Abstract
Aims
Wetland plants affect ammonia-oxidation rate (AOR) and nitrogen-fixation rate (NFR), resulting in changes in plant-available nitrogen and wetland nitrogen-cycling. This study aims to investigate the underlying mechanisms and influencing factors associated with ammonium oxidation and nitrogen fixation in response to wetland-emergent aquatic plants.
Methods
A field experiment was conducted to study the response of activity, abundance, and community structure of ammonia-oxidizers and diazotrophs to three wetland-emergent aquatic plants in summer and autumn. The root exudates and soil physicochemical properties were determined due to their important role in rhizosphere interactions.
Results
AOR and NFR were significantly higher in rhizosphere than in bulk soils. The increases of AOR and NFR in rhizosphere were significantly positively affected by oxidation-reduction potential, additionally, NFR was also significantly affected by sugar-containing root exudates. Furthermore, NFR strongly correlated with diazotroph abundance, whereas AOR was linearly correlated with ammonia-oxidizing archaea (AOA) activity and mostly determined by a specific AOA taxon.
Conclusions
Emergent plant rhizosphere exhibited strong positive effects on AOR and NFR by altering community structure and abundance of related microorganisms. Release of available oxygen and carbon in plant rhizospheres is vital for promoting ammonium oxidation and nitrogen fixation and might further mediate wetlands nitrogen-cycling.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- ANOVA:
-
analysis of variance
- AOA:
-
ammonia-oxidizing archaea
- AOB:
-
ammonia-oxidizing bacteria
- AOR:
-
ammonia-oxidation rate
- Cyp:
-
Cyperus alternifolius
- DM:
-
dry mas
- DOC:
-
dissolved organic carbon
- HPLC:
-
high-performance liquid chromatography
- NFR:
-
nitrogen-fixation rate
- ORP:
-
oxidation-reduction potential
- PCR:
-
polymerase chain reaction
- Phr:
-
Phragmites australis
- qPCR:
-
quantitative real-time polymerase chain reaction
- TN:
-
total nitrogen
- TOC:
-
total organic carbon
- Typ:
-
Typha angustifolia
- ZRCW:
-
Zhaoniu River Constructed Wetland
References
Armstrong J, Armstrong W (2001) Rice and Phragmites: effects of organic acids on growth, root permeability, and radial oxygen loss to the rhizosphere. Am J Bot 88:1359–1370. https://doi.org/10.2307/3558443
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266. https://doi.org/10.1146/annurev.arplant.57.032905.105159
Bardgett RD, Bowman WD, Kaufmann R, Schmidt SK (2005) A temporal approach to linking aboveground and belowground ecology. Trends Ecol Evol 20:634–641. https://doi.org/10.1016/j.tree.2005.08.005
Barraquio WL, Watanabe I (1981) Occurrence of aerobic nitrogen fixing bacteria in wetland and dryland plants. J Soil Sci Plant Nutr 27:121–125. https://doi.org/10.1080/00380768.1981.10431262
Bastviken SK, Eriksson PG, Martins I, Neto JM, Leonardson L, Tonderski K (2003) Potential nitrification and denitrification on different surfaces in a constructed treatment wetland. J Environ Qual 32:2414. https://doi.org/10.2134/jeq2003.2414
Briones AM, Okabe S, Umemiya Y, Ramsing N, Reichardt W, Okuyama H (2003) Ammonia-oxidizing bacteria on root biofilms and their possible contribution to N use efficiency of different rice cultivars. Plant Soil 250:335–348. https://doi.org/10.1023/A:1022897621223
Burgmann H, Meier S, Bunge M, Widmer F, Zeyer J (2005) Effects of model root exudates on structure and activity of a soil diazotroph community. Environ Microbiol 7:1711–1724. https://doi.org/10.1111/j.1462-2920.2005.00818.x
