Jeremiah D Hackett

The importance of 'eco-evolutionary feedbacks' in natural systems is currently unclear. Here, we advance a general hypothesis for a particular class of eco-evolutionary feedbacks with potentially large, long-lasting impacts in complex ecosystems. These eco-evolutionary feedbacks involve traits that mediate important interactions with abiotic and biotic features of the environment and a self-driven reversal of selection as the ecological impact of the trait varies between private (small scale) and public (large scale). Toxic algal blooms may involve such eco-evolutionary feedbacks due to the emergence of public goods. We review evidence that toxin production by microalgae may yield 'privatised' benefits for individual cells or colonies under pre- and early-bloom conditions; however, the large-scale, ecosystem-level effects of toxicity associated with bloom states yield benefits that are necessarily 'public'. Theory predicts that the replacement of private with public goods may reverse selection for toxicity in the absence of higher level selection. Indeed, blooms often harbor significant genetic and functional diversity: bloom populations may undergo genetic differentiation over a scale of days, and even genetically similar lineages may vary widely in toxic potential. Intriguingly, these observations find parallels in terrestrial communities, suggesting that toxic blooms may serve as useful models for eco-evolutionary dynamics in nature. Eco-evolutionary feedbacks involving the emergence of a public good may shed new light on the potential for interactions between ecology and evolution to influence the structure and function of entire ecosystems.

Abstract:

Phylomes (comprehensive sets of gene phylogenies for organisms) are built to investigate fundamental questions in genomics and evolutionary biology, such as those pertaining to the detection and characterization of horizontal gene transfer in microbes. To address these questions, phylome construction demands rigorous yet efficient phylogenetic methods. Currently, many sequence alignment and tree-building models can analyze several thousands of genes in a high-throughput manner. However, the phylogenetics is complicated by variability in sequence divergence and different taxon sampling among genes. In addition, homolog selection for automated approaches often relies on arbitrary sequence similarity thresholds that are likely inappropriate for all genes in a genome. To investigate the effects of automated homolog selection on the detection of horizontal gene transfer using phylogenomics, we constructed the phylome of a transcriptome assembly of Alexandrium tamarense, a microbial eukaryote with a history of horizontal and endosymbiotic gene transfer, using seven sequence similarity thresholds for selecting putative homologs to be included in phylogenetic analyses. We show that no single threshold recovered informative trees for the majority of A. tamarense unigenes compared to the pooled results from all pipeline iterations. As much as 29% of trees built could have misleading phylogenetic relationships that appear biased in favor of those otherwise indicative of horizontal gene transfer. Perhaps worse, nearly half of the unigenes were represented by a single tree built at just one threshold, making it difficult to assess the validity of phylogenetic relationships recovered in these cases. However, combining the results from several pipeline iterations maximizes the number of informative phylogenies. Moreover, when the same phylogenetic relationship for a given unigene is recovered in multiple pipeline iterations, conclusions regarding gene origin are more robust to methodological artifact. Using these methods, the majority of A. tamarense unigenes showed evolutionary relationships indicative of vertical inheritance. Nevertheless, many other unigenes revealed diverse phylogenetic associations, suggestive of possible gene transfer. This analysis suggests that caution should be used when interpreting the results from phylogenetic pipelines implementing a single similarity threshold. Our approach is a practical method to mitigate the problems associated with automated sequence selection in phylogenomics. © 2013 Elsevier Inc.

Dinoflagellates are important aquatic primary producers and cause "red tides." The most widespread plastid (photosynthetic organelle) in these algae contains the unique accessory pigment peridinin. This plastid putatively originated via a red algal secondary endosymbiosis and has some remarkable features, the most notable being a genome that is reduced to 1-3 gene minicircles with about 14 genes (out of an original 130-200) remaining in the organelle and a nuclear-encoded proteobacterial Form II Rubisco. The "missing" plastid genes are relocated to the nucleus via a massive transfer unequaled in other photosynthetic eukaryotes. The fate of these characters is unknown in a number of dinoflagellates that have replaced the peridinin plastid through tertiary endosymbiosis. We addressed this issue in the fucoxanthin dinoflagellates (e.g., Karenia brevis) that contain a captured haptophyte plastid. Our multiprotein phylogenetic analyses provide robust support for the haptophyte plastid replacement and are consistent with a red algal origin of the chromalveolate plastid. We then generated an expressed sequence tag (EST) database of 5,138 unique genes from K. brevis and searched for nuclear genes of plastid function. The EST data indicate the loss of the ancestral peridinin plastid characters in K. brevis including the transferred plastid genes and Form II Rubisco. These results underline the remarkable ability of dinoflagellates to remodel their genomes through endosymbiosis and the considerable impact of this process on cell evolution.

Abstract:

Expressed Sequence Tags (ESTs) provide a rapid and efficient approach for gene discovery and analysis of gene expression in eukaryotes. ESTs have also become particularly important with recent expanded efforts in complete genome sequencing of understudied, nonmodel eukaryotes such as protists and algae. For these projects, ESTs provide an invaluable source of data for gene identification and prediction of exon-intron boundaries. The generation of EST data, although straightforward in concept, requires nonetheless great care to ensure the highest efficiency and return for the investment in time and funds. To this end, key steps in the process include generation of a normalized cDNA library to facilitate a high gene discovery rate followed by serial subtraction of normalized libraries to maintain the discovery rate. Here we describe in detail, protocols for normalization and subtraction of cDNA libraries followed by an example using the toxic dinoflagellate Alexandrium tamarense. © 2009 Humana Press, a part of Springer Science+Business Media, LLC.

PMID: 20300646;PMCID: PMC2837391;Abstract:

Background: Dinoflagellates are unicellular, often photosynthetic protists that play a major role in the dynamics of the Earth's oceans and climate. Sequencing of dinoflagellate nuclear DNA is thwarted by their massive genome sizes that are often several times that in humans. However, modern transcriptomic methods offer promising approaches to tackle this challenging system. Here, we used massively parallel signature sequencing (MPSS) to understand global transcriptional regulation patterns in Alexandrium tamarense cultures that were grown under four different conditions. Methodology/Principal Findings: We generated more than 40,000 unique short expression signatures gathered from the four conditions. Of these, about 11,000 signatures did not display detectable differential expression patterns. At a p-value , 1E-10, 1,124 signatures were differentially expressed in the three treatments, xenic, nitrogen-limited, and phosphoruslimited, compared to the nutrient-replete control, with the presence of bacteria explaining the largest set of these differentially expressed signatures. Conclusions/Significance: Among microbial eukaryotes, dinoflagellates contain the largest number of genes in their nuclear genomes. These genes occur in complex families, many of which have evolved via recent gene duplication events. Our expression data suggest that about 73% of the Alexandrium transcriptome shows no significant change in gene expression under the experimental conditions used here and may comprise a "core" component for this species. We report a fundamental shift in expression patterns in response to the presence of bacteria, highlighting the impact of biotic interaction on gene expression in dinoflagellates. © 2010 Moustafa et al.