Archaeal amoA gene diversity points to distinct biogeography of ammonia‐oxidizing Crenarchaeota in the ocean

Abstract

Mesophilic ammonia-oxidizing Archaea (AOA) are abundant in a diverse range of marine environments, including the deep ocean, as revealed by the quantification of the archaeal amoA gene encoding the alpha-subunit of the ammonia monooxygenase. Using two different amoA primer sets, two distinct ecotypes of marine Crenarchaeota Group I (MCGI) were detected in the waters of the tropical Atlantic and the coastal Arctic. The HAC-AOA ecotype (high ammonia concentration AOA) was ≍ 8000 times and 15 times more abundant in the coastal Arctic and the top 300 m layer of the open equatorial Atlantic, respectively, than the LAC-AOA (low ammonia concentration AOA) ecotype. In contrast, the LAC-AOA ecotype dominated the lower meso- and bathypelagic waters of the tropical Atlantic (≍ 50 times more abundant than the HAC-AOA) where ammonia concentrations are well below the detection limit using conventional spectrophotometric or fluorometric methods. Cluster analysis of the sequences from the clone libraries obtained by the two amoA primer sets revealed two phylogenetically distinct clusters. Taken together, our results suggest the presence of two ecotypes of archaeal ammonia oxidizers corresponding to the medium (1.24 µM on average in the coastal Arctic) and low ammonia concentration (< 0.01 µM) in the shallow and the deep waters respectively.

Hadal biosphere: Insight into the microbial ecosystem in the deepest ocean on Earth

“…2), and the genomes of the MGI thaumarchaeotes in the publically accessible database are known to encode only one copy of the amoA and SSU rRNA genes. Thus, most of the MGI thaumarchaeotes distributed in the water column would harbor amoA, as suggested by Sintes et al (28). These results also suggest the coordination between the thaumarchaeal SSU rRNA and amoA gene clusters: group α in the SSU rRNA gene and D in amoA, β and A, γ and Ba, and δ and Ba, respectively.…”

“…S4B and S5). The niche separation of ammonia-oxidizing archaea (AOA) above the abyssal waters that suggested by the amoA gene clone analysis resembles the previously observed pattern that showed the distinctive distribution of the "high ammonia cluster" (HAC) and "low ammonia cluster" (LAC) of archaeal amoA along the water column (28) (Fig. S5).…”

“…The composition of nitrifiers could be indexes of carbon and nitrogen cycles in oceanic ecosystem because NH 4 + is provided by nitrogenous organic matter decomposition. In addition, it has been noted that the niche separation of nitrifiers is regulated by the amount of available electron donors such as ammonia and nitrite (28)(29)(30). Thus, the niche separation of nitrifiers could be a signature of NH 4 + flux from organic matter decomposition that cannot be identified from NH 4 + concentration measurements.…”

Differential contributions of archaeal ammonia oxidizer ecotypes to nitrification in coastal surface waters

“…There has been a widespread effort to determine the distribution of AOA in nearly all major oceanic regions (Lam et al, 2007;Beman et al, 2008;Church et al, 2010;Santoro et al, 2010;Christman et al, 2011;Alonso-Sáez et al, 2012;Baker et al, 2012;Sintes et al, 2013). Substantial evidence now exists that AOA have a primary role in determining the distribution and magnitude of nitrification in the sea (Mincer et al, 2007;Beman et al, 2008;Church et al, 2010;Hollibaugh et al, 2010;Newell et al, 2011;Santoro et al, 2013).…”

“…Here, we sought to elucidate the biogeochemical roles of AOA ecotypes by examining the linkages between patterns of archaeal amoA gene abundance and expression from the two dominant ecotypes of marine Thaumarchaeota and measured rates of nitrification in a coastal upwelling ecosystem. In contrast to the deep (for example, mesopelagic) ocean, these surface waters experience dramatic physicochemical changes over short spatiotemporal scales that setup natural gradients in factors hypothesized to regulate the distributions and activity of dominant AOA ecotypes, including light, ammonia concentrations and phytoplankton abundance and activity (Horrigan et al, 1981;Olson, 1981b;Ward 1985;Kudela et al, 1997;Dugdale et al, 2006;Merbt et al, 2011;Sintes et al, 2013). Our approach has the distinct advantage of allowing the acquisition of both expressional and biogeochemical activity data from a wide array of water column samples with common origins, undergoing an evolution of community structure and activity.…”