Caffrey JM, Bano N, Kalanetra K, Hollibaugh JT (2007) Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia. ISME J 1:660–662. https://doi.org/10.1038/ismej.2007.79
Capone D (1988) Benthic nitrogen fixation. In: Blackburn TH, Sorensen J (eds) Nitrogen cycling in coastal marine environments. Wiley, New York
Cocking EC (2003) Endophytic colonization of plant roots by nitrogen-fixing bacteria. Plant Soil 252:169–175. https://doi.org/10.1023/A:1024106605806
Dakora FD, Drake BG (2000) Elevated CO2 stimulates associative N2 fixation in a C3 plant of the Chesapeake Bay wetland. Plant Cell Environ 23:943–953. https://doi.org/10.1046/j.1365-3040.2000.00610.x
Di HJ, Cameron K, Shen J, Winefield C, O'Callaghan M, Bowatte S, He J (2009) Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci 2:621–624. https://doi.org/10.1038/ngeo613
Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. P Natl Acad Sci USA 112:E911–E920. https://doi.org/10.1073/pnas.1414592112
Falkowski P, Fenchel T, Delong EF (2008) Microbial genomes that drive Earth's biogeochemical cycles. Science 320:1034–1039. https://doi.org/10.1007/978-1-4614-6418-1_800-3
Fdz-polanco F, Mendez E, Urueña MA, Villaverde S, García PA (2000) Spatial distribution of heterotrophs and nitrifiers in a submerged biofilter for nitrification. Water Res 34:4081–4089. https://doi.org/10.1016/S0043-1354(00)00159-7
Fontaine S, Barot S (2005) Size and functional diversity of microbe populations control plant persistence and long-term soil carbon accumulation. Ecol Lett 8:1075–1087. https://doi.org/10.1111/j.1461-0248.2005.00813.x
García J, Ojeda E, Sales E, Chico F, Píriz T, Aguirre P, Mujeriego R (2003) Spatial variations of temperature, redox potential and contaminants in horizontal flow reed beds. Ecol Eng 21:129–142. https://doi.org/10.1016/j.ecoleng.2003.10.001
Gersberg R, Elkins B, Goldman C (1986) Role of aquatic plants in wastewater treatment by artificial wetlands. Water Res 20:363–368. https://doi.org/10.1016/0043-1354(86)90085-0
Giguere AT, Taylor AE, Myrold DD, Bottomley PJ (2015) Nitrification responses of soil ammonia-oxidizing archaea and bacteria to ammonium concentrations. Soil Sci Soc Am J 79:1366. https://doi.org/10.2136/sssaj2015.03.0107
Grayston SJ, Wang S, Campbell CD, Edwards AC (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem 30:369–378. https://doi.org/10.1016/S0038-0717(97)00124-7
Gremion F, Chatzinotas A, Harms H (2003) Comparative 16S rDNA and 16S rRNA sequence analysis indicates that Actinobacteria might be a dominant part of the metabolically active bacteria in heavy metal-contaminated bulk and rhizosphere soil. Environ Microbiol 5:896–907. https://doi.org/10.1046/j.1462-2920.2003.00484.x
Griffiths BRK, Ebblewhite N, Dobson G (1998) Soil microbial community structure: effect of substrate loading rates. Soil Biol Biochem 31:145–153. https://doi.org/10.1016/s0038-0717(98)00117-5
Gruber N, Galloway JN (2008) An earth-system perspective of the global nitrogen cycle. Nature 451:293–296. https://doi.org/10.1038/nature06592
Gubry-Rangin CX, Cile HB, Quince C, Engel M, Thomson BC, James P, Schloter M, Griffiths RI, Prosser JI, Nicol GW (2011) Niche specialization of terrestrial archaeal ammonia oxidizers. P Natl Acad Sci USA 108:21206–21211. https://doi.org/10.2307/23077211
Halm H, Lam P, Ferdelman T, Lavik G, Dittmar T, Laroche J, D'Hondt S, Kuypers MM (2011) Heterotrophic organisms dominate nitrogen fixation in the South Pacific Gyre. ISME J 6:1238–1249. https://doi.org/10.1038/ismej.2011.182
