Abstract
Nitrogen removal in constructed wetlands (CWs) may be inhibited by salinity. The clarification of the response of microbial community to salt stress is a premise for developing strategies to improve nitrogen removal efficiency in CWs under saline conditions. Results showed that the ammonia nitrogen (NH4+-N), nitrate nitrogen (NO3−-N), and total nitrogen (TN) removal percentages significantly (p < 0.05) decreased in CWs with increasing salinity. The structure and abundance of the microbial community varied with different salinity levels and sampling depths in CWs. Compared with a non-saline condition, the abundances of some bacteria with a denitrification function (e.g., Arthrobacter) significantly (p < 0.05) decreased in CWs under saline conditions (i.e., EC of 15 and 30 mS/cm). Aerobic bacteria (e.g., Sphingomonas) exhibited more abundance in soil and upper gravel samples in CWs than those in bottom gravel samples, while the abundance of some denitrifying bacteria (e.g., Thauera and Azoarcus) was significantly (p < 0.05) higher in bottom gravel samples compared with soil and upper gravel samples, respectively. This study provides both microbiological evidence for explaining the impact of salt stress on nitrogen removal in CWs and scientific reference for developing enhanced strategies to improve the nitrogen removal capacity of CWs.
Similar content being viewed by others
Data availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Ansola G, Arroyo P, Saenz de Miera LE (2014) Characterisation of the soil bacterial community structure and composition of natural and constructed wetlands. Sci Total Environ 473:63–71
Blossfeld S, Gansert D, Thiele B, Kuhn AJ, Löschd R (2011) The dynamics of oxygen concentration, pH value, and organic acids in the rhizosphere of Juncus spp. Soil Biol Biochem 43(6):1186–1197
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336
Chen M, Wang W, Feng Y, Zhu X, Zhou H, Tan Z, Li X (2014) Impact resistance of different factors on ammonia removal by heterotrophic nitrification-aerobic denitrification bacterium Aeromonas sp HN-02. Bioresour Technol 167:456–461
Chen X, Zhu H, Yan B, Shutes B, Xing D, Banuelos G, Cheng R, Wang X (2020) Greenhouse gas emissions and wastewater treatment performance by three plant species in subsurface flow constructed wetland mesocosms. Chemosphere 239:124795
Christian Q, Elmar P, Pelin Y, Jan G, Timmy S, Pablo Y, Jörg P, Oliver GF (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41(1):590–596
Coban O, Kuschk P, Kappelmeyer U, Spott O, Martienssen M, Jetten MSM, Knoeller K (2015) Nitrogen transforming community in a horizontal subsurface-flow constructed wetland. Water Res 74:203–212
Dalu T, Wasserman RJ, Magoro ML, Froneman PW, Weyl OL (2019) River nutrient water and sediment measurements inform on nutrient retention, with implications for eutrophication. Sci Total Environ 684:296–302
Du L, Trinh X, Chen Q, Wang C, Wang H, Xia X, Zhou Q, Xu D, Wu Z (2018) Enhancement of microbial nitrogen removal pathway by vegetation in integrated vertical-flow constructed wetlands (IVCWs) for treating reclaimed water. Bioresour Technol 249:644–651
Duan J, Fang H, Su B, Chen J, Lin J (2015) Characterization of a halophilic heterotrophic nitrification-aerobic denitrification bacterium and its application on treatment of saline wastewater. Bioresour Technol 179:421–428
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200
Fu G, Han J, Yu T, Huangshen L, Zhao L (2019a) The structure of denitrifying microbial communities in constructed mangrove wetlands in response to fluctuating salinities. J Environ Manag 238:1–9
Fu G, Zhao L, Huangshen L, Wu J (2019b) Isolation and identification of a salt-tolerant aerobic denitrifying bacterial strain and its application to saline wastewater treatment in constructed wetlands. Bioresour Technol 290:121725
Fu G, Wu J, Han J, Zhao L, Chan G, Leong K (2020) Effects of substrate type on denitrification efficiency and microbial community structure in constructed wetlands. Bioresour Technol 307:123222
He T, Xie D, Ni J, Li Z, Li Z (2020) Characteristics of nitrogen transformation and intracellular nitrite accumulation by the hypothermia bacterium Arthrobacter arilaitensis. Sci Total Environ 701:134730
Ho JC, Michalak AM, Pahlevan N (2019) Widespread global increase in intense lake phytoplankton blooms since the 1980s. Nature 574(7780):667–670
Hong J, Li W, Lin B, Zhan M, Liu C, Chen B-Y (2013) Deciphering the effect of salinity on the performance of submerged membrane bioreactor for aquaculture of bacterial community. Desalination 316:23–30
