Abstract
Purpose
Wetland eutrophication is a global ecological problem. Anaerobic oxidation of ammonium (ANAMMOX) and denitrification are the two major pathways of nitrogen removal in wetlands. However, little is known about the associated bacteria that are present around emergent macrophytes and their transcriptional activities. Here, we examine the transcriptional activity of bacteria that perform ANAMMOX and denitrification in the roots and vegetated sediments of three emergent macrophytes and in unvegetated sediment from a eutrophic wetland.
Materials and methods
Roots and vegetated sediments of three emergent macrophytes (Phragmites australis, Typha angustifolia, and Scirpus triqueter) and unvegetated sediment were collected from Wuliangsuhai wetland, China. The community structure and transcriptional activity of ANAMMOX and denitrifying bacteria were examined at the DNA and RNA levels. Additionally, the sediment physicochemical properties were determined.
Results and discussion
ANAMMOX (hzsB) and denitrifying bacteria (nirK, nirS, and nirSII) were detected in all sediments and roots at the DNA level. However, at the RNA level, root-associated ANAMMOX bacteria, including Candidatus Jettenia and Candidatus Brocadia, were detected only in the roots of P. australis. In contrast, nirK-carrying active denitrifiers, such as uncultured bacteria, Sinorhizobium, Rhizobiales, Mesorhizobium, Rhizobium, Devosia, and Bosea (all Rhizobiales), were detected in the roots of T. angustifolia and S. triqueter. The reduction of nitrogen concentration in the sediments of the vegetation zone was probably associated with active ANAMMOX bacteria and denitrifiers.
Conclusion
Active root-associated ANAMMOX bacteria and nirK-type denitrifiers were influenced by plant species, and they likely contribute to nitrogen removal in eutrophic wetlands.
References
Abbas T, Zhang QC, Jin H, Li Y, Liang YC, Di HJ, Zhao YH (2019) Anammox microbial community and activity changes in response to water and dissolved oxygen managements in a paddy-wheat soil of Southern China. Sci Total Environ 672:305–313. https://doi.org/10.1016/j.scitotenv.2019.03.392
Bai R, Xi D, He JZ, Hu HW, Fang YT, Zhang LM (2015) Activity, abundance and community structure of anammox bacteria along depth profiles in three different paddy soils. Soil Biol Biochem 91:212–221. https://doi.org/10.1016/j.soilbio.2015.08.040
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates inrhizosphere interations with plants and other organisms. Annu Rev Plant Biol 57:233–266. https://doi.org/10.1146/annurev.arplant.57.032905.105159
Bao ZH, Okubo T, Kubota K, Kasahara Y, Tsurumaru H, Anda M, Ikeda S, Minamisawa K (2014) Metaproteomic identification of diazotrophic methanotrophs and their localization in root tissues of field-grown rice plants. Appl Environ Microbiol 80:5043–5052. https://doi.org/10.1128/AEM.00969-14
Bhagowati B, Ahamad KU (2018) A review on lake eutrophication dynamics and recent developments in lake modeling. Ecohydrol Hydrobiol 19(1):155–166. https://doi.org/10.1016/j.ecohyd.2018.03.002
Chu JY, Zhang JP, Zhou XH, Liu B, Li LM (2015) A comparison of anammox bacterial abundance and community structures in three different emerged plants-related sediments. Curr Microbiol 71:421–427. https://doi.org/10.1007/s00284-015-0851-5
Compant S, Cambon MC, Vacher C, Mitter B, Sessitsch A (2020) The plant endosphere world–bacterial life within plants. Environ Microbiol. https://doi.org/10.1111/1462-2920.15240
Cui J, Zhao J, Wang Z, Cao WW, Zhang SH, Liu JM, Bao ZH (2020) Diversity of active root-associated methanotrophs of three emergent plants in a eutrophic wetland in northern China. AMB Express 10:48. https://doi.org/10.1186/s13568-020-00984-x
Duan XN, Wang XK, Mu YJ, Ouyang ZY (2005) Seasonal and diurnal variations in methane emissions from Wuliangsu Lake in arid regions of China. Atmos Environ 39:4479–4487. https://doi.org/10.1016/j.atmosenv.2005.03.045
Fu LL, Chen YY, Li SQ, He H, Mi TZ, Zhen Y, Yu ZG (2019) Shifts in the anammox bacterial community structure and abundance in sediments from the Changjiang Estuary and its adjacent area. Syst Appl Microbiol 42(3):383–396. https://doi.org/10.1016/j.syapm.2018.12.008
Humbert S, Tarnawski S, Fromin N, Mallet MP, Aragno M, Zopfi J (2010) Molecular detection of anammox bacteria in terrestrial ecosystems: distribution and diversity. ISME J 4:450–454. https://doi.org/10.1038/ismej.2009.125
Humbert S, Zopfi J, Tarnawski SE (2012) Abundance of anammox bacteria in different wetland soils. Environ Microbiol Rep 4(5):484–490. https://doi.org/10.1111/j.1758-2229.2012.00347.x
Ji XM, Wu ZY, Sung S, Lee P (2019) Metagenomics and metatranscriptomics analyses reveal oxygen detoxification and mixotrophic potentials of an enriched anammox culture in a continuous stirred-tank reactor. Water Res 166:115039. https://doi.org/10.1016/j.watres.2019.115039
