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Diazotroph Diversity in the Sea Ice, Melt Ponds, and Surface Waters of the Eurasian Basin of the Central Arctic Ocean

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ABSTRACT

The Eurasian basin of the Central Arctic Ocean is nitrogen limited, but little is known about the presence and role of nitrogen-fixing bacteria. Recent studies have indicated the occurrence of diazotrophs in Arctic coastal waters potentially of riverine origin. Here, we investigated the presence of diazotrophs in ice and surface waters of the Central Arctic Ocean in the summer of 2012. We identified diverse communities of putative diazotrophs through targeted analysis of the nifH gene, which encodes the iron protein of the nitrogenase enzyme. We amplified 529 nifH sequences from 26 samples of Arctic melt ponds, sea ice and surface waters. These sequences resolved into 43 clusters at 92% amino acid sequence identity, most of which were non-cyanobacterial phylotypes from sea ice and water samples. One cyanobacterial phylotype related to Nodularia sp. was retrieved from sea ice, suggesting that this important functional group is rare in the Central Arctic Ocean. The diazotrophic community in sea-ice environments appear distinct from other cold-adapted diazotrophic communities, such as those present in the coastal Canadian Arctic, the Arctic tundra and glacial Antarctic lakes. Molecular fingerprinting of nifH and the intergenic spacer region of the rRNA operon revealed differences between the communities from river-influenced Laptev Sea waters and those from ice-related environments pointing toward a marine origin for sea-ice diazotrophs. Our results provide the first record of diazotrophs in the Central Arctic and suggest that microbial nitrogen fixation may occur north of 77°N. To assess the significance of nitrogen fixation for the nitrogen budget of the Arctic Ocean and to identify the active nitrogen fixers, further biogeochemical and molecular biological studies are needed.

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Redundancy analysis (RDA) of nifH subcluster presence absence in Central Arctic samples and environmental variables. Environmental variables: temperature, salinity, nitrate, phosphate and silicate were standardized by z-scoring prior to RDA. The red circles represent the different samples and the intensity of the color indicates if there is one (light red) or many (dark red) samples at that coordinate in the plot. Sample names in red correspond to those in Supplementary Table S1. The black labels correspond to the different subclusters of nifH (Cluster number 1, 2, 3, or 4; and the subcluster letter A-K). The explanatory variables constrained ∼57% of the variance in the nifH subclusters across samples. The significance of this type I scaling was 0.001 and the residuals were mostly distributed around zero (Supplementary Figure S3).
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Figure 4: Redundancy analysis (RDA) of nifH subcluster presence absence in Central Arctic samples and environmental variables. Environmental variables: temperature, salinity, nitrate, phosphate and silicate were standardized by z-scoring prior to RDA. The red circles represent the different samples and the intensity of the color indicates if there is one (light red) or many (dark red) samples at that coordinate in the plot. Sample names in red correspond to those in Supplementary Table S1. The black labels correspond to the different subclusters of nifH (Cluster number 1, 2, 3, or 4; and the subcluster letter A-K). The explanatory variables constrained ∼57% of the variance in the nifH subclusters across samples. The significance of this type I scaling was 0.001 and the residuals were mostly distributed around zero (Supplementary Figure S3).

Mentions: Our RDA suggests that our current set of explanatory variables are only able to account for just over half (∼57%) of the variation in our nifH subcluster data (Figure 4). Salinity and silicate increasing concentrations showed strong positive covariation, while phosphate concentrations showed a negative covariation with the other variables (Figure 4). Nitrate concentrations and temperature showed strong negative covariation. In general, nifH genes are found across a wide range of temperature and nutrient values, but with changing community structure. For example, Laptev Sea samples, containing sequences from subclusters 1A (Deltaproteobacteria) and 2A (Firmicutes and Bacteroidetes), were more associated with increased temperatures and decreased nitrate concentrations relative to the other samples analyzed (Figure 4). The presence of cyanobacterial nifH genes at the upper layer of the ice at station 224 (labeled as 224IT in Figure 4), is associated with the high phosphate concentrations.


