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Changing roles of ammonia-oxidizing bacteria and archaea in a continuously acidifying soil caused by over-fertilization with nitrogen

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Abstract

Nitrification coupled with nitrate leaching contributes to soil acidification. However, little is known about the effect of soil acidification on nitrification, especially on ammonia oxidation that is the rate-limiting step of nitrification and performed by ammonia-oxidizing bacteria (AOB) and archaea (AOA). Serious soil acidification occurs in Chinese greenhouses due to the overuse of N-fertilizer. In the present study, greenhouse soils with 1, 3, 5, 7, and 9 years of vegetable cultivation showed a consistent pH decline (i.e., 7.0, 6.3, 5.6, 4.9, and 4.3). Across the pH gradient, we analyzed the community structure and abundance of AOB and AOA by pyrosequencing and real-time PCR techniques, respectively. The recovered nitrification potential (RNP) method was used to determine relative contributions of AOA and AOB to nitrification potential. The results revealed that soil acidification shaped the community structures of AOA and AOB. In acidifying soil, soil pH, NH3 concentration, and DOC content were critical factors shaping ammonia oxidizer community structure. AOB abundance, but not AOA, was strongly influenced by soil acidification. When soil pH was below 5.0, AOA rather than AOB were responsible for almost all of the RNP. However, when soil pH ranged from 5.6 to 7.0, AOB were the major contributors to RNP. The group I.1a-associatied AOA had more relative abundance in low pH (pH<6.3), whereas group I.1b tended to prefer neutral pH. Clusters 2, 10, and 12 in AOB were more abundant in acidic soil (pH <5.6), while Nitrosomonas-like lineage and unclassified lineage 3 were prevailing in neutral soil and slightly acidic soil (pH, 6.0–6.5), respectively. These results suggested that soil acidification had a profound impact on ammonia oxidation and more specific lineages in AOB occupying different pH-associated niches required further investigation.

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Acknowledgments

This work was jointly financed by National Natural Science Foundation of China (No. 41301258, 41230856), Anhui Provincial Natural Science Foundation (No. 1408085QC68), Crop subject high teacher term construction in Anhui province and Special Fund for Agro-scientific Research in the Public Interest (No. 201503121–02).

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    Authors and Affiliations

    1. College of Agronomy, Anhui Agricultural University, Hefei, 230036, China

      He Song, Zhao Che, Ting Huang & Zhaorong Dong

    2. College of Resources and Environmental Sciences, China Agricultural University, Beijing, 100193, China

      Wenchao Cao & Jingguo Wang

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    1. He Song
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    2. Zhao Che
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    3. Wenchao Cao
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    Correspondence to Zhaorong Dong.

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    Responsible editor: Zhihong Xu

    He Song and Zhao Che contributed equally to this work.

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    Supplementary Fig. 1

    Rarefaction curves for archaeal (a) and bacterial (b) amoA gene sequences amoA genes in greenhouse soils under different years of vegetable cultivation. -1, -2, -3 for each cropping year represent three replicates. (DOCX 296 kb)

    Supplementary Fig. 2

    Heat map illustrating the relative abundance of AOB amoA gene OTUs (> 2 % relative abundance) in greenhouse soils under different years of vegetable cultivation. (DOCX 37 kb)

    Supplementary Fig. 3

    Numbers of dominant OTUs (> 5 % relative abundance) for bacterial amoA in greenhouse soils under different years of vegetable cultivation; values are means ± SE (n = 3). (DOCX 86 kb)

    Supplementary Fig. 4

    Heat map illustrating the relative abundance of AOA amoA gene OTUs (> 2 % relative abundance) in greenhouse soils under different years of vegetable cultivation. (DOCX 38 kb)

    Supplementary Fig. 5

    Numbers of dominant OTUs (> 5 % relative abundance) for archaeal amoA in greenhouse soils under different years of vegetable cultivation; values are means ± SE (n = 3). (DOCX 76 kb)

    Supplementary Fig. 6

    Canonical correspondence analysis between community structure of AOA (a) or AOB (b) and soil characteristics (DOCX 48 kb)

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    Song, H., Che, Z., Cao, W. et al. Changing roles of ammonia-oxidizing bacteria and archaea in a continuously acidifying soil caused by over-fertilization with nitrogen. Environ Sci Pollut Res 23, 11964–11974 (2016). https://doi.org/10.1007/s11356-016-6396-8

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