Abstract
Purpose
The quality of organic matter influencing sediment nitrate (NO3−) reduction processes in estuarine zones is not well understood. This study aimed to assess the denitrification (DNF), anaerobic ammonium oxidation (ANA), and dissimilatory reduction of nitrate to ammonium (DNRA) in estuarine zones of South Africa, and to understand the effects of organic matter fractions and degradation states on anaerobic NO3− reduction processes.
Materials and methods
We measured the anaerobic NO3− reduction process rates using 15N isotope-tracing techniques in Knysna Estuary, South Africa. Total hydrolyzable amino acids and fractions and geochemical parameters were also measured. The correlation analysis and structural equation model were used to evaluate the key environmental factors driving NO3− reduction processes.
Results and discussion
Potential DNF, ANA, and DNRA rates in Knysna Estuary varied from 3.59 to 16.62, 0.28 to 1.16, and 1.52 to 8.38 nmol g−1 h−1, respectively, with a large spatial variation. The variations in NO3− reduction process rates can largely be explained by sediment water content, dissolved organic carbon, and amino acid–based degradation index, while the total organic carbon and inorganic nitrogen contents were not related to the NO3− reduction processes. The DNF process contributed 47.28–79.34% total NO3− reduction, as compared to 17.59–47.58% for DNRA and 2.53–5.76% for ANA. The retention of reactive nitrogen (N) attributed to the DNRA process was approximately 42 t N km−2 year−1.
Conclusions
This study reported the first simultaneous investigation of the anaerobic NO3− reduction processes in estuarine areas of South Africa, implying that the qualities of substrate were more important in regulating NO3− reduction processes than substrate quantities and highlighting that DNRA played an important role in reactive N retention.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Change history
06 August 2021
A Correction to this paper has been published: https://doi.org/10.1007/s11368-021-03033-7
References
Allanson BR, Human LRD, Claassens L (2016) Observations on the distribution and abundance of a green tide along an intertidal shore, Knysna Estuary. S Afr J Bot 107:49–54. https://doi.org/10.1016/j.sajb.2016.02.197
Babbin AR, Keil RG, Devol AH, Ward BB (2014) Organic matter stoichiometry, flux, and oxygen control nitrogen loss in the ocean. Science 344:406–408. https://doi.org/10.1126/science.1248364
Bai J, Ouyang H, Deng W, Zhu Y, Zhang X, Wang Q (2005) Spatial distribution characteristics of organic matter and total nitrogen of marsh soils in river marginal wetlands. Geoderma 124:181–192. https://doi.org/10.1016/j.geoderma.2004.04.012
Battye W, Aneja VP, Schlesinger WH (2017) Is nitrogen the next carbon? Earth’s future 5:894–904. https://doi.org/10.1002/2017EF000592
Bonaglia S, Hylén A, Rattray JE, Kononets MY, Ekeroth N, Roos P, Thamdrup B, Brüchert V, Hall POJ (2017) The fate of fixed nitrogen in marine sediments with low organic loading: an in situ study. Biogeosciences 14:285–300. https://doi.org/10.5194/bg-14-285-2017
Brin LD, Giblin AE, Rich JJ (2014) Environmental controls of anammox and denitrification in southern New England estuarine and shelf sediments. Limnol Oceanogr 59:851–860. https://doi.org/10.4319/lo.2014.59.3.0851
Canfield DE, Glazer AN, Falkowski PG (2010) The evolution and future of Earth’s nitrogen cycle. Science 330:192–196. https://doi.org/10.1126/science.1186120
Cao W, Yang J, Li Y, Liu B, Wang F, Chang C (2016) Dissimilatory nitrate reduction to ammonium conserves nitrogen in anthropogenically affected subtropical mangrove sediments in Southeast China. Mar Pollut Bull 110:155–161. https://doi.org/10.1016/j.marpolbul.2016.06.068
Carlson HK, Lui LM, Price MN, Kazakov AE, Carr AV, Kuehl JV, Owens TK, Nielsen T, Arkin AP, Deutschbauer AM (2020) Selective carbon sources influence the end products of microbial nitrate respiration. ISME J 14:2034–2045. https://doi.org/10.1038/s41396-020-0666-7
Chambers LG, Osborne TZ, Reddy KR (2013) Effect of salinity-altering pulsing events on soil organic carbon loss along an intertidal wetland gradient: a laboratory experiment. Biogeochemistry 115:363–383. https://doi.org/10.1007/s10533-013-9841-5
