Advertisement

Exotic Spartina alterniflora invasion alters soil nitrous oxide emission dynamics in a coastal wetland of China

  • Dengzhou Gao
  • Lijun HouEmail author
  • Xiaofei Li
  • Min LiuEmail author
  • Yanling Zheng
  • Guoyu Yin
  • Yi Yang
  • Cheng Liu
  • Ping Han
Regular Article
  • 90 Downloads

Abstract

Aims

Exotic Spartina alterniflora invasion resulting from anthropogenic activities significantly affects microbial nitrogen (N) transformation and associated nitrous oxide (N2O) emission in coastal wetland soils. However, the responses of soil N2O emission dynamics to plant invasion remain unclear. This study assesses the effects of S. alterniflora invasion on soil N2O potential production and consumption processes.

Methods

We used natural isotope tracing technique to investigate potential N2O production and consumption rates in S. alterniflora invaded and native saltmarsh zones (Phragmites australis, Scirpus mariqueter and bare mudflat) in the Yangtze Estuary.

Results

Soil potential net N2O production rates in summer were lower in S. alterniflora stands than in S. mariqueter and bare mudflat stands, but no significant differences among these saltmarsh habitats occurred during winter. Potential gross N2O production and consumption rates were higher in S. alterniflora and P. australis stands compared to S. mariqueter and bare mudflat stands. The gross consumption proportion in S. alterniflora and P. australis stands was higher, which affected net N2O production. Hydroxylamine (NH2OH) oxidation and nitrifier denitrification contributed 4.52–12.62% and 13.87–21.58% of soil N2O source, respectively, but denitrification was the dominant pathway (69.83–80.09%). S. alterniflora invasion increased the contributions of NH2OH oxidation and nitrifier denitrification to N2O source slightly, but decreased the contribution of denitrification to N2O source. Soil potential N2O production and consumption processes were influenced by water-filled pore space, pH, sulfide, and carbon and N substrates.

Conclusion

Exotic S. alterniflora invasion affected soil N2O dynamics by increasing substrates and altering microenvironments, thus mediating N2O emission from coastal saltmarsh soils.

Keywords

Nitrous oxide Dynamics Saltmarsh wetland Spartina alterniflora Yangtze estuary 

Notes

Acknowledgments

This work was funded by the Natural Science Foundation of China (Nos. 41671463, 41725002, 41761144062, 41730646, and 41601530). It was also supported by Chinese National Key Programs for Fundamental Research and Development (Nos. 2016YFA0600904, and 2016YFE0133700), Fundamental Research Funds for the Central Universities, and the Yangtze Delta Estuarine Wetland Station (ECNU). We thank Wayne S. Gardner, anonymous reviewers and editor for constructive comments and valuable suggestions on this manuscript.

Supplementary material

11104_2019_4179_MOESM1_ESM.docx (649 kb)
ESM 1 (DOCX 648 kb)

