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The contribution of nirK gene-containing thaumarchaea to denitrification and N2O production across coastal sediment and terrestrial ecosystems

  • Soils, Sec 5 • Soil and Landscape Ecology • Research Article
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Abstract

Purpose

Ammonia-oxidizing archaea (AOA) are ubiquitous in aquatic and terrestrial environments, and the copper-containing nitrite reductase (NirK) plays a pivotal role in AOA metabolism. However, distribution and function of nirK gene-containing thaumarchaea (AnirK) have rarely been estimated, especially in terrestrial ecosystems.

Methods

Soil and sediment samples were taken from 20 sites including coastal mud flat, freshwater wetland, paddy soil, agricultural upland, and forest soil. Potential N2O production rates, community composition, and transcriptional activity of nirK gene-containing thaumarchaea in different habitats were investigated by combining field surveys with microcosm incubations.

Results

AnirK gene abundance and N2O production rates were significantly higher in flooded habitats like freshwater wetland and paddy soil than in agricultural upland and forest soils. In comparison to the AOA amoA gene, AnirK gene was less diverse and mainly affiliated within Candidatus Nitrosoarchaeum, Nitrosopumilus, and Candidatus Nitrosotenuis (Group I.1a) and Candidatus Nitrosotalea (Group I.1a-associated). Microcosm incubations further demonstrated that AnirK gene transcription activity was significantly higher than bacterial nirK and nirS genes, corresponding to the high nitrate reduction and N2O emissions in wetland and paddy soil. Nitrosopumilus in coastal sediment and Candidatus Nitrosoarchaeum in paddy soil and wetland were identified as the active AnirK gene carriers.

Conclusion

Our study demonstrated that the AnirK gene was widely present in coastal sediment and terrestrial ecosystem like wetland and paddy soils, and that AnirK gene-containing Nitrosopumilus and Candidatus Nitrosoarchaeum are potential active contributors to nitrite reduction and N2O production in these ecosystems.

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Acknowledgements

We would like to thank Anhui Ge, Yabo Zhang, Yaqi Wang, and Wei Shi for assistance in soil sampling, and Ren Bai for helps in laboratory analysis.

Funding

This study was financially supported by the National Natural Science Foundation of China (41771288).

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Correspondence to Li-Mei Zhang.

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11368_2022_3219_MOESM1_ESM.pdf

Supplementary file1 (PDF 1823 kb). Fig. S1 Location of sampling sites. Different colors represent different ecosystem types including coastal mud flat, freshwater wetland, paddy soil, agricultural upland, and forest soil. The sites indicated by stars are chosen for microcosm incubation.

11368_2022_3219_MOESM2_ESM.pdf

Supplementary file2 (PDF 444 kb). Fig. S2 The abundances of archaeal nirK gene estimated with the primer pair 58F/579R for AnirK and the primer pair qAnirK1F/qAnirK1R for qAnirK in each site. “N.” means below the detection limit. The asterisks above the bars indicate a significant difference (P < 0.05) between AnirK and qAnirK gene abundances. Vertical bars indicate standard errors of three replicates within each site.

11368_2022_3219_MOESM3_ESM.pdf

Supplementary file3 (PDF 234 kb). Fig. S3 Regression relationship between the NO3-N reduction amount and rates of N2O production. Different colors refer to the different sites, and different shapes refer to different incubation time points.

Supplementary file4 (DOCX 30 kb)

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Han, B., Liu, SY., Han, LL. et al. The contribution of nirK gene-containing thaumarchaea to denitrification and N2O production across coastal sediment and terrestrial ecosystems. J Soils Sediments 22, 2246–2261 (2022). https://doi.org/10.1007/s11368-022-03219-7

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