Diazotroph Diversity in the Sea Ice, Melt Ponds, and Surface Waters of the Eurasian Basin of the Central Arctic Ocean
Redundancy analysis (RDA) of nifH subcluster presence absence in Central Arctic samples and environmental variables. Environmental variables: temperature, salinity, nitrate, phosphate and silicate were standardized by z-scoring prior to RDA. The red circles represent the different samples and the intensity of the color indicates if there is one (light red) or many (dark red) samples at that coordinate in the plot. Sample names in red correspond to those in Supplementary Table S1. The black labels correspond to the different subclusters of nifH (Cluster number 1, 2, 3, or 4; and the subcluster letter A-K). The explanatory variables constrained ∼57% of the variance in the nifH subclusters across samples. The significance of this type I scaling was 0.001 and the residuals were mostly distributed around zero (Supplementary Figure S3).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5120112&req=5

Figure 4: Redundancy analysis (RDA) of nifH subcluster presence absence in Central Arctic samples and environmental variables. Environmental variables: temperature, salinity, nitrate, phosphate and silicate were standardized by z-scoring prior to RDA. The red circles represent the different samples and the intensity of the color indicates if there is one (light red) or many (dark red) samples at that coordinate in the plot. Sample names in red correspond to those in Supplementary Table S1. The black labels correspond to the different subclusters of nifH (Cluster number 1, 2, 3, or 4; and the subcluster letter A-K). The explanatory variables constrained ∼57% of the variance in the nifH subclusters across samples. The significance of this type I scaling was 0.001 and the residuals were mostly distributed around zero (Supplementary Figure S3).
Mentions: Our RDA suggests that our current set of explanatory variables are only able to account for just over half (∼57%) of the variation in our nifH subcluster data (Figure 4). Salinity and silicate increasing concentrations showed strong positive covariation, while phosphate concentrations showed a negative covariation with the other variables (Figure 4). Nitrate concentrations and temperature showed strong negative covariation. In general, nifH genes are found across a wide range of temperature and nutrient values, but with changing community structure. For example, Laptev Sea samples, containing sequences from subclusters 1A (Deltaproteobacteria) and 2A (Firmicutes and Bacteroidetes), were more associated with increased temperatures and decreased nitrate concentrations relative to the other samples analyzed (Figure 4). The presence of cyanobacterial nifH genes at the upper layer of the ice at station 224 (labeled as 224IT in Figure 4), is associated with the high phosphate concentrations.

View Article: PubMed Central - PubMed

ABSTRACT

The Eurasian basin of the Central Arctic Ocean is nitrogen limited, but little is known about the presence and role of nitrogen-fixing bacteria. Recent studies have indicated the occurrence of diazotrophs in Arctic coastal waters potentially of riverine origin. Here, we investigated the presence of diazotrophs in ice and surface waters of the Central Arctic Ocean in the summer of 2012. We identified diverse communities of putative diazotrophs through targeted analysis of the nifH gene, which encodes the iron protein of the nitrogenase enzyme. We amplified 529 nifH sequences from 26 samples of Arctic melt ponds, sea ice and surface waters. These sequences resolved into 43 clusters at 92% amino acid sequence identity, most of which were non-cyanobacterial phylotypes from sea ice and water samples. One cyanobacterial phylotype related to Nodularia sp. was retrieved from sea ice, suggesting that this important functional group is rare in the Central Arctic Ocean. The diazotrophic community in sea-ice environments appear distinct from other cold-adapted diazotrophic communities, such as those present in the coastal Canadian Arctic, the Arctic tundra and glacial Antarctic lakes. Molecular fingerprinting of nifH and the intergenic spacer region of the rRNA operon revealed differences between the communities from river-influenced Laptev Sea waters and those from ice-related environments pointing toward a marine origin for sea-ice diazotrophs. Our results provide the first record of diazotrophs in the Central Arctic and suggest that microbial nitrogen fixation may occur north of 77°N. To assess the significance of nitrogen fixation for the nitrogen budget of the Arctic Ocean and to identify the active nitrogen fixers, further biogeochemical and molecular biological studies are needed.

No MeSH data available.


Related in: MedlinePlus