References

  1. Allen DE, Dalal RC, Rennenberg H, Meyer RL, Reeves S, Schmidt S (2007) Spatial and temporal variation of nitrous oxide and methane flux between subtropical mangrove sediments and the atmosphere. Soil Biol Biochem 39:622–631CrossRefGoogle Scholar
  2. Baral BR, Kuyper TW, Van Groenigen JW (2014) Liebig’s law of the minimum applied to a greenhouse gas: alleviation of P-limitation reduces soil N2O emission. Plant Soil 374:539–548CrossRefGoogle Scholar
  3. Bowden WB (1986) Nitrification, nitrate reduction, and nitrogen immobilization in a tidal freshwater marsh sediment. Ecology 67:88–99CrossRefGoogle Scholar
  4. Bu N, Qu JF, Li ZL, Li G, Zhao H, Zhao B, Chen JK, Fang CM (2015) Effects of Spartina alterniflora invasion on soil respiration in the Yangtze River estuary, China. PLoS One 10:e0121571CrossRefGoogle Scholar
  5. Butterbach-Bahl K, Baggs EM, Dannenmann M, Kiese R, Zechmeister-Boltenstern S (2013) Nitrous oxide emissions from soils: how well do we understand the processes and their controls? Philos T R Soc B 368:20130122CrossRefGoogle Scholar
  6. Burgin AJ, Hamilton SK (2008) NO3 -driven SO4 2− production in freshwater ecosystems: implications for N and S cycling. Ecosystems 11:908–922CrossRefGoogle Scholar
  7. Canfield DE, Glazer AN, Falkowski PG (2010) The evolution and future of Earth’s nitrogen cycle. Science 330:192–196CrossRefGoogle Scholar
  8. Cheng XL, Peng RH, Chen JQ, Luo YQ, Zhang QF, An SQ, Chen JK, Li B (2007) CH4 and N2O emissions from Spartina alterniflora and Phragmites australis in experimental mesocosms. Chemosphere 68:420–427CrossRefGoogle Scholar
  9. Chmura GL, Kellman L, Guntenspergen GR (2011) The greenhouse gas flux and potential global warming feedbacks of a northern macrotidal and microtidal salt marsh. Environ Res Lett 6:044016CrossRefGoogle Scholar
  10. Cline JD (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14:454–458CrossRefGoogle Scholar
  11. Cohen Y, Gordon LI (1978) Nitrous oxide in the oxygen minimum of the eastern tropical North Pacific: evidence for its consumption during denitrification and possible mechanisms for its production. Deep-Sea Res 25:509–524CrossRefGoogle Scholar
  12. Deng F, Hou L, Liu M, Zheng Y, Yin G, Li X, Jiang X (2015) Dissimilatory nitrate reduction processes and associated contribution to nitrogen removal in sediments of the Yangtze estuary. J Geophys Res Biogeosci 120:1521–1531CrossRefGoogle Scholar
  13. Deppe M, Well R, Giesemann A, Spott O, Flessa H (2017) Soil N2O fluxes and related processes in laboratory incubations simulating ammonium fertilizer depots. Soil Biol Biochem 104:68–80CrossRefGoogle Scholar
  14. Dollhopf SL, Hyun JH, Smith AC, Adams HJ, O'Brien S, Kostka JE (2005) Quantification of ammonia-oxidizing bacteria and factors controlling nitrification in salt marsh sediments. Appl Environ Microbiol 71:240–246CrossRefGoogle Scholar
  15. Dong LF, Nedwell DB, Underwood GJ, Thornton DC, Rusmana I (2002) Nitrous oxide formation in the Colne estuary, England: the central role of nitrite. Appl Environ Micro 68:1240–1249CrossRefGoogle Scholar
  16. Firestone MK, Davidson EA (1989) Microbiological basis of NO and N2O production and consumption in soil. Exchange of trace gases between terrestrial ecosystems and the atmosphere: report of the Dahlem workshop on exchange of trace gases between terrestrial ecosystems and the atmosphere, Berlin 1989, February 19–24. Wiley, pp 7–21Google Scholar
