Protistan Diversity in the Arctic: A Case of Paleoclimate Shaping Modern Biodiversity?

The impact of climate on biodiversity is indisputable. Climate changes over geological time must have significantly influenced the evolution of biodiversity, ultimately leading to its present pattern. Here we consider the paleoclimate data record, inferring that present-day hot and cold environments should contain, respectively, the largest and the smallest diversity of ancestral lineages of microbial eukaryotes.We investigate this hypothesis by analyzing an original dataset of 18S rRNA gene sequences from Western Greenland in the Arctic, and data from the existing literature on 18S rRNA gene diversity in hydrothermal vent, temperate sediments, and anoxic water column communities. Unexpectedly, the community from the cold environment emerged as one of the richest observed to date in protistan species, and most diverse in ancestral lineages.This pattern is consistent with natural selection sweeps on aerobic non-psychrophilic microbial eukaryotes repeatedly caused by low temperatures and global anoxia of snowball Earth conditions. It implies that cold refuges persisted through the periods of greenhouse conditions, which agrees with some, although not all, current views on the extent of the past global cooling and warming events. We therefore identify cold environments as promising targets for microbial discovery

Minimum evolution phylogenetic tree of 18S rDNA sequences showing the position of ophistokont Disko Island sequences.

<p>The tree was constructed using a Tamura Nei DNA substitution model with the variable-site gamma distribution shape parameter (G) at 0.6200, and is based on 669 unambiguously aligned and conserved positions. Distance bootstrap values over 50% from an analysis of 1000 bootstrap replicates are given at the respective nodes; dots identify nodes with 100% bootstrap support. Clone names in red, blue, and green identify sequences reported in this study (DI) and from hydrothermal vent and temperate environments, respectively. The first two identifiers of the DI sequences (D1–D5) designate the different PCR primer sets used in this study (detailed information in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000728#pone-0000728-t002" target="_blank">Table 2</a>).</p

Minimum evolution phylogenetic tree of 18S rDNA sequences showing the position of autotrophic stramenopile Disko Island sequences.

<p>The tree was constructed under using a Tamura Nei substitution model with the variable-site gamma distribution shape parameter (G) at 0.7606 and the proportion of invariable sites (I) at 0.4458, and is based on 851 unambiguously aligned and conserved positions; dots identify nodes with 100% bootstrap support. Clone names in red, blue, and green identify sequences reported in this study (DI) and from hydrothermal vent and temperate environments, respectively. The first two identifiers of the DI sequences (D1–D5) designate the different PCR primer sets used in this study (detailed information in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000728#pone-0000728-t002" target="_blank">Table 2</a>).</p

Minimum evolution phylogenetic tree of 18S rDNA sequences showing the position of basal-branching Disko Island sequences.

<p>The tree was constructed under Maximum Likelihood criteria (ML) using a General Time Reversible (GTR) DNA substitution model with the variable-site gamma distribution shape parameter (G) at 1.3667, the proportion of invariable sites (I) at 0.0658, and base frequencies and a rate matrix for the substitution model as suggested by Modeltest (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000728#s3" target="_blank">Material and Methods</a>), based on 553 unambiguously aligned and conserved positions. Because of their uncertain position in phylogenetic 18S rDNA sequence trees, the branching orders of the primitive jakobid flagellates and the <i>Myrionecta</i>/<i>Mesodinium</i> (Ciliophora) group are not supported. For a detailed explanation of the basal branching of the latter group see e.g. <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000728#pone.0000728-Zuendorf1" target="_blank">[31]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000728#pone.0000728-Johnson1" target="_blank">[68]</a>. Distance bootstrap values over 50% from an analysis of 1000 bootstrap replicates are given at the respective nodes; dots identify nodes with 100% bootstrap support. Clone names in red, blue, and green identify sequences reported in this study (DI) and from hydrothermal vent and temperate environments, respectively. The first two identifiers of the DI sequences (D1–D5) designate the different PCR primer sets used in this study (detailed information in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000728#pone-0000728-t002" target="_blank">Table 2</a>).</p

Minimum evolution phylogenetic tree of 18S rDNA sequences showing the position of rhizarian Disko Island sequences.

