Skip to main content

Advertisement

Log in

Response of the nitrogen processing bacterial community to water level fluctuation and nitrate availability in an intact marsh soil column

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Wetlands are known to experience fluctuations in water levels and receive exogenous nitrogen inputs that affect various organisms, including soil microorganisms. To study the impact of these factors on microbial diversity, we collected intact soil columns from a Phragmites australis-dominated site in the Qixing River National Nature Reserve in Northeast China. In a laboratory experiment, we simulated water level fluctuations and exogenous nitrogen inputs to the soil columns and examined the associated changes in the relative abundance of 51 bacterial genera involved in nitrogen cycling processes. Our findings revealed that different bacterial genera exhibited varying relative abundances across treatments. Specifically, Massilia showed the highest total relative abundance at the genus level, while Planctomyces had the second highest, and Campylobacter had the lowest abundance. The DESeq2 model, based on negative binomial distribution, revealed that the tags of bacterial genera were significantly correlated with soil depth, but not with water levels or nitrogen concentrations. However, the addition of a 30 mg/L nitrate solution caused a decrease in the relative abundances of bacterial genera with decreasing water levels, while a 60 mg/L concentration of nitrogen resulted in a decrease and then an increase in the relative abundances of bacterial genera with decreasing water levels. Our study provides valuable insights into the response of nitrogen-cycling bacteria to changes in different environmental conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

The R codes for the data analysis and raw data are available from the corresponding author upon request.

References

  • BÖttcher J, Strebel O, Voerkelius S al e (1990) Using isotope fractionation of nitrate-nitrogen and nitrate-oxygen for evaluation of microbial denitrification in a sandy aquifer. 112: 0–424

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  Google Scholar 

  • Chen S, Zhou Y, Chen Y, Gu J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Cold Spring Harbor Lab 34:i884–i890

  • Compton JE, Watrud LS, Porteous LA, Degrood S (2004) Response of soil microbial biomass and community composition to chronic nitrogen additions at Harvard forest. Forest Ecol Manag 196:0–158

  • Daims H, Luecker S, Wagner M (2016) A new perspective on microbes formerly known as nitrite-oxidizing bacteria. Trends Microbiol 24:699–712

    Article  CAS  Google Scholar 

  • Du P, Wu X, Xu J, Dong F, Liu X, Zheng Y (2018) Effects of triuralin on the soil microbial community and functional groups involved in nitrogen cycling. J Hazard Mater 353:204–213

    Article  CAS  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

  • Elmar P, Christian Q, Katrin K, Fuchs BM, Wolfgang L, Jrg P et al (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 7188–96

  • Fu G, Han J, Yu T, Huangshen L, Zhao L (2019) The structure of denitrifying microbial communities in constructed mangrove wetlands in response to fluctuating salinities. J Environ Manage 238:1–9

    Article  CAS  Google Scholar 

  • Gaspar H, Ferreira R, Gonzalez JM, da Clara MI, Santana MM (2016) Influence of temperature and copper on oxalobacteraceae in soil enrichments. Curr Microbiol 72:370–376

    Article  CAS  Google Scholar 

  • Hadley Wickham, Romain Fran?ois, Henry L, Müller K. dplyr: a grammar of data manipulation. R package version 1.0.7. https://CRAN.R-project.org/package=dplyr, 2021.

  • Hawinkel S, Rayner J, Bijnens L, Thas O (2020) Sequence count data are poorly fit by the negative binomial distribution. PLoS ONE 15:e0224909

    Article  CAS  Google Scholar 

  • Hayatsu M, Tago K, Saito M (2008) Various players in the nitrogen cycle: diversity and functions of the microorganisms involved in nitrification and denitrification. Soil Sci Plant Nutr 54:33–45

  • He H, Miao Y, Zhang L, Chen Y, Chen W (2020) The structure and diversity of nitrogen functional groups from different cropping systems in Yellow River Delta. Microorganisms 8:424

    Article  CAS  Google Scholar 

  • Ishida CK, Kelly JJ, Gray KA (2006) Effects of variable hydroperiods and water level fluctuations on denitrification capacity, nitrate removal, and benthic-microbial community structure in constructed wetlands. Ecol Eng 28:363–373

    Article  Google Scholar 

  • Jiang Y, Chen J, Wang J, Zeng Q, Zhu D (2021) Linkage of soil organic matter composition and soil bacterial community structure as influenced by dominant plants and hydrological fluctuation in Poyang Lake. J Soils Sediments 21:2865–2881