  17. Gao D, Li X, Lin X, Wu D, Jin B, Huang Y, Liu M, Chen X (2017) Soil dissimilatory nitrate reduction processes in the Spartina alterniflora invasion chronosequences of a coastal wetland of southeastern China: dynamics and environmental implications. Plant Soil 421:383–399CrossRefGoogle Scholar
  18. Gao GF, Li PF, Zhong JX, Shen ZJ, Chen J, Li YT, Isabwe A, Zhu XY, Ding QS, Zhang S, Gao CH, Zheng HL (2019) Spartina alterniflora invasion alters soil bacterial communities and enhances soil N2O emissions by stimulating soil denitrification in mangrove wetland. Sci Total Environ 653:231–240CrossRefGoogle Scholar
  19. Hines ME (1994) Acetate concentrations and oxidation in salt-marsh sediments. Limnol Oceanogr 39:140–148CrossRefGoogle Scholar
  20. Holtan-Hartwig L, Dörsch P, Bakken LR (2002) Low temperature control of soil denitrifying communities: kinetics of N2O production and reduction. Soil Biol Biochem 34:1797–1806CrossRefGoogle Scholar
  21. Hou L, Zheng Y, Liu M, Gong J, Zhang XL, Yin GY, You L (2013) Anaerobic ammonium oxidation (anammox) bacterial diversity, abundance, and activity in marsh sediments of the Yangtze estuary. J Geophys Res Biogeosci 118:1237–1246CrossRefGoogle Scholar
  22. Ishii S, Song Y, Rathnayake L, Tumendelger A, Satoh H, Toyoda S, Okabe S (2014) Identification of key nitrous oxide production pathways in aerobic partial nitrifying granules. Environ Microbiol 16:3168–3180CrossRefGoogle Scholar
  23. Jia D, Qi F, Xu X, Feng J, Wu H, Guo J, Lin G (2016) Co-regulations of Spartina alterniflora invasion and exogenous nitrogen loading on soil N2O efflux in subtropical mangrove mesocosms. PLoS One 11:e0146199CrossRefGoogle Scholar
  24. Jørgensen CJ, Struwe S, Elberling B (2012) Temporal trends in N2O flux dynamics in a Danish wetland–effects of plant-mediated gas transport of N2O and O2 following changes in water level and soil mineral-N availability. Glob Chang Biol 18:210–222CrossRefGoogle Scholar
  25. Kaspar HF (1982) Nitrite reduction to nitrous oxide by propionibacteria: detoxication mechanism. Arch Microbiol 133:126–130CrossRefGoogle Scholar
  26. Koba K, Osaka K, Tobari Y, Toyoda S, Ohte N, Katsuyama M, Suzuki N, Itoh M, Yamagishi H, Kawasaki M, Kim SJ, Yoshida N, Nakajima T (2009) Biogeochemistry of nitrous oxide in groundwater in a forested ecosystem elucidated by nitrous oxide isotopomer measurements. Geochim Cosmochim Ac 73:3115–3133CrossRefGoogle Scholar
  27. Kraft B, Tegetmeyer HE, Sharma R, Klotz MG, Ferdelman TG, Hettich RL, Strous M (2014) The environmental controls that govern the end product of bacterial nitrate respiration. Science 345:676–679CrossRefGoogle Scholar
  28. Li B, Liao CH, Zhang XD, Chen HL, Wang Q, Chen ZY, Cheng XL (2009) Spartina alterniflora invasions in the Yangtze River estuary, China: an overview of current status and ecosystem effects. Ecol Eng 35:511–520CrossRefGoogle Scholar
  29. Liao CZ, Luo YQ, Fang CM, Chen JK, Li B (2008) Litter pool sizes, decomposition, and nitrogen dynamics in Spartina alterniflora-invaded and native coastal marshlands of the Yangtze estuary. Oecologia 156:589–600CrossRefGoogle Scholar
  30. Lovley DR, Phillips EJ (1987) Rapid assay for microbially reducible ferric iron in aquatic sediments. Appl Environ Microb 53:1536–1540Google Scholar