Cline JD (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14:454–458. https://doi.org/10.4319/lo.1969.14.3.0454
Cui S, Shi Y, Groffman PM, Schlesinger WH, Zhu Y-G (2013) Centennial-scale analysis of the creation and fate of reactive nitrogen in China (1910-2010). Proc Natl Acad Sci U S A 110:2052–2057. https://doi.org/10.1073/pnas.1221638110
Dalsgaard T, Thamdrup B (2002) Factors controlling anaerobic ammonium oxidation with nitrite in marine sediments. Appl Environ Microbiol 68:3802–3808. https://doi.org/10.1128/AEM.68.8.3802-3808.2002
Damashek J, Francis CA (2018) Microbial nitrogen cycling in estuaries: from genes to ecosystem processes. Estuaries Coasts 41:626–660. https://doi.org/10.1007/s12237-017-0306-2
Dauwe B, Middelburg JJ, Herman PMJ, Heip CHR (1999) Linking diagenetic alteration of amino acids and bulk organic matter reactivity. Limnol Oceanogr 44:1809–1814. https://doi.org/10.4319/lo.1999.44.7.1809
Decleyre H, Heylen K, Van Colen C, Willems A (2015) Dissimilatory nitrogen reduction in intertidal sediments of a temperate estuary: small scale heterogeneity and novel nitrate-to-ammonium reducers. Front Microbiol 6:1124. https://doi.org/10.3389/fmicb.2015.01124
Deegan LA, Johnson DS, Warren RS, Peterson BJ, Fleeger JW, Fagherazzi S, Wollheim WM (2012) Coastal eutrophication as a driver of salt marsh loss. Nature 490:388–392. https://doi.org/10.1038/nature11533
Deng F, Hou L, Liu M, Zheng Y, Yin G, Li X, Lin X, Chen F, Gao J, Jiang X (2015) Dissimilatory nitrate reduction processes and associated contribution to nitrogen removal in sediments of the Yangtze Estuary. J Geophys Res: Biogeosciences 120:1521–1531. https://doi.org/10.1002/2015jg003007
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 Microbiol 68:1240–1249. https://doi.org/10.1128/AEM.68.3.1240-1249.2002
Dong LF, Sobey MN, Smith CJ, Rusmana I, Phillips W, Stott A, Osborn AM, Nedwell DB (2011) Dissimilatory reduction of nitrate to ammonium, not denitrification or anammox, dominates benthic nitrate reduction in tropical estuaries. Limnol Oceanogr 56:279–291. https://doi.org/10.4319/lo.2011.56.1.0279
Fozia ZY, Hou L, Zhang Z, Gao D, Yin G, Han P, Dong H, Liang X, Yang Y, Liu M (2020) Community dynamics and activity of nirS-harboring denitrifiers in sediments of the Indus River Estuary. Mar Pollut Bull 153:110971. https://doi.org/10.1016/j.marpolbul.2020.110971
Giblin AE, Tobias CR, Song B, Weston N, Banta GT, Rivera-Monroy VH (2013) The importance of dissimilatory nitrate reduction to ammonium (DNRA) in the nitrogen cycle of coastal ecosystems. Oceanography 26:124–131. https://doi.org/10.5670/oceanog.2013.54
Gosling P, Parsons N, Bending GD (2013) What are the primary factors controlling the light fraction and particulate soil organic matter content of agricultural soils? Biol Fertil Soils 49:1001–1014. https://doi.org/10.1007/s00374-013-0791-9
Hecky RE, Mopper K, Kilham P, Degens ET (1973) The amino acid and sugar composition of diatom cell-walls. Mar Biol 19:323–331. https://doi.org/10.1007/BF00348902
Hou L, Liu M, Carini SA, Gardner WS (2012) Transformation and fate of nitrate near the sediment–water interface of Copano Bay. Cont Shelf Res 35:86–94. https://doi.org/10.1016/j.csr.2012.01.004
Hou LJ, Zheng YL, 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: Biogeosciences 118:1237–1246. https://doi.org/10.1002/jgrg.20108
Human LRD, Adams JB, Allanson BR (2016) Insights into the cause of an Ulva lactuca Linnaeus bloom in the Knysna Estuary. S Afr J Bot 107:55–62. https://doi.org/10.1016/j.sajb.2016.05.016
Human LRD, Weitz R, Allanson BR, Adams JB (2020) Nutrient fluxes from sediments pose management challenges for the Knysna Estuary, South Africa. Afr J Aquat Sci 45:1–9. https://doi.org/10.2989/16085914.2019.1671787
Jin B, Lai DYF, Gao D, Tong C, Zeng C (2017) Changes in soil organic carbon dynamics in a native C4 plant-dominated tidal marsh following spartina alterniflora invasion. Pedosphere 27:856–867. https://doi.org/10.1016/S1002-0160(17)60396-5
