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. 2012 Oct 1;48(5):1130-1142.
doi: 10.1111/j.1529-8817.2012.01194.x. Epub 2012 Jun 19.

ANALYSIS OF ALEXANDRIUM TAMARENSE (DINOPHYCEAE) GENES REVEALS THE COMPLEX EVOLUTIONARY HISTORY OF A MICROBIAL EUKARYOTE()

Cheong Xin Chan  1 , Marcelo B Soares, Maria F Bonaldo, Jennifer H Wisecaver, Jeremiah D Hackett, Donald M Anderson, Deana L Erdner, Debashish Bhattacharya
Affiliations

ANALYSIS OF ALEXANDRIUM TAMARENSE (DINOPHYCEAE) GENES REVEALS THE COMPLEX EVOLUTIONARY HISTORY OF A MICROBIAL EUKARYOTE()

Cheong Xin Chan et al. J Phycol. .

Abstract

Microbial eukaryotes may extinguish much of their nuclear phylogenetic history due to endosymbiotic/horizontal gene transfer (E/HGT). We studied E/HGT in 32,110 contigs of expressed sequence tags (ESTs) from the dinoflagellate Alexandrium tamarense (Dinophyceae) using a conservative phylogenomic approach. The vast majority of predicted proteins (86.4%) in this alga are novel or dinoflagellate-specific. We searched for putative homologs of these predicted proteins against a taxonomically broadly sampled protein database that includes all currently available data from algae and protists and reconstructed a phylogeny from each of the putative homologous protein sets. Of the 2,523 resulting phylogenies, 14-17% are potentially impacted by E/HGT involving both prokaryote and eukaryote lineages, with 2-4% showing clear evidence of reticulate evolution. The complex evolutionary histories of the remaining proteins, many of which may also have been affected by E/HGT, cannot be interpreted using our approach with currently available gene data. We present empirical evidence of reticulate genome evolution that combined with inadequate or highly complex phylogenetic signal in many proteins may impede genome-wide approaches to infer the tree of microbial eukaryotes.

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Figures

FIGURE 1
FIGURE 1
The putative eukaryote tree of life (TOL). (A) Schematic tree showing major endosymbiotic/horizontal gene transfer (E/HGT) events that have occurred as a result of plastid evolution. The contribution of genes from lineages of the red and green algae is thought to be prominent in most chromalveolate (including dinoflagellates), whereas haptophyte-derived genes are known to be present in fucoxanthin-type dinoflagellates. Other dinoflagellates have undergone tertiary endosymbiosis with different algae (Hackett et al. 2004). The arrows represent instances of gene transfer/sharing. The grouping of “Chromalveolata”, in which the ancestral branch is shown as a dashed line remains controversial in the literature. (B) The number of Alexandrium tamarense genes used in this study, breakdown by those with no hits in the current database, those with hits only in dinoflagellates, and those with hits with other taxa.
FIGURE 2
FIGURE 2
Evolutionary origins of dinoflagellate protein families. (A) The distribution of phyla with exclusive BLASTP hits to A. tamarense proteins, across the minimum number of hits per query, x ≥2, ≥5, ≥10, and ≥15. The different phyla that share proteins exclusively with A. tamarense are shown. For each bar, the number of proteins for each phylum is shown, with the total on top. (B) Distribution of phyla that are found to share genes with dinoflagellates, based on the number of protein phylogenies in which a strongly supported (bootstrap ≥90%) monophyly between these phyla and dinoflagellates was recovered. This distribution is also shown for (C) bootstrap ≥70% and (D) bootstrap ≥50%. In these cases, at least two dinoflagellate sequences and two from the sister taxon are required to be counted as a monophyletic lineage at the prescribed bootstrap cut-off value.
FIGURE 3
FIGURE 3
Phylogeny of acyl-CoA dehydrogenase that provides evidence of an HGT event involving dinoflagellates and fungi. Non-parametric bootstrap support values ≥50% are shown at the nodes of the tree. Dinoflagellates are highlighted in boldface. The unit of branch length is in the number of substitutions per site.
FIGURE 4
FIGURE 4
Examples of proteins that have an origin in dinoflagellates via E/HGT. (A) Phylogeny of genes encoding the DNA-binding major basic nuclear proteins in dinoflagellates that has a proteobacterial HGT origin prior to the diversification of these algal taxa. (B) Phylogeny of a gene encoding a GTP-binding protein of the YchF family. This tree shows strong bootstrap support (97%) for a shared origin of the gene in picoprasinophytes and dinoflagellates. For both trees, non-parametric bootstrap support values ≥50% are shown at the nodes. Dinoflagellates are highlighted in boldface. The unit of branch length is in the number of substitutions per site.
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