  • Kaneko T (2002) Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110 (Supplement). DNA Res 9:225–256

    Article  CAS  Google Scholar 

  • Kennison RL, Fong P (2014) Extreme eutrophication in shallow estuaries and lagoons of California is driven by a unique combination of local watershed modifications that trump variability associated with wet and dry seasons. Estuaries & Coasts 37:164–179

  • Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194

    Article  Google Scholar 

  • Kusai NA, Ayob Z (2020) Bacterial diversity in peat soils of forest ecosystems and oil palm plantation. Eurasian Soil Sci 53:485–493

    Article  Google Scholar 

  • Kuypers M, Marchant H, Kartal B (2018) The microbial nitrogen-cycling network. Nature Rev Microbiol 16:263–276. https://doi.org/10.1038/nrmicro.2018.9

  • Lee CG, Fletcher TD, Sun G (2010) Nitrogen removal in constructed wetland systems. Eng Life Sci 9:11–22

    Article  Google Scholar 

  • Li Y, Sun Y, Zhang H, Wang L, Wang C (2019) The responses of bacterial community and N2O emission to nitrogen input in lake sediment: estrogen as a co-pollutant. Environ Res 179:108769

    Article  CAS  Google Scholar 

  • Ling, Wang, Rong, Sheng, Huicui, Yang et al (2017) Stimulatory effect of exogenous nitrate on soil denitrifiers and denitrifying activities in submerged paddy soil. Geoderma 286:64–72

  • Love MI, Wolfgang H, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:1–21

    Article  Google Scholar 

  • Mago T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963

    Article  Google Scholar 

  • Mushinski RM, Payne ZC, Raff JD, Craig ME, Pusede SE, Rusch DB et al (2021) Nitrogen cycling microbiomes are structured by plant mycorrhizal associations with consequences for nitrogen oxide fluxes in forests. Glob Change Biol 27:1068–1082

    Article  CAS  Google Scholar 

  • Mwagona PC, Yao Y, Yuanqi S, Yu H (2021) Effect of water level fluctuation and nitrate concentration on soil-surface CO2 and CH4 emissions from Riparian freshwater marsh wetland. Wetlands 41:109

    Article  Google Scholar 

  • Mwagona PC, Yao Y, Yuanqi S, Yu H, Sihi D (2019) Laboratory study on nitrate removal and nitrous oxide emission in intact soil columns collected from nitrogenous loaded riparian wetland, Northeast China. Plos One 14:e0214456

  • Nico T, Andreas M, Kay K et al (2018) River water infiltration enhances denitrification efficiency in riparian groundwater. Water Res: A Journal of the International Water Association 130:185–199

    Article  Google Scholar 

  • Pishgar R, Dominic JA, Sheng Z, Tay JH (2019) Denitrification performance and microbial versatility in response to different selection pressures. Bioresour Technol 281:72–83

  • Qiao Z, Sun R, Wu Y, Hu S, Chan J (2020) Microbial heterotrophic nitrification-aerobic denitrification dominates simultaneous removal of aniline and ammonium in aquatic ecosystems. Water Air Soil Pollution 231:1–14

  • Rahman M, Grace MR, Roberts KL, Kessler AJ, Cook PLM (2019a) Effect of temperature and drying-rewetting of sediments on the partitioning between denitrification and DNRA in constructed urban stormwater wetlands. Ecological engineering: J Ecotechnol 140:105586

  • Rahman MM, Roberts KL, Grace MR, Kessler AJ, Cook PLM (2019b) Role of organic carbon, nitrate and ferrous iron on the partitioning between denitriflcation and DNRA in constructed stormwater urban wetlands. Sci Total Environ 666:608–617

    Article  CAS  Google Scholar 

  • Reed SC, Townsend AR, Cleveland CC, Nemergut DR (2010) Microbial community shifts influence patterns in tropical forest nitrogen fixation. Oecologia 164:521–531

    Article  Google Scholar 

  • Ren Z, Qu X, Zhang M, Yu Y, Peng W (2019) Distinct bacterial communities in wet and dry seasons during a seasonal water level fluctuation in the largest freshwater lake (Poyang Lake) in ChinaData_Sheet_1.docx. Front Microbiol 10:1167