  31. Lu J, Zhang Y (2013) Spatial distribution of an invasive plant Spartina alterniflora and its potential as biofuels in China. Ecol Eng 52:175–181CrossRefGoogle Scholar
  32. Lu R (2000) Methods of soil and agro-chemical analysis. China Agric Sci Tech Press, BeijingGoogle Scholar
  33. Metcalfe DB, Fisher RA, Wardle DA (2011) Plant communities as drivers of soil respiration: pathways, mechanisms, and significance for global change. Biogeosciences 8:2047–2061CrossRefGoogle Scholar
  34. Murray R, Erler D, Rosentreter J, Maher D, Eyre B (2018) A seasonal source and sink of nitrous oxide in mangroves: insights from concentration, isotope, and isotopomer measurements. Geochim Cosmochim Ac 238:169–192CrossRefGoogle Scholar
  35. Moseman-Valtierra S, Gonzalez R, Kroeger KD, Tang J, Chao WC, Crusius J, Shelton J (2011) Short-term nitrogen additions can shift a coastal wetland from a sink to a source of N2O. Atmos Environ 45:4390–4397CrossRefGoogle Scholar
  36. Onley JR, Ahsan S, Sanford RA, Löffler FE (2018) Denitrification by Anaeromyxobacter dehalogenans, a common soil bacterium lacking the nitrite reductase genes nirS and nirK. Appl Environ Microb 84:e01985–e01917Google Scholar
  37. Ostrom NE, Pitt A, Sutka R, Ostrom PH, Grandy AS, Huizinga KM, Robertson GP (2007) Isotopologue effects during N2O reduction in soils and in pure cultures of denitrifiers. J Geophys Res Biogeosci 112:G02005CrossRefGoogle Scholar
  38. Peng RH, Fang CM, Li B, Chen JK (2011) Spartina alterniflora invasion increases soil inorganic nitrogen pools through interactions with tidal subsidies in the Yangtze estuary, China. Oecologia 165:797–807CrossRefGoogle Scholar
  39. Ravishankara AR, Daniel JS, Portmann RW (2009) Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326:123–125CrossRefGoogle Scholar
  40. Robertson GP (1987) Nitrous oxide sources in aerobic soils: nitrification, denitrification and other biological processes. Soil Biol Biochem 19:187–193CrossRefGoogle Scholar
  41. Sanford RA, Wagner DD, Wu Q, Chee-Sanford JC, Thomas SH, Cruz-García C, Nissen S (2012) Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils. P Natl Acad Sci USA 109:19709–19714CrossRefGoogle Scholar
  42. Seitzinger SP, Kroeze C, Styles RV (2000) Global distribution of N2O emissions from aquatic systems: natural emissions and anthropogenic effects. Chemosphere Global Change Sci 2:267–279CrossRefGoogle Scholar
  43. Seliskar DM, Smart KE, Higashikubo BT, Gallagher JL (2004) Seedling sulfide sensitivity among plant species colonizing Phragmites-infested wetlands. Wetlands 24:426–433CrossRefGoogle Scholar
  44. Shoun H, Tanimoto T (1991) Denitrification by the fungus Fusarium oxysporum and involvement of cytochrome P-450 in the respiratory nitrite reduction. J Biol Chem 266:11078–11082Google Scholar
  45. Sørensen J, Tiedje JM, Firestone RB (1980) Inhibition by sulfide of nitric and nitrous oxide reduction by denitrifying Pseudomonas fluorescens. Appl Environ Microbiol 39:105–108Google Scholar
  46. Stribling JM, Cornwell JC (2001) Nitrogen, phosphorus, and sulfur dynamics in a low salinity marsh system dominated by Spartina alterniflora. Wetlands 21:629–638CrossRefGoogle Scholar
  47. Sun Z, Sun W, Tong C, Zeng C, Yu X, Mou X (2015) China's coastal wetlands: conservation history, implementation efforts, existing issues and strategies for future improvement. Environ Int 79:25–41CrossRefGoogle Scholar