He J, Shen J, Zhang L, Zhu Y, Zheng Y, Xu M, Di H (2007) Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ Microbiol 9:2364–2374. https://doi.org/10.1111/j.1462-2920.2007.01358.x
He Y, Hu W, Ma D, Lan H, Yang Y, Gao Y (2017) Abundance and diversity of ammonia-oxidizing archaea and bacteria in the rhizosphere soil of three plants in the Ebinur Lake wetland. Can J Microbiol 63:2016–2492. https://doi.org/10.1139/cjm-2016-0492
Herrmann M, Scheibe A, Avrahami S, Küsel K (2011) Ammonium availability affects the ratio of ammonia-oxidizing bacteria to ammonia-oxidizing archaea in simulated creek ecosystems. Appl Environ Microbiol 77:1896–1899. https://doi.org/10.1128/AEM.02879-10
Hsu SF, Buckley DH (2009) Evidence for the functional signifcance of diazotroph community structure in soil. ISME J 3:124–136. https://doi.org/10.1038/ismej.2008.82
Huang J, Xu X, Wang M, Nie M, Qiu S, Wang Q, Quan Z, Xiao M, Li B (2016) Responses of soil nitrogen fixation to Spartina alterniflora invasion and nitrogen addition in a Chinese salt marsh. Sci Rep-UK 6. https://doi.org/10.1038/srep20384
Jia Z, Conrad R (2010) Bacteriarather than Archaeadominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11:1658–1671. https://doi.org/10.1111/j.1462-2920.2009.01891.x
Jiang H, Dong H, Yu B, Lv G, Deng SC, Berzins N, Dai M (2009) Diversity and abundance of ammonia-oxidizing archaea and bacteria in Qinghai lake, northwestern China. Geomicrobiology 26:199–211. https://doi.org/10.1080/01490450902744004
Kirchman DL, Elifantz H, Dittel AI, Malmstrom RR, Cottrell MT (2007) Standing stocks and activity of archaea and bacteria in the western arctic ocean. Limnol Oceanogr 52:495–507. https://doi.org/10.4319/lo.2007.52.2.0495
Kirk G, Kronzucker H (2005) The potential for nitrification and nitrate uptake in the rhizosphere of wetland plants: a modelling study. Ann Bot-London 96:639–646. https://doi.org/10.1093/aob/mci216
Kowalchuk G, Stephen J (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol 55:485–529. https://doi.org/10.1146/annurev.micro.55.1.485
Levičnik Höfferle Š, Nicol G, Pal L, Hacin J, Prosser JI, Mandic-Mulec I (2010) Ammonium supply rate influences archaeal and bacterial ammonia oxidizers in a wetland soil vertical profile. FEMS Microbiol Ecol 74:302–315. https://doi.org/10.1111/j.1574-6941.2010.00961.x
Li H, Weng B, Huang F, Su JQ, Yang X (2015) pH regulates ammonia-oxidizing bacteria and archaea in paddy soils in southern China. Appl Microbiol Biotechnol 99:6113–6123. https://doi.org/10.1007/s00253-015-6488-2
Li B, Yang Y, Chen J, Wu Z, Liu Y, Xie S (2018) Nitrifying activity and ammonia-oxidizing microorganisms in a constructed wetland treating polluted surface water. Sci Total Environ 628-629:310–318. https://doi.org/10.1016/j.scitotenv.2018.02.041
Li Y, Pan F, Yao H (2019) Response of symbiotic and asymbiotic nitrogen-fixing microorganisms to nitrogen fertilizer application. J Siol Sediment 19:1948–1958. https://doi.org/10.1007/s11368-018-2192-z
Liu G, Jiang N, Zhang L, Liu Z (1996) Soil physical and chemical analysis and description of soil profiles, vol. 24. China Standard Methods Press, Beijing, p 266
Liu S, Shen L, Lou L, Tian G, Zheng P, Hu B (2013) Spatial distribution and factors shaping the niche segregation of ammonia-oxidizing microorganisms in the qiantang river, China. Appl Environ Microbiol 79:4065–4071. https://doi.org/10.1128/AEM.00543-13
Liu Y, Chen L, Zhang N, Li Z, Zhang G, Xu Y, Shen Q, Zhang R (2016) Plant-microbe communication enhances auxin biosynthesis by a root-associated bacterium bacillus amyloliquefaciens sqr9. Mol Plant Microbe In 29:324–330. https://doi.org/10.1094/MPMI-10-15-0239-R