Ibekwe AM, Grieve CM, Lyon SR (2003) Characterization of microbial communities and composition in constructed dairy wetland wastewater effluent. Appl Environ Microb 69(9):5060–5069
Iorhemen OT, Hamza RA, Sheng Z, Tay JH (2019) Submerged aerobic granular sludge membrane bioreactor (AGMBR): organics and nutrients (nitrogen and phosphorus) removal. Bioresour Technol Rep 6:260–267
Jeppesen E, Beklioğlu M, Özkan K, Akyürek Z (2020) Salinization increase due to climate change will have substantial negative effects on inland waters and freshwater resources: A call for multifaceted research at the local and global scale. Innovation 1:100030
Jia L, Wang R, Feng L, Zhou X, Lv J, Wu H (2018) Intensified nitrogen removal in intermittently-aerated vertical flow constructed wetlands with agricultural biomass: Effect of influent C/N ratios. Chem Eng J 345:22–30
Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-Index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79(17):5112–5120
Lehl HK, Ong S-A, Ho L-N, Wong Y-S, Saad FNM, Oon Y-L, Oon Y-S, Yong C-Y, Thung W-E (2016) Multiple aerobic and anaerobic baffled constructed wetlands for simultaneous nitrogen and organic compounds removal. Desalin Water Treat 57(60):29160–29167
Lemley DA, Adams JB, Rishworth GM, Bouland C (2019) Phytoplankton responses to adaptive management interventions in eutrophic urban estuaries. Sci Total Environ 693:133601
Levy-Booth DJ, Prescott CE, Grayston SJ (2014) Microbial functional genes involved in nitrogen fixation, nitrification and denitrification in forest ecosystems. Soil Biol Biochem 75:11–25
Li H, Jiapeng Q, Tongtong L, Jiabao L, Qiang L, Xiangzhen L (2016) Pika population density is associated with the composition and diversity of gut microbiota. Front Microbiol 7:758–758
Li X, Li Y, Lv D, Li Y, Wu J (2020) Nitrogen and phosphorus removal performance and bacterial communities in a multi-stage surface flow constructed wetland treating rural domestic sewage. Sci Total Environ 709:136235
Liang YX, Zhu H, Banuelos G, Yan BX, Shutes B, Cheng XW, Chen X (2017a) Removal of nutrients in saline wastewater using constructed wetlands: plant species, influent loads and salinity levels as influencing factors. Chemosphere 187:52–61
Liang YX, Zhu H, Banuelos G, Yan BX, Zhou QW, Yu XF, Cheng XW (2017b) Constructed wetlands for saline wastewater treatment: a review. Ecol Eng 98:275–285
Lind L, Schuler MS, Hintz WD, Stoler AB, Jones DK, Mattes BM, Relyea RA (2018) Salty fertile lakes: how salinization and eutrophication alter the structure of freshwater communities. Ecosphere 9(9):e02383
Mastrorillo L, Mazza R, Manca F, Tuccimei P (2016) Evidences of different salinization sources in the roman coastal aquifer (Central Italy). J Coast Conserv 20(6):423–441
Meng P, Pei H, Hu W, Shao Y, Li Z (2014) How to increase microbial degradation in constructed wetlands: Influencing factors and improvement measures. Bioresour Technol 157:316–326
Miao Y, Liao R, Zhang X-X, Liu B, Li Y, Wu B, Li A (2015) Metagenomic insights into salinity effect on diversity and abundance of denitrifying bacteria and genes in an expanded granular sludge bed reactor treating high-nitrate wastewater. Chem Eng J 277:116–123
Peralta RM, Ahn C, Gillevet PM (2013) Characterization of soil bacterial community structure and physicochemical properties in created and natural wetlands. Sci Total Environ 443:725–732
Shalem Y, Weinstein Y, Levi E, Herut B, Goldman M, Yechieli Y (2015) The extent of aquifer salinization next to an estuarine river: an example from the eastern Mediterranean. Hydrogeol J 23(1):69–79
Shapovalova AA, Khijniak TV, Tourova TP, Muyzer G, Sorokin DY (2008) Heterotrophic denitrification at extremely high salt and pH by haloalkaliphilic Gammaproteobacteria from hypersaline soda lakes. Extremophiles 12(5):619–625
Su JF, Yang S, Huang TL, Li M, Liu JR, Yao YX (2020) Enhancement of the denitrification in low C/N condition and its mechanism by a novel isolated Comamonas sp. YSF15. Environ Pollut 256(Jan.):113294.1–113294.7
Van Den Hende S, Claessens L, De Muylder E, Boon N, Vervaeren H (2014) Microalgal bacterial flocs originating from aquaculture wastewater treatment as diet ingredient for Litopenaeus vannamei (Boone). Aquac Res 47(4):1075–1089
Vymazal J (2007) Removal of nutrients in various types of constructed wetlands. Sci Total Environ 380(1-3):48–65
