Abstract
In marine ecosystems, Thaumarchaeota are most likely the major ammonia oxidizers. While ammonia concentrations vary by about two orders of magnitude in the oceanic water column, archaeal ammonia oxidizers (AOA) vary by only one order of magnitude from surface to bathypelagic waters. Thus, the question arises whether the key enzyme responsible for ammonia oxidation, ammonia monooxygenase (amo), exhibits different affinities to ammonia along the oceanic water column and consequently, whether there are different ecotypes of AOA present in the oceanic water column. We determined the abundance and phylogeny of AOA based on their amoA gene. Two ecotypes of AOA exhibited a distribution pattern reflecting the reported availability of ammonia and the physico-chemical conditions throughout the Atlantic, and from epi- to bathypelagic waters. The distinction between these two ecotypes was not only detectable at the nucleotide level. Consistent changes were also detected at the amino acid level. These changes include substitutions of polar to hydrophobic amino acid, and glycine substitutions that could have an effect on the configuration of the amo protein and thus, on its activity. Although we cannot identify the specific effect, the ratio of non-synonymous to synonymous substitutions (dN/dS) between the two ecotypes indicates a strong positive selection between them. Consequently, our results point to a certain degree of environmental selection on these two ecotypes that have led to their niche specialization.
Highlights
Nitrogen is fundamental for all living organisms and is present in the environment in a variety of organic and inorganic forms
Relatively higher abundances of the 16S rRNA gene were found in upper and lower bathypelagic environments at high latitudes (ARCT, North Atlantic Drift province (NADR), and Subantarctic province (SANT) provinces, with average gene abundance ranging from 2.0 − 7.4 × genes mL−1) and at the equator than in the gyre regions (NAG and South Atlantic Gyral (SATL) provinces with average gene abundance of 1.3 − 6.7 × 103 genes mL−1)
The ubiquitous distribution of ammonia oxidizers (AOA) is well documented in marine waters (Francis et al, 2005; Coolen et al, 2007; Herfort et al, 2007), with a few studies spanning over the entire water column to the deep ocean (Mincer et al, 2007; Yakimov et al, 2007; Agogué et al, 2008; De Corte et al, 2009; Beman et al, 2012)
Summary
Nitrogen is fundamental for all living organisms and is present in the environment in a variety of organic and inorganic forms. The out-competition of Bacteria by Archaea in specific environments was proposed to be driven by chronic energy stress (Valentine, 2007), and in particular in the case of archaeal nitrifiers, they were proposed to out-compete Bacteria in conditions of low energy availability such as in the oligotrophic ocean This hypothesis was supported by the finding of a lower half saturation constant (Km) and substrate threshold for AOA (Martens-Habbena et al, 2009; Horak et al, 2013) as compared to AOB (Stark and Firestone, 1996), with important implications for the nitrogen cycle in the ocean (Martens-Habbena et al, 2009), where ammonia concentration is generally lower than the requirements of AOB
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