Abundance, diversity, and activity of ammonia-oxidizing prokaryotes in the coastal Arctic ocean in summer and winter

Abstract

Ammonia oxidation, the first step in nitrification, is performed by certain Beta- and Gammaproteobacteria and Crenarchaea to generate metabolic energy. Ammonia monooxygenase (amoA) genes from both Bacteria and Crenarchaea have been found in a variety of marine ecosystems, but the relative importance of Bacteria versus Crenarchaea in ammonia oxidation is unresolved, and seasonal comparisons are rare. In this study, we compared the abundance of betaproteobacterial and crenarchaeal amoA genes in the coastal Arctic Ocean during summer and winter over 2 years. Summer and winter betaproteobacterial amoA clone libraries were significantly different, although the gene sequences were similar to those found in temperate and polar environments. Betaproteobacterial and crenarchaeal amoA genes were 30- to 115-fold more abundant during the winter than during the summer in both years of the study. Archaeal amoA genes were more abundant than betaproteobacterial amoA genes in the first year, but betaproteobacterial amoA was more abundant than archaeal amoA the following year. The ratio of archaeal amoA gene copies to marine group I crenarchaeal 16S rRNA genes averaged 2.9 over both seasons and years, suggesting that ammonia oxidation was common in Crenarchaea at this location. Potential nitrification rates, as well as the total amoA gene abundance, were highest in the winter when competition with phytoplankton was minimal and ammonium concentrations were the highest. These results suggest that ammonium concentrations were important in determining the rates of ammonia oxidation and the abundance of ammonia-oxidizing Betaproteobacteria and Crenarchaea.

FIG. 1.

Neighbor-joining phylogenetic tree of betaproteobacterial amoA. The phylogeny is based on nucleotide sequences. Bootstrap values lower than 50% are omitted. GenBank accession numbers are shown for sequences from other studies.

FIG. 2.

Neighbor-joining phylogenetic tree of archaeal amoA. The phylogeny is based on nucleotide sequences. Bootstrap values lower than 50% are omitted. GenBank accession numbers are shown for sequences from other studies.

FIG. 3.

Copies of amoA genes per ng of DNA for betaproteobacteria and archaea. Error bars represent the standard deviations of all triplicate qPCR measurements from each sample location during the season. There were three replicate measurements for each sample location, and the numbers of sample locations were four (summer 2007 and winter 2009), three (winter 2008), and six (summer 2008).

FIG. 4.

Ratio of archaea amoA copies to marine group I copies of the 16S rRNA gene. The 16S rRNA gene data do not include archaea in the pSL12 group.

FIG. 5.

Potential nitrification rate versus amoA gene copies. Estimates of gene copies include both betaproteobacterial and archaeal amoA.