  48. Sutka RL, Ostrom NE, Ostrom PH, Gandhi H, Breznak JA (2003) Nitrogen isotopomer site preference of N2O produced by Nitrosomonas europaea and Methylococcus capsulatus Bath. Rapid Commun Mass Sp 17:738–745CrossRefGoogle Scholar
  49. Sutka RL, Ostrom NE, Ostrom PH, Breznak JA, Gandhi H, Pitt AJ, Li F (2006) Distinguishing nitrous oxide production from nitrification and denitrification on the basis of isotopomer abundances. Appl Environ Microb 72:638–644CrossRefGoogle Scholar
  50. Sutka RL, Adams GC, Ostrom NE, Ostrom PH (2008) Isotopologue fractionation during N2O production by fungal denitrification. Rapid Commun Mass Sp 22:3989–3996CrossRefGoogle Scholar
  51. Stevens RJ, Laughlin RJ, Malone JP (1998) Soil pH affects the processes reducing nitrate to nitrous oxide and di-nitrogen. Soil Biol Biochem 30:1119–1126CrossRefGoogle Scholar
  52. Tiedje JM, Sexstone AJ, Myrold DD, Robinson JA (1983) Denitrification: ecological niches, competition and survival. Anton Leeuw Int J G 48:569–583CrossRefGoogle Scholar
  53. Thamdrup B, Dalsgaard T (2002) Production of N2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl Environ Microb 68:1312–1318CrossRefGoogle Scholar
  54. Tong C, Zhang L, Wang W, Gauci V, Marrs R, Liu B, Zeng C (2011) Contrasting nutrient stocks and litter decomposition in stands of native and invasive species in a sub-tropical estuarine marsh. Environ Res 111:909–916CrossRefGoogle Scholar
  55. Toyoda S, Yano M, Nishimura SI, Akiyama H, Hayakawa A, Koba K, Ogawa NO (2011) Characterization and production and consumption processes of N2O emitted from temperate agricultural soils determined via isotopomer ratio analysis. Global Biogeochem Cy 25:96–101CrossRefGoogle Scholar
  56. Toyoda S, Mutobe H, Yamagishi H, Yoshida N, Tanji Y (2005) Fractionation of N2O isotopomers during production by denitrifier. Soil Biol Biochem 37:1535–1545CrossRefGoogle Scholar
  57. Wang DQ, Chen ZL, Wang J, Xu SY, Yang HX, Chen H, Yang LY, Hu LZ (2007) Summer-time denitrification and nitrous oxide exchange in the intertidal zone of the Yangtze estuary. Estuar Coast Shelf S 73:43–53CrossRefGoogle Scholar
  58. Wei J, Zhou M, Vereecken H, Brüggemann N (2017) Large variability in CO2 and N2O emissions and in 15N site preference of N2O from reactions of nitrite with lignin and its derivatives at different pH. Rapid Commun Mass Sp 31:1333–1343CrossRefGoogle Scholar
  59. Wrage N, Velthof GL, Van Beusichem ML, Oenema O (2001) Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol Biochem 33:1723–1732CrossRefGoogle Scholar
  60. Wrage-Mönnig N, Horn MA, Well R, Müller C, Velthof G, Oenema O (2018) The role of nitrifier denitrification in the production of nitrous oxide revisited. Soil Biol Biochem 123:A3–A16CrossRefGoogle Scholar
  61. Wu LB, Liu XD, Fang YT, Hou SJ, Xu LQ, Wang XY, Fu PQ (2018) Nitrogen cycling in the soil–plant system along a series of coral islands affected by seabirds in the South China Sea. Sci Total Environ 627:166–175CrossRefGoogle Scholar
  62. Wunderlin P, Mohn J, Joss A, Emmenegger L, Siegrist H (2012) Mechanisms of N2O production in biological wastewater treatment under nitrifying and denitrifying conditions. Water Res 46:1027–1037CrossRefGoogle Scholar
  63. Wunderlin P, Lehmann MF, Siegrist H, Tuzson B, Joss A, Emmenegger L, Mohn J (2013) Isotope signatures of N2O in a mixed microbial population system: constraints on N2O producing pathways in wastewater treatment. Environ Sci Technol 47:1339–1348CrossRefGoogle Scholar