Kraiem K, Kallali H, Wahab MA, Fra-vazquez A, Mosquera-Corral A, Jedidi N (2019) Comparative study on pilots between ANAMMOX favored conditions in a partially saturated vertical flow constructed wetland and a hybrid system for rural wastewater treatment. Sci Total Environ 670:644–653. https://doi.org/10.1016/j.scitotenv.2019.03.220
Liu JM, Bao ZH, Cao WW, Han JJ, Zhao J, Kang ZZ, Wang LX, Zhao J (2020) Enrichment of type I methanotrophs with nirs genes of three emergent macrophytes in a eutrophic wetland in China. Microbes Environ 35:n/a. https://doi.org/10.1264/jsme2.me19098
Mitter EK, de Freitas JR, Germida JJ (2017) Bacterial root microbiome of plants growing in oil sands reclamation covers. Front Microbiol 8(849):1–15. https://doi.org/10.3389/fmicb.2017.00849
Mulder A, vandeGraaf AA, Robertson LA, Kuenen JG (1995) Anaerobic ammonium oxidation discovered in a denitrifying fluidized-bed reactor. FEMS Microbiol Ecol 16:177–184. https://doi.org/10.1016/0168-6496(94)00081-7
Paranychianakis NV, Tsiknia M, Kalogerakis N (2016) Pathways regulating the removal of nitrogen in planted and unplanted subsurface flow constructed wetlands. Water Res 102:321–329. https://doi.org/10.1016/j.watres.2016.06.048
Ruiz B, Le Scornet A, Sauviac L, Remy A, Bruand C, Meilhoc E (2019) The nitrate assimilatory pathway in Sinorhizobium meliloti: contribution to NO production. Front Microbiol 10:1526. https://doi.org/10.3389/fmicb.2019.01526
Ruiz-Rueda O, Hallin S, Bañeras L (2009) Structure and function of denitrifying and nitrifying bacterial communities in relation to the plant species in a constructed wetland[J]. FEMS Microbiol Ecol 67(2):308–319. https://doi.org/10.1111/j.1574-6941.2008.00615.x
Sharma S, Aneja MK, Mayer J, Munch JC, Schloter M (2005) Diversity of transcripts of nitrite reductase genes (nirK and nirS) in rhizospheres of grain legumes. Appl Environ Microbiol 71:2001–2007. https://doi.org/10.1128/AEM.71.4.2001-2007.2005
Tan E, Hsu TC, Huang XF, Lin HJ, Kao SJ (2017) Nitrogen transformations and removal efficiency enhancement of a constructed wetland in subtropical Taiwan. Sci Total Environ 601-602:1378–1388. https://doi.org/10.1016/j.scitotenv.2017.05.282
Throback IN, Enwall K, Jarvis A, Hallin S (2004) Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE. FEMS Microbiol Ecol 49:401–417. https://doi.org/10.1016/j.femsec.2004.04.011
Vymazal J (2013) Emergent plants used in free water surface constructed wetlands: a review. Ecol Eng 61:582–592. https://doi.org/10.1016/j.ecoleng.2013.06.023
Wang SY, Pi YX, Jiang YY, Pan HW, Wang XX, Wang XM, Zhou JM, Zhu GB (2020) Nitrate reduction in the reed rhizosphere of a riparian zone: from functional genes to activity and contribution. Environ Res 180:108867. https://doi.org/10.1016/j.envres.2019.108867
Wei W, Isobe K, Nishizawa T, Zhu L, Shiratori Y, Ohte N, Koba K, Otsuka S, Senoo K (2015) Higher diversity and abundance of denitrifying microorganisms in environments than considered previously. ISME J 9:1954–1965. https://doi.org/10.1038/ismej.2015.9
Yin XJ, Lu J, Wang YC, Liu GL, Hua YM, Wan XQ, Zhao JW, Zhu DW (2020) The abundance of nirS-type denitrifiers and anammox bacteria in rhizospheres was affected by the organic acids secreted from roots of submerged macrophytes. Chemosphere 240:124903. https://doi.org/10.1016/j.chemosphere.2019.124903
Zhu GB, Wang SY, Wang Y, Wang CX, Risgaard-Petersen N, Jetten MSM, Yin CQ (2011a) Anaerobic ammonia oxidation in a fertilized paddy soil. ISME J 5:1905–1912. https://doi.org/10.1038/ismej.2011.63
Zhu GB, Wang SY, Feng XJ, Fan GN, Jetten MSM, Yin CQ (2011b) Anammox bacterial abundance, biodiversity and activity in a constructed wetland. Environ Sci Technol 45:9951–9958. https://doi.org/10.1021/es202183w
Zhu GB, Wang SY, Wang C, Zhou LG, Zhao SY, Li YX, Li FB, Jetten MSM, Lu YL, Schwark L (2019) Resuscitation of anammox bacteria after >10,000 years of dormancy. ISME J 13:1098–1109. https://doi.org/10.1038/s41396-018-0316-5
Funding
This study was funded by the Science and Technology Major Project on Lakes of Inner Mongolia grant (ZDZX2018054), National Natural Science Foundation of China grants (41563009, 41963008), and Natural Science Foundation of Inner Mongolia (2019MS04005).
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Shaohua Zhang: Conceptualization, Investigation, Formal analysis, Writing - original draft, Writing - review & editing. Jing Cui: Investigation, Methodology, Writing - review& editing. Meng Zhang: Investigation, Writing - review& editing. Jumei Liu: Investigation, Writing - review& editing. Lixin Wang: Investigation, Writing - review& editing. Ji Zhao: Conceptualization, Investigation, Writing - review& editing. Zhihua Bao: Conceptualization, Investigation, Formal analysis, Writing - original draft, Writing - review & editing.
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Zhang, S., Cui, J., Zhang, M. et al. Diversity of active anaerobic ammonium oxidation (ANAMMOX) and nirK-type denitrifying bacteria in macrophyte roots in a eutrophic wetland. J Soils Sediments 21, 2465–2473 (2021). https://doi.org/10.1007/s11368-021-02926-x
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DOI: https://doi.org/10.1007/s11368-021-02926-x