Diversity and genomics of Antarctic marine micro-organisms

Abstract

Marine bacterioplanktons are thought to play a vital role in Southern Ocean ecology and ecosystem function, as they do in other ocean systems. However, our understanding of phylogenetic diversity, genome-enabled capabilities and specific adaptations to this persistently cold environment is limited. Bacterioplankton community composition shifts significantly over the annual cycle as sea ice melts and phytoplankton bloom. Microbial diversity in sea ice is better known than that of the plankton, where culture collections do not appear to represent organisms detected with molecular surveys. Broad phylogenetic groupings of Antarctic bacterioplankton such as the marine group I Crenarchaeota, alpha-Proteobacteria (Roseobacter-related and SAR-11 clusters), gamma-Proteobacteria (both cultivated and uncultivated groups) and Bacteriodetes-affiliated organisms in Southern Ocean waters are in common with other ocean systems. Antarctic SSU rRNA gene phylotypes are typically affiliated with other polar sequences. Some species such as Polaribacter irgensii and currently uncultivated gamma-Proteobacteria (Ant4D3 and Ant10A4) may flourish in Antarctic waters, though further studies are needed to address diversity on a larger scale. Insights from initial genomics studies on both cultivated organisms and genomes accessed through shotgun cloning of environmental samples suggest that there are many unique features of these organisms that facilitate survival in high-latitude, persistently cold environments.

Figure 1

Seasonal variation in bacterial community structure over two annual cycles in nearshore waters off Palmer Station, Antarctica. Data are based on the presence/absence of bands in denaturing gradient electrophoresis. Pairwise similarity (Sorenson's index, C_S) calculated for all months with respect to the August profile is plotted on the y-axis and the months are plotted on the x-axis. The black line is drawn at the 50% similarity level. Data from 1996–1997 were presented previously (Murray et al. 1998).

Figure 2

Distribution of bacterial and archaeal phylogenetic groups based on SSU rDNA sequences in a PCR-based bacterial clone library prepared from seawater in mid-October 2001 (black bars), a PCR-based bacterial clone library prepared from sea ice in mid-October 2001 (stripped bars), in an environmental shotgun library prepared from picoplankton DNA collected in late August 1996 (open bars), in a bacterial culture collection from seawater and sea ice collected in October 2001 and 2002 (dotted bars) and a PCR-based archaeal clone library prepared with seawater in mid-October 2001 (grey bars).

Figure 3

Neighbour-joining tree showing phylogenetic relationships between Antarctic marine plankton and sea-ice α-Proteobacteria and many of their nearest neighbours isolated or directly sequenced from marine environments. Sequences from SSU rRNA gene bacterioplankton libraries are indicated by filled triangles, sea-ice bacterial clones by open diamonds and shotgun clone library by filled circles.

Figure 4

Neighbour-joining tree showing phylogenetic relationships between Antarctic marine plankton and sea-ice γ-Proteobacteria and many of their nearest neighbours isolated or directly sequenced from marine environments. Symbols are as described in figure 3 but shotgun clone libraries are indicated by open circles and in addition, open squares represent sequences for cultivated organisms and nodes representing both SSU rRNA gene libraries.

Figure 5

Neighbour-joining tree showing phylogenetic relationships between Antarctic marine plankton and sea-ice Bacteriodetes-related sequences and many of their nearest neighbours isolated or directly sequenced from marine environments. Symbols are the same as in figures 3 and 4.

Figure 6

Three indices of amino acid modification in the predicted coding regions of Antarctic proteins: (a) reduced proline content, (b) reduction in the arginine ratio (arg/arg+lys), and (c) reduction in acidic residues (Asn+Gln/Asn+Gln+Glu+Asp). Proteins compared here had at least two homologues with Blast e-scores less than 10⁻¹⁵. Black bars represent number of Antarctic open reading frames in comparison to mesophilic homologues with G+C content ±2.5% that of the Antarctic sequence. Grey bars represent data compared to the UniSwiss database (all characterized proteins). All data are significant based on a one-sample Student's t-test (p<0.05).