Pole-to-pole biogeography of surface and deep marine bacterial communities

Abstract

The Antarctic and Arctic regions offer a unique opportunity to test factors shaping biogeography of marine microbial communities because these regions are geographically far apart, yet share similar selection pressures. Here, we report a comprehensive comparison of bacterioplankton diversity between polar oceans, using standardized methods for pyrosequencing the V6 region of the small subunit ribosomal (SSU) rRNA gene. Bacterial communities from lower latitude oceans were included, providing a global perspective. A clear difference between Southern and Arctic Ocean surface communities was evident, with 78% of operational taxonomic units (OTUs) unique to the Southern Ocean and 70% unique to the Arctic Ocean. Although polar ocean bacterial communities were more similar to each other than to lower latitude pelagic communities, analyses of depths, seasons, and coastal vs. open waters, the Southern and Arctic Ocean bacterioplankton communities consistently clustered separately from each other. Coastal surface Southern and Arctic Ocean communities were more dissimilar from their respective open ocean communities. In contrast, deep ocean communities differed less between poles and lower latitude deep waters and displayed different diversity patterns compared with the surface. In addition, estimated diversity (Chao1) for surface and deep communities did not correlate significantly with latitude or temperature. Our results suggest differences in environmental conditions at the poles and different selection mechanisms controlling surface and deep ocean community structure and diversity. Surface bacterioplankton may be subjected to more short-term, variable conditions, whereas deep communities appear to be structured by longer water-mass residence time and connectivity through ocean circulation.

Fig. 1.

Polar oriented maps of sample locations in the Southern (A) and Northern (B) hemispheres, including Southern Ocean (pink), Arctic (blue), and lower latitudes (gray).

Fig. 2.

Unweighted pair group method with arithmetic mean (UPGMA) dendrogram based on Bray–Curtis dissimilarities of V6 16 rRNA tags from pelagic samples taken in Arctic (blue), Southern Ocean (purple), and in lower latitudes (gray). The x axis represents Bray–Curtis dissimilarity. Ecosystem clusters are represented with labels and letters A through I. Sample names at left are encoded as ocean region, VAMPS code number, open (O) or coastal (C) sites, and water depth in meters. Polar ocean regions in the Southern Ocean (SO) are Amundsen Sea (AS), Antarctic Peninsula (AP), Kerguelen Islands (KI), Ross Sea (RS), and Weddell Sea (WS). In the Arctic Ocean (AO), regions sampled are Baffin Bay (BB), Beaufort Sea (BS), Chukchi Sea (CS), East Siberian Sea (ES), and Franklin Bay (FB). A sample name followed by an asterisk refers to winter sampling.

Fig. 3.

Diversity accumulation in deep vs. surface communities represented by the percentage of OTUs in a dataset when the sequence similarity threshold used to define OTUs increases. Datasets included Mediterranean Sea (MS), Azores (AZ), North Atlantic (NA), South Pacific (SP), Arctic Ocean (AO) and Southern Ocean (SO).

Fig. 4.

Bacterial OTUs associated with the polar ecosystem clusters identified in Fig. 2 (clusters A to H). SSU rRNA gene tags (distance of 0.03) were averaged across each ecosystem cluster (3–29 samples per cluster) and summed across the eight polar ecosystems. Shown are OTUs representing 5% or greater in each compared ecosystem cluster (totaling 28 OTUs), where the circle size corresponds to the relative average abundance the OTU in each cluster. OTUs assigned to the highest taxonomic level possible using a Bayesian classification tool (RDP) BLAST and sequence alignments to polar SSU rRNA gene clone libraries, are grouped phylogenetically on the vertical dimension. OTUs with average relative abundances < 0.01 (rare OTUs in a fraction of the samples in an ecosystem cluster) are indicated with an x, whereas very low values (0.01–0.5) appear as a continuation of dashes. Pairwise comparisons of ecosystem clusters (delimited with vertical black lines and gray background) were conducted using SIMPER to determine OTUs contributing to dissimilarity between the clusters. Dominant tags (top five to six OTUs) that contributed to dissimilarity between two clusters are in white. For example, the six frequent OTUs explaining the dissimilarity between the coastal surface summer samples in the Antarctic and the Arctic included three Antarctic OTUs: Sulfitobacter, OMGAnt4D3-cluster1, Gammaproteobacterium HTTC 2207-Cluster1, and three Arctic OTUs: Burkholderiales, Polaribacter, and Microbacteriaceae); the discerning OTUs are often distributed between the two clusters being compared.