Liu Z, Xie H, Hu Z, Zhang J, Zhang J, Sun H, Lan W (2017) Role of ammonia-oxidizing archaea in ammonia removal of wetland under low-temperature condition. Water Air Soil Pollut 228:356. https://doi.org/10.1007/s11270-017-3519-x
Lu Y, Rosencrantz D, Liesack W, Conrad R (2006) Structure and activity of bacterial community inhabiting rice roots and the rhizosphere. Environ Microbiol 8:1351–1360. https://doi.org/10.1111/j.1462-2920.2006.01028.x
Marschner P, Yang CH, Lieberei R, Crowley D (2001) Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biol Biochem 33:1437–1445
Moseman-Valtierra SM, Armaiz-Nolla K, Levin LA (2010) Wetland response to sedimentation and nitrogen loading: diversification and inhibition of nitrogen-fixing microbes. Ecol Appl 20:1556–1568. https://doi.org/10.2307/25741326
Qin W, Amin SA, Martens-Habbena W, Walker CB, Urakawa H, Devol AH, Stahl DA (2014) Marine ammonia-oxidizing archaeal isolates display obligate mixotrophy and wide ecotypic variation. P Natl Acad Sci USA 111:12504–12509. https://doi.org/10.1073/pnas.1324115111
Ramakrishna C, Sethunathan N (1982) Stimulation of autotrophic ammonium oxidation in rice rhizosphere soil by the insecticide carbofuran. Appl Environ Microbiol 44:1–4. https://doi.org/10.1007/BF00448446
Rengel Z (2002) Genetic control of root exudation. Plant Soil 245:59–70. https://doi.org/10.1023/A:1020692715291
Rösch C, Bothe H (2010) Diversity of total, nitrogen-fixing and denitrifying bacteria in an acid forest soil. Eur J Soil Sci 60:883–894. https://doi.org/10.1111/j.1365-2389.2009.01167.x
Rosenblueth M, Martinez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant-Microbe Interact 19:827–837. https://doi.org/10.1094/MPMI-19-0827
Ruiz-Rueda O, Hallin S, Baneras L (2009) Structure and function of denitrifying and nitrifying bacterial communities in relation to the plant species in a constructed wetland. FEMS Microbiol Ecol 67:308–319. https://doi.org/10.1111/j.1574-6941.2008.00615.x
Šantrůčková H, Rejmánková E, Pivničková B, Snyder JM (2010) Nutrient enrichment in tropical wetlands: shifts from autotrophic to heterotrophic nitrogen fixation. Biogeochemistry 101:295–310. https://doi.org/10.1007/s10533-010-9479-5
Seitzinger SP (1988) Denitrification in freshwater and coastal marine ecosystems: ecological and geochemical significance. Limnol Oceanogr 33:702–724. https://doi.org/10.4319/lo.1988.33.4part2.0702
Simons M, Permentier H, de Weger LA, Wijffelman CA, Lugtenberg BJJ (1997) Amino acid synthesis is necessary for tomato root colonization by pseudomonas fluorescens strain wcs365. Mol Plant Microbe In 10:102–106. https://doi.org/10.1094/mpmi.1997.10.1.102
Taylor AE, Vajrala N, Giguere AT, Gitelman AI, Arp DJ, Myrold DD, Bottomley PJ (2013) Use of aliphatic n-alkynes to discriminate soil nitrification activities of ammonia-oxidizing thaumarchaea and bacteria. Appl Environ Microbiol 79:6544–6551. https://doi.org/10.1128/AEM.01928-13
Tourna M, Stieglmeier M, Spang A, Konneke M, Schintlmeister A, Urich T, Engel M, Schloter M, Wagner M, Richter A, Schleper C (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. P Natl Acad Sci USA 108:8420–8425. https://doi.org/10.1073/pnas.1013488108
Trias R, Ruiz-Rueda O, García-Lledó A, Vilar-Sanz A, López-Flores R, Quintana XD, Hallin S, Bañeras L (2012) Emergent macrophytes act selectively on ammonia-oxidizing bacteria and archaea. Appl Environ Microbiol 78:6352–6356. https://doi.org/10.1128/AEM.00919-12
