes which are important crop pathogens, including potato late blight [4].
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