<p>The tree was constructed under Maximum Likelihood criteria (ML) using a General Time Reversible (GTR) DNA substitution model with the variable-site gamma distribution shape parameter (G) at 0.8312 and the proportion of invariable sites (I) at 0.2533, and is based on 817 unambiguously aligned and conserved positions. Distance bootstrap values over 50% from an analysis of 1000 bootstrap replicates are given at the respective nodes; dots identify nodes with 100% bootstrap support. Clone names in red, blue, and green identify sequences reported in this study (DI) and from hydrothermal vent and temperate environments, respectively. The first two identifiers of the DI sequences (D1–D5) designate the different PCR primer sets used in this study (detailed information in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000728#pone-0000728-t002" target="_blank">Table 2</a>).</p

Minimum evolution phylogenetic tree of 18S rDNA sequences showing the position of euglenozoan Disko Island sequences.

<p>The tree was constructed under Maximum Likelihood criteria (ML) using a General Time Reversible (GTR) DNA substitution model with the variable-site gamma distribution shape parameter (G) at 0.8904 and the proportion of invariable sites (I) at 0.1517, and is based on 730 unambiguously aligned and conserved positions. Distance bootstrap values over 50% from an analysis of 1000 bootstrap replicates are given at the respective nodes; dots identify nodes with 100% bootstrap support. Clone names in red, blue, and green identify sequences reported in this study (DI) and from hydrothermal vent and temperate environments, respectively. The first two identifiers of the DI sequences (D1–D5) designate the different PCR primer sets used in this study (detailed information in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000728#pone-0000728-t002" target="_blank">Table 2</a>).</p

18S rDNA Maximum Parsimony (MP) tree showing the assignment of Disko Island phylotypes to major eukaryote clades.

<p>The numbers a/b indicate the total number of GenBank sequences representing the clade/the number of phylotypes detected. Ancestral sequences to a specific clade were included in the clade itself. Only protistan and fungal sequences are shown in the tree. Detailed phylogenies (partial treeing analyses) can be found in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000728#pone-0000728-g002" target="_blank">Figures 2</a>–<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000728#pone-0000728-g003" target="_blank"></a><a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000728#pone-0000728-g004" target="_blank"></a><a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000728#pone-0000728-g005" target="_blank"></a><a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000728#pone-0000728-g006" target="_blank"></a><a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000728#pone-0000728-g007" target="_blank"></a><a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000728#pone-0000728-g008" target="_blank"></a><a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000728#pone-0000728-g009" target="_blank"></a><a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000728#pone-0000728-g010" target="_blank">10</a>.</p

Minimum evolution phylogenetic tree of 18S rDNA sequences showing the position of apicomplexan and perkinsozoan Disko Island phylotypes (Alveolata).

<p>The tree was constructed under Maximum Likelihood criteria (ML) using a General Time Reversible (GTR) DNA substitution model with the variable-site gamma distribution shape parameter (G) at 0.6830 and the proportion of invariable sites (I) at 0.1125, and is based on 784 unambiguously aligned and conserved positions. Distance bootstrap values over 50% from an analysis of 1000 bootstrap replicates are given at the respective nodes; dots identify nodes with 100% bootstrap support. Clone names in red, blue, and green identify sequences reported in this study (DI) and from hydrothermal vent and temperate environments, respectively. The first two identifiers of the DI sequences (D1–D5) designate the different PCR primer sets used in this study (detailed information in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000728#pone-0000728-t002" target="_blank">Table 2</a>).</p

Minimum evolution phylogenetic tree of 18S rDNA sequences showing the position of heterotrophic stramenopile Disko Island sequences.

<p>The tree was constructed using a Tamura Nei DNA substitution model with the variable-site gamma distribution shape parameter (G) at 0.6830 and the proportion of invariable sites (I) at 0.1125, and is based on 784 unambiguously aligned and conserved positions. Distance bootstrap values over 50% from an analysis of 1000 bootstrap replicates are given at the respective nodes; dots identify nodes with 100% bootstrap support. Clone names in red, blue, and green identify sequences reported in this study (DI) and from hydrothermal vent and temperate environments, respectively. The first two identifiers of the DI sequences (D1–D5) designate the different PCR primer sets used in this study (detailed information in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000728#pone-0000728-t002" target="_blank">Table 2</a>).</p