  • Su Z, Dai T, Tang Y, Tao Y, Huang B, Mu Q et al (2018) Sediment bacterial community structures and their predicted functions implied the impacts from natural processes and anthropogenic activities in coastal area. Mar Pollut Bull 131:481–495

    Article  CAS  Google Scholar 

  • Su X, Xue B, Wang Y, Hashmi MZ, Lin H, Chen J et al (2019) Bacterial community shifts evaluation in the sediments of Puyang River and its nitrogen removal capabilities exploration by resuscitation promoting factor. Ecotoxicol Environ Saf 179:188–197

    Article  CAS  Google Scholar 

  • Sutka RL, Ostrom NE, Ostrom PH, Breznak JA, Gandhi H, Pitt AJ et al (2006) Distinguishing nitrous oxide production from nitrification and denitrification on the basis of isotopomer abundances. Appl Environ Microbiol 72:638–644

    Article  CAS  Google Scholar 

  • Wang J, Wang Y, Bai J, Liu Z, Yan D (2016) High efficiency of inorganic nitrogen removal by integrating biofilm-electrode with constructed wetland: autotrophic denitrifying bacteria analysis. Biores Technol 227:7

    Article  Google Scholar 

  • Wang Q, Garrity G, Tiedje J, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

  • Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York

    Book  Google Scholar 

  • Wickham H (2007) Reshaping data with the reshape Package. J Stat Soft 21(12),1–20. URL http://www.jstatsoft.org/v21/i12/

  • William J, Mitsch (2016) Wetlands and climate change. National wetlands newsletter

  • Xing W, Li J, Li D, Hu J, Deng S, Cui Y et al (2018) Stable-isotope probing reveals the activity and function of autotrophic and heterotrophic denitrifiers in nitrate removal from organic-limited wastewater. Environ Sci Technol 52:7867–7875

    Article  CAS  Google Scholar 

  • Xu M, Zhang Q, Xia C et al (2014) Elevated nitrate enriches microbial functional genes for potential bioremediation of complexly contaminated sediments. Isme J 8:1932–1944

  • Yuan CL, Zhang LM, Wang JT, Teng WK, Hu HW, Shen JP et al (2020) Limited effects of depth (0–80cm) on communities of archaea, bacteria and fungi in paddy soil profiles. EuroJ Soil Sci 71:955–966

  • Zhang H, Sun L, Li Y, Zhang W, Wang L (2021) The bacterial community structure and N-cycling gene abundance in response to dam construction in a riparian zone. Environ Res 194:110717

    Article  CAS  Google Scholar 

  • Zhao H, Zheng W, Zhang S, Gao W, Fan Y (2021) Soil microbial community variation with time and soil depth in Eurasian Steppe (Inner Mongolia, China). Annal Microbiol 71:21

  • Zhou Z, Wang C, Zheng M, Jiang L, Luo Y (2017) Patterns and mechanisms of responses by soil microbial communities to nitrogen addition. Soil Biol Biochem 115:433–441

    Article  CAS  Google Scholar 

  • Zhu L (2021) Enhanced sediment denitrification for nitrogen removal by manipulating water level in the lakeshore zone. Water 13:3323

Download references

Acknowledgements

We appreciate the thoughtful comments of Claudia Knief Professor, whose perspectives improved this paper.

Funding

This paper was supported by National Key R&D Program of China (2022YFF1300903) and the Fundamental Research Funds for the Central Universities [grant number 2572021BE04].

Author information

Authors and Affiliations

Authors

Contributions

Yuanqi Shan: complete experiment, data curation, data analysis, writing—original draft, and visualization. Yi Fu: data analysis and writing—review and editing. Lei Wang: supervising and writing—review and editing. Yunlong Yao: supervising, writing—review and editing, and funding acquisition.

Corresponding author

Correspondence to Yunlong Yao.

Ethics declarations

Ethics approval

Not applicable.

Consent to participate

No human participant is involved in this study.

Consent for publication

All authors have read and agreed to publish the manuscript in this version.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Robert Duran

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 24569 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shan, Y., Fu, Y., Wang, L. et al. Response of the nitrogen processing bacterial community to water level fluctuation and nitrate availability in an intact marsh soil column. Environ Sci Pollut Res 30, 111947–111957 (2023). https://doi.org/10.1007/s11356-023-30020-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-023-30020-x

Keywords

Navigation