  64. Yang W, Yan YE, Jiang F, Leng X, Chen XL, An SQ (2016) Response of the soil microbial community composition and biomass to a short-term Spartina alterniflora invasion in a coastal wetland of eastern China. Plant Soil 408:443–456CrossRefGoogle Scholar
  65. Yang WH, Teh YA, Silver WL (2011) A test of a field-based 15 N–nitrous oxide pool dilution technique to measure gross N2O production in soil. Glob Chang Biol 17:3577–3588CrossRefGoogle Scholar
  66. Yang WH, Silver WL (2016) Gross nitrous oxide production drives net nitrous oxide fluxes across a salt marsh landscape. Glob Chang Biol 22:2228–2237CrossRefGoogle Scholar
  67. Yin GY, Hou LJ, Liu M, Liu ZF, Gardner WS (2014) A novel membrane inlet mass spectrometer method to measure 15NH4 + for isotope-enrichment experiments in aquatic ecosystems. Environ Sci Technol 48:9555–9562CrossRefGoogle Scholar
  68. Yin GY, Hou LJ, Liu M, Li XF, Zheng YL, Gao J, Lin XB (2017) DNRA in intertidal sediments of the Yangtze estuary. J Geophys Res Biogeosci 122:1988–1998CrossRefGoogle Scholar
  69. Yu X, Yang J, Liu L, Tian Y, Yu Z (2015) Effects of Spartina alterniflora invasion on biogenic elements in a subtropical coastal mangrove wetland. Environ Sci Pollut R 22:3107–3115CrossRefGoogle Scholar
  70. Yuan J, Ding W, Liu D, Kang H, Freeman C, Xiang J, Lin Y (2015) Exotic Spartina alterniflora invasion alters ecosystem–atmosphere exchange of CH4 and N2O and carbon sequestration in a coastal salt marsh in China. Glob Chang Biol 21:1567–1580CrossRefGoogle Scholar
  71. Zhang WL, Zeng CS, Tong C, Zhai SJ, Lin X, Gao DZ (2015) Spatial distribution of phosphorus speciation in marsh sediments along a hydrologic gradient in a subtropical estuarine wetland, China. Estuar Coast Shelf S 154:30–38CrossRefGoogle Scholar
  72. Zhang Y, Wang L, Xie X, Huang L, Wu Y (2013) Effects of invasion of Spartina alterniflora and exogenous N deposition on N2O emissions in a coastal salt marsh. Ecol Eng 58:77–83CrossRefGoogle Scholar
  73. Zhang W, Li Y, Xu C, Li Q, Lin W (2016) Isotope signatures of N2O emitted from vegetable soil: Ammonia oxidation drives N2O production in NH4 +-fertilized soil of North China. Sci Rep 6:29257CrossRefGoogle Scholar
  74. Zheng YL, Hou LJ, Liu M, Yin GY, Gao J, Jiang XF, Wang R (2016) Community composition and activity of anaerobic ammonium oxidation bacteria in the rhizosphere of salt-marsh grass Spartina alterniflora. Appl Microbiol Biot 100:8203–8212CrossRefGoogle Scholar
  75. Zhu X, Burger M, Doane TA, Horwath WR (2013) Ammonia oxidation pathways and nitrifier denitrification are significant sources of N2O and NO under low oxygen availability. P Natl Acad Sci USA 110:201219993Google Scholar
  76. Zou Y, Hirono Y, Yanai Y, Hattori S, Toyoda S, Yoshida N (2014) Isotopomer analysis of nitrous oxide accumulated in soil cultivated with tea (Camellia sinensis) in Shizuoka, Central Japan. Soil Biol Biochem 77:276–291CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.College of Geographical SciencesEast China Normal UniversityShanghaiChina
  2. 2.State Key Laboratory of Estuarine and Coastal ResearchEast China Normal UniversityShanghaiChina
  3. 3.Key Laboratory for Humid Subtropical Eco-geographical Processes of the Ministry of EducationFujian Normal UniversityFuzhouChina

Personalised recommendations