skip to main content

This content will become publicly available on August 1, 2023

Title: Phylogenomic Analyses of 2,786 Genes in 158 Lineages Support a Root of the Eukaryotic Tree of Life between Opisthokonts and All Other Lineages
Abstract Advances in phylogenomics and high-throughput sequencing have allowed the reconstruction of deep phylogenetic relationships in the evolution of eukaryotes. Yet, the root of the eukaryotic tree of life remains elusive. The most popular hypothesis in textbooks and reviews is a root between Unikonta (Opisthokonta + Amoebozoa) and Bikonta (all other eukaryotes), which emerged from analyses of a single-gene fusion. Subsequent, highly cited studies based on concatenation of genes supported this hypothesis with some variations or proposed a root within Excavata. However, concatenation of genes does not consider phylogenetically-informative events like gene duplications and losses. A recent study using gene tree parsimony (GTP) suggested the root lies between Opisthokonta and all other eukaryotes, but only including 59 taxa and 20 genes. Here we use GTP with a duplication-loss model in a gene-rich and taxon-rich dataset (i.e., 2,786 gene families from two sets of 155 and 158 diverse eukaryotic lineages) to assess the root, and we iterate each analysis 100 times to quantify tree space uncertainty. We also contrasted our results and discarded alternative hypotheses from the literature using GTP and the likelihood-based method SpeciesRax. Our estimates suggest a root between Fungi or Opisthokonta and all other eukaryotes; but based on further analysis more » of genome size, we propose that the root between Opisthokonta and all other eukaryotes is the most likely. « less
Authors:
; ; ; ;
Editors:
Phadke, Sujal
Award ID(s):
1924570
Publication Date:
NSF-PAR ID:
10356835
Journal Name:
Genome Biology and Evolution
Volume:
14
Issue:
8
ISSN:
1759-6653
Sponsoring Org:
National Science Foundation
More Like this
  1. Archibald, John (Ed.)
    Abstract Epigenetic processes in eukaryotes play important roles through regulation of gene expression, chromatin structure, and genome rearrangements. The roles of chromatin modification (e.g., DNA methylation and histone modification) and non-protein-coding RNAs have been well studied in animals and plants. With the exception of a few model organisms (e.g., Saccharomyces and Plasmodium), much less is known about epigenetic toolkits across the remainder of the eukaryotic tree of life. Even with limited data, previous work suggested the existence of an ancient epigenetic toolkit in the last eukaryotic common ancestor. We use PhyloToL, our taxon-rich phylogenomic pipeline, to detect homologs of epigenetic genes and evaluate their macroevolutionary patterns among eukaryotes. In addition to data from GenBank, we increase taxon sampling from understudied clades of SAR (Stramenopila, Alveolata, and Rhizaria) and Amoebozoa by adding new single-cell transcriptomes from ciliates, foraminifera, and testate amoebae. We focus on 118 gene families, 94 involved in chromatin modification and 24 involved in non-protein-coding RNA processes based on the epigenetics literature. Our results indicate 1) the presence of a large number of epigenetic gene families in the last eukaryotic common ancestor; 2) differential conservation among major eukaryotic clades, with a notable paucity of genes within Excavata; and 3)more »punctate distribution of epigenetic gene families between species consistent with rapid evolution leading to gene loss. Together these data demonstrate the power of taxon-rich phylogenomic studies for illuminating evolutionary patterns at scales of >1 billion years of evolution and suggest that macroevolutionary phenomena, such as genome conflict, have shaped the evolution of the eukaryotic epigenetic toolkit.« less
  2. Viruses rely on their host’s translation machinery for the synthesis of their own proteins. Problems belie viral translation when the host has a codon usage bias (CUB) that is different from an infecting virus due to differences in the GC content between the host and virus genomes. Here, we examine the hypothesis that chloroviruses adapted to host CUB by acquisition and selection of tRNAs that at least partially favor their own CUB. The genomes of 41 chloroviruses comprising three clades, each infecting a different algal host, have been sequenced, assembled and annotated. All 41 viruses not only encode tRNAs, but their tRNA genes are located in clusters. While differences were observed between clades and even within clades, seven tRNA genes were common to all three clades of chloroviruses, including the tRNAArg gene, which was found in all 41 chloroviruses. By comparing the codon usage of one chlorovirus algal host, in which the genome has been sequenced and annotated (67% GC content), to that of two of its viruses (40% GC content), we found that the viruses were able to at least partially overcome the host’s CUB by encoding tRNAs that recognize AU-rich codons. Evidence presented herein supports the hypothesis thatmore »a chlorovirus tRNA cluster was present in the most recent common ancestor (MRCA) prior to divergence into three clades. In addition, the MRCA encoded a putative isoleucine lysidine synthase (TilS) that remains in 39/41 chloroviruses examined herein, suggesting a strong evolutionary pressure to retain the gene. TilS alters the anticodon of tRNAMet that normally recognizes AUG to then recognize AUA, a codon for isoleucine. This is advantageous to the chloroviruses because the AUA codon is 12–13 times more common in the chloroviruses than their host, further helping the chloroviruses to overcome CUB. Among large DNA viruses infecting eukaryotes, the presence of tRNA genes and tRNA clusters appear to be most common in the Phycodnaviridae and, to a lesser extent, in the Mimiviridae.« less
