Diversity and distribution of marine microbial eukaryotes in the Arctic Ocean and adjacent seas

Abstract

We analyzed microbial eukaryote diversity in perennially cold arctic marine waters by using 18S rRNA gene clone libraries. Samples were collected during concurrent oceanographic missions to opposite sides of the Arctic Ocean Basin and encompassed five distinct water masses. Two deep water Arctic Ocean sites and the convergence of the Greenland, Norwegian, and Barents Seas were sampled from 28 August to 2 September 2002. An additional sample was obtained from the Beaufort Sea (Canada) in early October 2002. The ribotypes were diverse, with different communities among sites and between the upper mixed layer and just below the halocline. Eukaryotes from the remote Canada Basin contained new phylotypes belonging to the radiolarian orders Acantharea, Polycystinea, and Taxopodida. A novel group within the photosynthetic stramenopiles was also identified. One sample closest to the interior of the Canada Basin yielded only four major taxa, and all but two of the sequences recovered belonged to the polar diatom Fragilariopsis and a radiolarian. Overall, 42% of the sequences were <98% similar to any sequences in GenBank. Moreover, 15% of these were <95% similar to previously recovered sequences, which is indicative of endemic or undersampled taxa in the North Polar environment. The cold, stable Arctic Ocean is a threatened environment, and climate change could result in significant loss of global microbial biodiversity.

FIG. 1.

Map showing sites sampled. European Arctic sites GNB-M09 and GNB-Z59 were south of Svalbard in the GNB. North American sites were in (AO-NW08) and on the border of (AO-NW01) the Canada Basin and from the Beaufort Sea-Mackenzie Delta region (BS-MD65).

FIG. 2.

Novelty or discovery histogram of sequences from this study, binned by 0.5% identity to sequences in GenBank (x axis). The y axis (counts) shows the number of sequences in each bin.

FIG. 3.

NJ tree of partial 18S rRNA gene sequences from all taxonomic clades reported here (boldface). Sequences with >99% similarity were pruned from the tree for clarity. Palmata palmata is the red algal outgroup. Choanoflagellates are shown separately, as these were difficult to align within the larger tree. For Fig. 3 to 6 the scale bars represent 0.1 nucleotide substitution per site; the actual value depends on the branch lengths in the tree.

FIG. 4.

Classification of photosynthetic stramenopiles (PS) from this study (boldface). Panel a shows the overall ML tree structure from 1,710-bp alignments of the 18S rRNA gene, showing the position of a novel PS cluster (represented by clone NW414.14) within the photosynthetic heterokonts. Panels b to d show the remainder of all PS environmental sequences from this study (boldface) over 750 bp. (b) The novel phototrophic stramenopile cluster and bolidophytes from this study; (c) centric diatoms; (d) mostly araphid diatoms. ML trees are shown; NJ and Bayesian trees had similar topologies. Bayesian clade support was 100% at major branches.

FIG.5.

ML analysis of 750-bp fragments of our alveolate sequences (boldface) and closest GenBank matches. The three trees were rooted using alveolates from outside the group treated (the outgroup has been removed from the tree for clarity). (a) Dinoflagellates; (b) group I and group II alveolates; (c) ciliates (Strom A and B are two distinct Strombidium clusters). NJ and Bayesian trees were topologically similar, and nodes were supported by 97 to 100% Bayesian posterior probabilities (not shown). Distance measures are for ML.

FIG. 6.

(a) ML tree derived from 1,750-bp sequences indicating the overall position of the rhizarian sequences from this study (boldface), with a choanoflagellate root. Topology was essentially the same for NJ and Bayesian trees, with 100% clade support at all main branches. (b to d) Expansions to include our partial environmental sequences (750 bp) from the three radiolarian groups: Acantharea (b), Spumellarida (c), and Taxopodida/Spongodiscidae (d) (see text). Distance measures are for ML.