Nitrification rates in Arctic soils are associated with functionally distinct populations of ammonia-oxidizing archaea

Abstract

The functioning of Arctic soil ecosystems is crucially important for global climate, and basic knowledge regarding their biogeochemical processes is lacking. Nitrogen (N) is the major limiting nutrient in these environments, and its availability is strongly dependent on nitrification. However, microbial communities driving this process remain largely uncharacterized in Arctic soils, namely those catalyzing the rate-limiting step of ammonia (NH 3 ) oxidation. Eleven Arctic soils were analyzed through a polyphasic approach, integrating determination of gross nitrification rates, qualitative and quantitative marker gene analyses of ammonia-oxidizing archaea (AOA) and bacteria (AOB) and enrichment of AOA in laboratory cultures. AOA were the only NH 3 oxidizers detected in five out of 11 soils and outnumbered AOB in four of the remaining six soils. The AOA identified showed great phylogenetic diversity and a multifactorial association with the soil properties, reflecting an overall distribution associated with tundra type and with several physico-chemical parameters combined. Remarkably, the different gross nitrification rates between soils were associated with five distinct AOA clades, representing the great majority of known AOA diversity in soils, which suggests differences in their nitrifying potential. This was supported by selective enrichment of two of these clades in cultures with different NH 3 oxidation rates. In addition, the enrichments provided the first direct evidence for NH 3 oxidation by an AOA from an uncharacterized Thaumarchaeota-AOA lineage. Our results indicate that AOA are functionally heterogeneous and that the selection of distinct AOA populations by the environment can be a determinant for nitrification activity and N availability in soils.

Characteristics of ammonia oxidation potentials and ammonia oxidizers in mineral soil under Salix polaris–moss vegetation in Ny-Ålesund, Svalbard

“…At the study site, vascular plants, mostly consisting of S. polaris, covered about 20 % of the ground (Muraoka et al 2008), and the typical vegetation type was S. polaris-moss. The vegetation at our study site was similar to that at the study site of moss tundra on a dry mound in Longyearbyen, Svalbard, in the work of Alves et al (2013), though the locations were different.…”

“…The sequencing reads were grouped into 13 OTUs at an OTU cutoff of 0.07. The clusters and clades of AOA-amoA genes defined by Pester et al (2012) and Alves et al (2013) were used for the phylogenetic analysis. All OTUs were classified into the Nitrososphaera cluster and were distributed into clades A, B, and Nitrososphaera (Fig.…”

“…To our knowledge, the study by Alves et al (2013) is the only one ever to have elucidated the nitrification properties of Svalbard's high-Arctic soils. Alves et al (2013) measured both gross and net rates of in situ and potential nitrification at 15°C by using an 15 N dilution technique on eight types of tundra soils in Svalbard (mineral soils of shrub tundra, tussock tundra, moss tundra on a wet ridge, moss tundra on a dry mound, and in two plots of frost-boil tundra; organic soils in two plots of tundra fen peat). Potential gross nitrification rates of the mineral soils with the addition of 1.7-2.5 mM ammonium as substrate ranged from about 10-200 ng N g -1 ds h -1 .…”

“…Potential net nitrification rates ranged from about -70 to 35 ng N g -1 ds h -1 , the negative value indicating that nitrate consumption exceeded production. According to Alves et al (2013), the nitrification rates of soils in Svalbard were directly dependent on functionally distinct populations of AOA, rather than on abiotic factors. They also revealed that clade A of AOA was dominant in many cases (in the mineral soils of tussock tundra and moss tundra on the dry mound, and in two plots of frost-boil tundra); these sequences within clade A were low-temperature adapted and had low, or no, nitrification potential.…”

Significance of archaeal nitrification in hypoxic waters of the Baltic Sea

“…These studies often revealed the dominance of archaeal over bacterial ammonia oxidizers (Francis et al, 2005;Wuchter et al, 2006;Mincer et al, 2007;Agogué et al, 2008;Newell et al, 2013). Further support for the strong role for AOA in nitrification comes from observations of the co-occurrence of archaeal amoA in areas of nitrification activity (Caffrey et al, 2007;Beman et al, 2008;Alves et al, 2013) and from metatranscriptomic studies (Baker et al, 2012;Lesniewski et al, 2012). However, to determine the actual contribution and impact of AOA on the nitrogen cycle requires measurements of ammonium oxidation rates, as they cannot be deduced from transcript abundance alone (Mu mann et al, 2011), given that quantification is influenced by, for example, mRNA degradation during sampling (Feike et al, 2012) and, in addition, may not inevitably reflect environmental activity.…”