  3. Ouangraoua, Aida (Ed.)
    Abstract Previous evolutionary reconstructions have concluded that early eukaryotic ancestors including both the last common ancestor of eukaryotes and of all fungi had intron-rich genomes. By contrast, some extant eukaryotes have few introns, underscoring the complex histories of intron–exon structures, and raising the question as to why these few introns are retained. Here, we have used recently available fungal genomes to address a variety of questions related to intron evolution. Evolutionary reconstruction of intron presence and absence using 263 diverse fungal species supports the idea that massive intron reduction through intron loss has occurred in multiple clades. The intron densities estimated in various fungal ancestors differ from zero to 7.6 introns per 1 kb of protein-coding sequence. Massive intron loss has occurred not only in microsporidian parasites and saccharomycetous yeasts, but also in diverse smuts and allies. To investigate the roles of the remaining introns in highly-reduced species, we have searched for their special characteristics in eight intron-poor fungi. Notably, the introns of ribosome-associated genes RPL7 and NOG2 have conserved positions; both intron-containing genes encoding snoRNAs. Furthermore, both the proteins and snoRNAs are involved in ribosome biogenesis, suggesting that the expression of the protein-coding genes and noncoding snoRNAs may be functionallymore »coordinated. Indeed, these introns are also conserved in three-quarters of fungi species. Our study shows that fungal introns have a complex evolutionary history and underappreciated roles in gene expression.« less
  4. Wolfe, Kenneth (Ed.)
    Abstract The DNA mismatch repair (MMR) pathway corrects mismatched bases produced during DNA replication and is highly conserved across the tree of life, reflecting its fundamental importance for genome integrity. Loss of function in one or a few MMR genes can lead to increased mutation rates and microsatellite instability, as seen in some human cancers. Although loss of MMR genes has been documented in the context of human disease and in hypermutant strains of pathogens, examples of entire species and species lineages that have experienced substantial MMR gene loss are lacking. We examined the genomes of 1,107 species in the fungal phylum Ascomycota for the presence of 52 genes known to be involved in the MMR pathway of fungi. We found that the median ascomycete genome contained 49/52 MMR genes. In contrast, four closely related species of obligate plant parasites from the powdery mildew genera Erysiphe and Blumeria, have lost between five and 21 MMR genes, including MLH3, EXO1, and DPB11. The lost genes span MMR functions, include genes that are conserved in all other ascomycetes, and loss of function of any of these genes alone has been previously linked to increased mutation rate. Consistent with the hypothesis that lossmore »of these genes impairs MMR pathway function, we found that powdery mildew genomes with higher levels of MMR gene loss exhibit increased numbers of mononucleotide runs, longer microsatellites, accelerated sequence evolution, elevated mutational bias in the A|T direction, and decreased GC content. These results identify a striking example of macroevolutionary loss of multiple MMR pathway genes in a eukaryotic lineage, even though the mutational outcomes of these losses appear to resemble those associated with detrimental MMR dysfunction in other organisms.« less
  5. Stomatopoda, commonly known as mantis shrimps, are notable for their enlarged second maxillipeds encompassing the raptorial claw. The form of the claw can be used to divide them into two basic groups: smashers and spearers. Previous phylogenetic studies of Stomatopoda have focused on morphology or a few genes, though there have been whole mitochondrial genomes published for 15 members of Stomatopoda. However, the sampling has been somewhat limited with key taxa not included. Here, nine additional stomatopod mitochondrial genomes were generated and combined with the other available mitogenomes for a phylogenetic analysis. We used the 13 protein coding genes, as well as 12S rRNA, 16S rRNA genes, and included nuclear 18S rRNA gene sequences. Different rooting options were used for the analyses: (1) single and multiple outgroups from various eumalocostracan relatives and (2) a stomatopod-only dataset, with Hemisquilla californiensis used to root the topologies, based on the current hypothesis that Hemisquilla is the sister group to the rest of Stomatopoda. The eumalocostracan-rooted analyses all showed H. californiensis nested within Stomatopoda, raising doubts as to previous hypotheses as to its placement. Allowing for the rooting difference, the H. californiensis outgroup datasets had the same tree topology as the eumalocostracan outgroup datasetsmore »with slight variation at poorly supported nodes. Of the major taxonomic groupings sampled to date, Squilloidea was generally found to be monophyletic while Gonodactyloidea was not. The position of H. californiensis was found inside its superfamily, Gonodactyloidea, and grouped in a weakly supported clade containing Odontodactylus havanensis and Lysiosquillina maculata for the eumalocostracan-rooted datasets. An ancestral state reconstruction was performed on the raptorial claw form and provides support that spearing is the ancestral state for extant Stomatopoda, with smashing evolving subsequently one or more times.« less