Diversity and vertical distribution of microbial eukaryotes in the snow, sea ice and seawater near the north pole at the end of the polar night

Abstract

Our knowledge about the microorganisms living in the high Arctic Ocean is still rudimentary compared to other oceans mostly because of logistical challenges imposed by its inhospitable climate and the presence of a multi-year ice cap. We have used 18S rRNA gene libraries to study the diversity of microbial eukaryotes in the upper part of the water column (0-170 m depth), the sea ice (0-1.5 m depth) and the overlying snow from samples collected in the vicinity of the North Pole (N88°35', E015°59) at the very end of the long polar night. We detected very diverse eukaryotes belonging to Alveolata, Fungi, Amoebozoa, Viridiplantae, Metazoa, Rhizaria, Heterokonta, and Telonemia. Different alveolates (dinoflagellates and Marine Alveolate Groups I and II species) were the most abundant and diverse in gene libraries from water and sea ice, representing 80% of the total number of clones and operational taxonomic units. Only contaminants and/or species from continental ecosystems were detected in snow, suggesting wind- and animal- or human-mediated cosmopolitan dispersal of some taxa. By contrast, sea ice and seawater samples harbored a larger and more similar inter-sample protist diversity as compared with snow. The North Pole was found to harbor distinctive eukaryotic communities along the vertical gradient with an unparalleled diversity of core dinoflagellates, largely dominant in libraries from the water column, as compared to other oceanic locations. In contrast, phototrophic organisms typical of Arctic sea ice and plankton, such as diatoms and prasinophytes, were very rare in our samples. This was most likely due to a decrease of their populations after several months of polar night darkness and to the presence of rich populations of diverse grazers. Whereas strict phototrophs were scarce, we identified a variety of likely mixotrophic taxa, which supports the idea that mixotrophy may be important for the survival of diverse protists through the long polar night.

Keywords: North Pole; alveolates; arctic; dinoflagellates; plankton; protist diversity; sea ice.

Figure 1

Origin of samples. (A) Sampling site in the Arctic Ocean, the boxed area shows the path of the Barneo-2008 expedition; (B) profile of the sampling depths from the upper snow layer, through the ice cover, to the bottom of the euphotic zone. Base map is the International Bathymetric Chart of the Arctic Ocean (Jakobsson et al., 2008).

Figure 2

Relative 18S rDNA abundance of major eukaryotic groups in gene libraries from samples near the North Pole. For sample names, see Figure 1.

Figure 3

Heatmaps comparing the diversity of eukaryotes among samples using the shared OTUs defined at clustering identity of 98% (left) or 95% (right). Scale bar: Theta_YC coefficient as measure of similarity between the structures of two communities, ranging from 0 (black) to 1 (red).

Figure 4

Maximum likelihood phylogenetic tree of ciliate phylotypes. Names in italics correspond to cultivated species or strains, while the rest correspond to 18S rDNA environmental clones. Names in bold correspond to clones retrieved in this study, numbers in parentheses indicating the number of clones for each phylotype in the different libraries. Accession numbers are given in brackets. Long branches shortened to one half of their length are indicated by (1/2). Maximum likelihood bootstrap values above 50% are indicated at nodes, and Bayesian posterior probabilities higher than 0.90 are indicated by filled circles.

Figure 5

Maximum likelihood phylogenetic tree of Marine Alveolate Group I and II (Syndiniales) phylotypes. The tree was rooted with perkinsozoan sequences (not shown).

Figure 6

Maximum likelihood phylogenetic tree of core dinoflagellate phylotypes. The tree was rooted with perkinsozoan sequences (not shown).

Figure 7

Maximum likelihood phylogenetic tree of diverse animal, fungal and amoebozoan phylotypes.

Figure 8

Maximum likelihood phylogenetic tree of diverse heterokont, green algae and plant, telonemid and rhizarian phylotypes.