Vymazal J (2011) Constructed wetlands for wastewater treatment: five decades of experience. Environ Sci Technol 45(1):61–69
Vymazal J (2013) The use of hybrid constructed wetlands for wastewater treatment with special attention to nitrogen removal: a review of a recent development. Water Res 47(14):4795–4811
Wahyudi, Suntoyo, Sholihin (2017) Influence of seawater to the river water quality in Kalibuntung estuary southeastern coast of Surabaya city Indonesia. Appl Mech Mater 862:107–114
Wang Q, Yang L, Wu Z (2010) Treatment efficiency of integrated vertical-flow constructed wetland for saline wastewater. Wuhan Univ J Nat Sci 15:544–548
Wang Q, Cao Z, Liu Q, Zhang J, Hu Y, Zhang J, Xu W, Kong Q, Yuan X, Chen Q (2019a) Enhancement of COD removal in constructed wetlands treating saline wastewater: intertidal wetland sediment as a novel inoculation. J Environ Manag 249:109398–109398
Wang XY, Zhu H, Shutes B, Fu BR, Yan BX, Yu XF, Wen HY, Chen X (2019b) Identification and denitrification characteristics of a salt-tolerant denitrifying bacterium Pannonibacter phragmitetus F1. AMB Express 9(1):193–193
Wang XY, Zhu H, Yan BX, Shutes B, Banuelos G, Wen HY (2020) Bioaugmented constructed wetlands for denitrification of saline wastewater: A boost for both microorganisms and plants. Environ Int 138:5628–5628
Xia Z, Wang Q, She Z, Gao M, Zhao Y, Guo L, Jin C (2019) Nitrogen removal pathway and dynamics of microbial community with the increase of salinity in simultaneous nitrification and denitrification process. Sci Total Environ 697:134047
Yu GL, Peng HY, Fu YJ, Yan XJ, Du CY, Chen H (2019) Enhanced nitrogen removal of low C/N wastewater in constructed wetlands with co-immobilizing solid carbon source and denitrifying bacteria. Bioresour Technol 280:337–344
Yun L, Yu ZH, Li YY, Luo P, Jiang X, Tian YS, Ding XQ (2019) Ammonia nitrogen and nitrite removal by a heterotrophic Sphingomonas sp. strain LPN080 and its potential application in aquaculture. Aquaculture 500:477–484
Zhao G, Mehta SK, Liu Z (2010) Use of saline aquaculture wastewater to irrigate salt-tolerant Jerusalem artichoke and sunflower in semiarid coastal zones of China. Agric Water Manag 97(12):1987–1993
Zhao D, Huang R, Zeng J, Yan W, Wang J, Ma T, Wang M, Wu QL (2012) Diversity analysis of bacterial community compositions in sediments of urban lakes by terminal restriction fragment length polymorphism (T-RFLP). World J Microbiol Biotechnol 28(11):3159–3170
Zhao W, Wang Y, Liu S, Pan M, Yang J, Chen S (2013) Denitrification activities and N2O production under salt stress with varying COD/N ratios and terminal electron acceptors. Chem Eng J 215:252–260
Zhu H, Yan B, Xu Y, Guan J, Liu S (2014) Removal of nitrogen and COD in horizontal subsurface flow constructed wetlands under different influent C/N ratios. Ecol Eng 63:58–63
Zhuang L-L, Yang T, Zhang J, Li X (2019) The configuration, purification effect and mechanism of intensified constructed wetland for wastewater treatment from the aspect of nitrogen removal: A review. Bioresour Technol 293:122086
Zou J, Guo XS, Han YP, Liu JX, Liang HW (2012) Study of a novel vertical flow constructed wetland system with drop aeration for rural wastewater treatment. Water Air Soil Pollut 223(2):889–900
Funding
This work was supported by the Environmental Protection Project of Ecology and Environment Department of Jilin Province (No. 2018-06), the National Key Research and Development Program of China (No. 2016YFC0500404-4) and the Youth Innovation Promotion Association CAS (No. 2017274).
Author information
Authors and Affiliations
Contributions
XW carried out all experiments and drafted the manuscript. HZ (corresponding author) is responsible for this study, participated its design, and helped to draft the manuscript. BY, BS, and GB provided technical and theoretical support. RC executed the experiments, analyzed all data, and produced figures. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no competing interests.
Ethics approval and consent to participate
This article does not contain any studies with animals or human participants performed by any of the authors.
Consent for publication
Not applicable.
Additional information
Responsible Editor: Alexandros Stefanakis
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Wang, X., Zhu, H., Yan, B. et al. Response of the microbial community to salt stress and its stratified effect in constructed wetlands. Environ Sci Pollut Res 28, 18089–18101 (2021). https://doi.org/10.1007/s11356-020-11937-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-11937-z