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Abstract

Nitrous acid (HONO) is a precursor of the hydroxyl radical (OH), a key oxidant in the degradation of most air pollutants. Field measurements indicate a large unknown source of HONO during the day time. Release of nitrous acid (HONO) from soil has been suggested as a major source of atmospheric HONO. We hypothesize that nitrite produced by biological nitrate reduction in oxygen-limited microzones in wet soils is a source of such HONO. Indeed, we found that various contrasting soil samples emitted HONO at high water-holding capacity (75–140%), demonstrating this to be a widespread phenomenon. Supplemental nitrate stimulated HONO emissions, whereas ethanol (70% v/v) treatment to minimize microbial activities reduced HONO emissions by 80%, suggesting that nitrate-dependent biotic processes are the sources of HONO. High-throughput Illumina sequencing of 16S rRNA as well as functional gene transcripts associated with nitrate and nitrite reduction indicated that HONO emissions from soil samples were associated with nitrate reduction activities of diverse Proteobacteria. Incubation of pure cultures of bacterial nitrate reducers and gene-expression analyses, as well as the analyses of mutant strains deficient in nitrite reductases, showed positive correlations of HONO emissions with the capability of microbes to reduce nitrate to nitrite. Thus, we suggest biological nitrate reduction in oxygen-limited microzones as a hitherto unknown source of atmospheric HONO, affecting biogeochemical nitrogen cycling, atmospheric chemistry, and global modeling.

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Data availability

The sequence data reported in this paper have been deposited in the Genome Sequence Archive of the Beijing Institute of Genomics, Chinese Academy of Sciences (http://bigd.big.ac.cn/gsub/) with accession number CRA000459. All data needed to evaluate the conclusions are present in the paper and/or the Supplementary Information. Additional data related to this paper may be requested from the authors.

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Acknowledgements

We thank J. Cui and M. Badawy for helping to collect the soil samples. We also thank G. Braker and L.R. Bakken for providing pure bacteria cultures. We are grateful to J. Kesselmeier, F.X. Meixner, and H.L. Drake for allowing us to complete experiments in their laboratories. We are also grateful to M. Welling, D. Plake, U. Parchatka, A. Moravek, A. Dallinger, S. Hetz, M. Morawe, N. Roßbach, R. Mertel, and A. Wieczorek for supporting techniques in our experiments. This work was supported by the Max Planck Society and the Chinese Academy of Sciences. D. Wu was sponsored by the National Natural Science Foundation of China (41807449), Shanghai Pujiang Program (18PJ1403500), and “the Fundamental Research Funds for the Central Universities”. M. Liu was supported by the National Natural Science Foundation of China (41761144062). B. Weber would like to thank Paul Crutzen for awarding her a Nobel Laureate Fellowship (2013–2015).

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Author notes

  1. These authors contributed equally: Dianming Wu, Marcus A. Horn

Affiliations

  1. Key Laboratory of Geographic Information Sciences, Ministry of Education, School of Geographic Sciences, East China Normal University, Shanghai, 200241, China

    • Dianming Wu
    •  & Min Liu
  2. Biogeochemistry Department, Max Planck Institute for Chemistry, P.O. Box 3060, Mainz, 55020, Germany

    • Dianming Wu
    • , Thomas Behrendt
    • , Michael Ermel
    • , Robert Oswald
    • , Meinrat O. Andreae
    • , Ivonne Trebs
    •  & Matthias Sörgel
  3. Key Laboratory of Agricultural Water Research, Center for Agricultural Resources Research, Institute of Genetic and Developmental Biology, Chinese Academy of Sciences, Shijiazhuang, 050021, China

    • Dianming Wu
    •  & Chunsheng Hu
  4. Department of Ecological Microbiology, University of Bayreuth and BayCEER, Bayreuth, 95440, Germany

    • Marcus A. Horn
  5. Institute of Microbiology, Leibniz University of Hannover, Hannover, 30419, Germany

    • Marcus A. Horn
  6. Institute for Atmospheric Physics, Johannes Gutenberg University Mainz, Mainz, 55128, Germany

    • Stefan Müller
    •  & Peter Hoor
  7. Key Laboratory of Opto-Electronic Information Acquisition and Manipulation of Ministry of Education, Anhui University, Hefei, 230601, China

    • Jingsong Li
  8. School of Biosciences and Institute of Microbiology and Infection, University of Birmingham, Birmingham, B15 2TT, UK

    • Jeff A. Cole
  9. Key Laboratory of Coastal Environmental Processes and Ecological Remediation, Yantai Institute of Coastal Zone Research (YIC), Chinese Academy of Sciences (CAS), Shandong Provincial Key Laboratory of Coastal Environmental Processes, YICCAS, Yantai, 264003, China

    • Baohua Xie
  10. College of Resources and Environmental Sciences, China Agricultural University, Beijing, 100193, China

    • Xiaotang Ju
  11. Multiphase Chemistry Department, Max Planck Institute for Chemistry, P.O. Box 3060, Mainz, 55020, Germany

    • Guo Li
    • , Janine Fröhlich-Nowoisky
    • , Ulrich Pöschl
    • , Yafang Cheng
    • , Hang Su
    •  & Bettina Weber
  12. Luxembourg Institute of Science and Technology, Environmental Research and Innovation (ERIN) Department, Belvaux, 4422, Luxembourg

    • Ivonne Trebs
  13. Department of Geology and Geophysics, King Saud University, P.O. Box 2455, Riyadh, 11451, Saudi Arabia

    • Meinrat O. Andreae
  14. Atmospheric Chemistry Department, Max Planck Institute for Chemistry, P.O. Box 3060, Mainz, 55020, Germany

    • Matthias Sörgel

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Contributions

This study was co-initiated by D.W., I.T., T.B., Y.C., and H.S. The development of the experimental design and investigations were guided by M.A.H., M.S., B.W., and U.P. The measurements were performed by D.W., M.A.H., S.M., and J.L. The mutants were constructed by J.A.C. The soil samples and the corresponding nutrient data were supported by T.B., B.X., and X.J. Equilibrium model calculations were accomplished by D.W., M.S., U.P., Y.C., H.S., and G.L. The paper was written by D.W. and M.A.H. with the major input from M.S., J.A.C., U.P., and B.W., and further input from all the other authors.

Conflict of interest

The authors declare that they have no conflict of interest.

Corresponding authors

Correspondence to Dianming Wu or Marcus A. Horn or Bettina Weber or Matthias Sörgel.

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https://doi.org/10.1038/s41396-019-0379-y