Winter bloom of a rare betaproteobacterium in the Arctic Ocean

Abstract

Extremely low abundance microorganisms (members of the "rare biosphere") are believed to include dormant taxa, which can sporadically become abundant following environmental triggers. Yet, microbial transitions from rare to abundant have seldom been captured in situ, and it is uncertain how widespread these transitions are. A bloom of a single ribotype (≥99% similarity in the 16S ribosomal RNA gene) of a widespread betaproteobacterium (Janthinobacterium sp.) occurred over 2 weeks in Arctic marine waters. The Janthinobacterium population was not detected microscopically in situ in January and early February, but suddenly appeared in the water column thereafter, eventually accounting for up to 20% of bacterial cells in mid February. During the bloom, this bacterium was detected at open water sites up to 50 km apart, being abundant down to more than 300 m. This event is one of the largest monospecific bacterial blooms reported in polar oceans. It is also remarkable because Betaproteobacteria are typically found only in low abundance in marine environments. In particular, Janthinobacterium were known from non-marine habitats and had previously been detected only in the rare biosphere of seawater samples, including the polar oceans. The Arctic Janthinobacterium formed mucilagenous monolayer aggregates after short (ca. 8 h) incubations, suggesting that biofilm formation may play a role in maintaining rare bacteria in pelagic marine environments. The spontaneous mass occurrence of this opportunistic rare taxon in polar waters during the energy-limited season extends current knowledge of how and when microbial transitions between rare and abundant occur in the ocean.

Keywords: Arctic; Janthinobacterium; betaproteobacteria; biofilm; bloom; rare biosphere.

Figure 1

Map showing the location of the stations in this study and the dates when they were sampled in 2008. Two different samples were collected at station D19 while the research vessel was passively drifting with the ice. Filled dots represent stations where Janthinobacterium cells were detected in situ by CARD-FISH, and their contribution (in percentage of total cells) are shown.

Figure 2

Depth profiles of temperature, salinity and concentration of nitrate during the study. The dotted blue line corresponds to the temperature profile on January 28th, when an oceanographic eddy crossed the Arctic area of study. The yellow line correspond to the station where Janthinobacterium was first detected in situ and orange lines correspond to the stations where maximal abundances of Janthinobacterium were found by CARD-FISH.

Figure 3

Maximum-likelihood phylogenetic tree of sequences affiliated with Janthinobacterium including the environmental clones retrieved from Arctic seawater (highlighted in bold) from the clone libraries constructed with DNA from different size-fractions. Janthinobacterium representatives with their genomes sequenced have also been highlighted in bold, and those isolated from cold environments (including ice, snow, glacier melt waters and high-mountain lakes) appear in blue. Isolation sources are shown to the right. The tree was rooted with a clade containing sequences of Burkholderia spp. (full tree is shown in Supplementary Figure 4), and bootstrap values based on 1000 replicates (>50%) are indicated on the branches. The pie charts show the proportion of clones affiliated with different bacterial phylogenetic groups as identified by the RDP classifier in the small and large size-fraction clone libraries (Verruco: Verrucomicrobia, Alpha: Alphaproteobacteria, Beta: Betaproteobacteria, Gamma: Gammaproteobacteria, Delta: Deltaproteobacteria, Janthino: Janthinobacterium).

Figure 4

Temporal dynamics of the in situ abundance of Janthinobacterium (probe Jan64) in surface Arctic seawater as analyzed by CARD-FISH (A), and abundances reached by the same population after 8 h incubations (for MAR-CARD-FISH analysis) of the corresponding environmental samples (B). Fluorescence microscope images of Arctic Janthinobacterium cells in situ (where they appeared mostly as single-cells) and in the MAR-CARD-FISH incubations (where they formed mucilaginous aggregates) are shown on the right side. The arrows in (A) indicate the day that an eddy crossed the Arctic area of study and the presence of strong spring tides due to the full moon on February 7th. Specific growth rates (h⁻¹) of Janthinobacterium estimated in the incubations from February 11th to March 2nd are shown in the gray circles below the graph in (B). All samples were collected onboard at 12 m depth, except for the MAR-CARD-FISH sample from February 5th, which was collected at 5 m depth through a hole in the ice. Replicate counts are shown when available.

Figure 5

Microscope images of the Arctic Janthinobacterium population (right) and all cells stained with DAPI (left) in a sample collected on February 25th. Some of the hybridized cells are highlighted with arrows in the DAPI images.

Figure 6

Abundance of Janthinobacterium down the depth profile on the two dates when maximal abundances were found (February 18th and 25th), as analyzed by CARD-FISH.