Verhamme DT, Prosser JI, Nicol GW (2011) Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J 5:1067–1071. https://doi.org/10.1038/ismej.2010.191
Vranova V, Rejsek K, Skene KR, Janous D, Formanek P (2013) Methods of collection of plant root exudates in relation to plant metabolism and purpose: a review. J Soil Sci Plant Nutr 176:175–199. https://doi.org/10.1002/jpln.201000360
Wardle DA (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633. https://doi.org/10.1126/science.1094875
Weier KL, Pittaway PA, Wildin JH (1995) Role of N2-fixation in the sustainability of the ponded grass pasture system. Soil Biol Biochem 27:441–445. https://doi.org/10.1016/0038-0717(95)98616-v
Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511. https://doi.org/10.1093/jxb/52.suppl_1.487
Winship L, Tjepkema J (1985) Nitrogen fixation and respiration by root nodules of Alnus rubra Bong.: effects of temperature and oxygen concentration. Plant Soil 87:91–107. https://doi.org/10.1007/BF02277651
Wu H, Wang X, He X, Zhang S, Liang R, Shen J (2017) Effects of root exudates on denitrifier gene abundance, community structure and activity in a micro-polluted constructed wetland. Sci Total Environ 598:697–703. https://doi.org/10.1016/j.scitotenv.2017.04.150
Yang B, Wang X, Ma H, Yang T, Jia Y, Zhou J, Dai C (2015) Fungal endophyte Phomopsis liquidambari affects nitrogen transformation processes and related microorganisms in the rice rhizosphere. Front Microbiol 6:982. https://doi.org/10.3389/fmicb.2015.00982
Yang Y, Ren Y, Wang X, Hu Y, Wang Z, Zeng Z (2018) Ammonia-oxidizing archaea and bacteria responding differently to fertilizer type and irrigation frequency as revealed by Illumina Miseq sequencing. J Soils Sediments 18:1029–1040. https://doi.org/10.1007/s11368-017-1792-3
Zehr JP, Jenkins BD, Short SM, Steward GF (2003) Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microbiol 5:539–554. https://doi.org/10.1046/j.1462-2920.2003.00451.x
Zhai X, Piwpuan N, Arias CA, Headley T, Brix H (2013) Can root exudates from emergent wetland plants fuel denitrification in subsurface flow constructed wetland systems? Ecol Eng 61:555–563. https://doi.org/10.1016/j.ecoleng.2013.02.014
Zhang J, Liu B, Zhou X, Chu J, Li Y, Wang M (2015) Effects of emergent aquatic plants on abundance and community structure of ammonia-oxidising microorganisms. Ecol Eng 81:504–513. https://doi.org/10.1016/j.ecoleng.2015.04.029
Zhao D, Luo J, Zeng J, Wang M, Yan W, Huang R, Wu QL (2013) Effects of submerged macrophytes on the abundance and community composition of ammonia-oxidizing prokaryotes in a eutrophic lake. Environ Sci Pollut R 21:389–398. https://doi.org/10.1007/s11356-013-1909-1
Acknowledgments
We thank Professor Yupeng Geng in Yunnan University and three anonymous referees for their valuable comments and suggestions on the manuscript. This study was supported by the “China Major Science and Technology Program for Water Pollution Control and Treatment” (No.2017ZX07101003), the “Natural Science Foundation of Shandong Province, China” (No. ZR2017MC013) and the “National Natural Science Foundation of China” (No. 41601333). We would like to thank Editage for English language editing.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Hans Lambers.
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
Fang, J., Zhao, R., Cao, Q. et al. Effects of emergent aquatic plants on nitrogen transformation processes and related microorganisms in a constructed wetland in northern China. Plant Soil 443, 473–492 (2019). https://doi.org/10.1007/s11104-019-04249-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-019-04249-w