Kessler AJ, Roberts KL, Bissett A, Cook PLM (2018) Biogeochemical controls on the relative importance of denitrification and dissimilatory nitrate reduction to ammonium in estuaries. Global Biogeochem Cycles 32:1045–1057. https://doi.org/10.1029/2018GB005908
Largier J, Attwood C, Harcourt-Baldwin J-L (2000) The hydrographic character of the Knysna Estuary. Trans R Soc S Afr 55:107–122. https://doi.org/10.1080/00359190009520437
Lee C, Wakeham SG, Hedges IJ (2000) Composition and flux of particulate amino acids and chloropigments in equatorial Pacific seawater and sediments. Deep Sea Res Part I 47:1535–1568. https://doi.org/10.1016/S0967-0637(99)00116-8
Li XF, Gao DZ, Hou LJ, Liu M (2018) Salinity stress changed the biogeochemical controls on CH4 and N2O emissions of estuarine and intertidal sediments. Sci Total Environ 652:593–601. https://doi.org/10.1016/j.scitotenv.2018.10.294
Li XF, Gao DZ, Hou LJ, Liu M (2019) Soil substrates rather than gene abundance dominate DNRA capacity in the Spartina alterniflora ecotones of estuarine and intertidal wetlands. Plant Soil 436:123–140. https://doi.org/10.1007/s11104-018-03914-w
Li XF, Qian W, Hou LJ, Liu M, Chen ZB, Tong C (2020) Soil organic carbon controls dissimilatory nitrate reduction to ammonium along a freshwater-oligohaline gradient of Min River Estuary, Southeast China. Mar Pollut Bull 160:111696. https://doi.org/10.1016/j.marpolbul.2020.111696
Liu Z, Xue J (2020) The lability and source of particulate organic matter in the northern gulf of mexico hypoxic zone. J Geophys Res: Biogeosciences 125:e2020JG005653. https://doi.org/10.1029/2020JG005653
Lovley DR, Phillips EJ (1987) Rapid assay for microbially reducible ferric iron in aquatic sediments. Appl Environ Microbiol 53:1536–1540. https://doi.org/10.1128/AEM.53.7.1536-1540.1987
Maie N, Boyer JN, Yang C, Jaffé R (2006) Spatial, geomorphological, and seasonal variability of CDOM in estuaries of the Florida Coastal Everglades. Hydrobiologia 569:135–150. https://doi.org/10.1007/s10750-006-0128-x
Marcé R, von Schiller D, Aguilera R, Martí E, Bernal S (2018) Contribution of hydrologic opportunity and biogeochemical reactivity to the variability of nutrient retention in river networks. Global Biogeochem Cycles 32:376–388. https://doi.org/10.1002/2017GB005677
Mctigue ND, Gardner WS, Dunton KH, Hardison AK (2016) Biotic and abiotic controls on co-occurring nitrogen cycling processes in shallow Arctic shelf sediments. Nat Commun 7:13145. https://doi.org/10.1038/ncomms13145
Murphy AE, Anderson IC, Smyth AR, Song B, Luckenbach MW (2016) Microbial nitrogen processing in hard clam (Mercenaria mercenaria) aquaculture sediments: the relative importance of denitrification and dissimilatory nitrate reduction to ammonium (DNRA). Limnol Oceanogr 61:1589–1604. https://doi.org/10.1002/lno.10305
Murray RH, Erler DV, Eyre BD (2015) Nitrous oxide fluxes in estuarine environments: response to global change. Glob Chang Biol 21:3219–3245. https://doi.org/10.1111/gcb.12923
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 Acta 238:169–192. https://doi.org/10.1016/j.gca.2018.07.003
Pang Y, Wang J, Li S, Ji G (2021) Long-term sulfide input enhances chemoautotrophic denitrification rather than DNRA in freshwater lake sediments. Environ Pollut 270:116201. https://doi.org/10.1016/j.envpol.2020.116201
Plummer P, Tobias C, Cady D (2015) Nitrogen reduction pathways in estuarine sediments: influences of organic carbon and sulfide. J Geophys Res: Biogeosciences 120:1958–1972. https://doi.org/10.1002/2015JG003057
Poffenbarger HJ, Needelman BA, Megonigal JP (2011) Salinity influence on methane emissions from tidal marshes. Wetlands 31:831–842. https://doi.org/10.1007/s13157-011-0197-0
Raw JL, Riddin T, Wasserman J, Lehman TWK, Bornman TG, Adams JB (2020) Salt marsh elevation and responses to future sea-level rise in the Knysna Estuary, South Africa. Afr J Aquat Sci 45:49–64. https://doi.org/10.2989/16085914.2019.1662763
Risgaard-Petersen N, Nielsen LP, Rysgaard S, Dalsgaard T, Meyer RL (2003) Application of the isotope pairing technique in sediments where anammox and denitrification coexist. Limnol Oceanogr Methods 1:63–73. https://doi.org/10.4319/lom.2003.1.63
Roberts KL, Kessler AJ, Grace MR, Cook PLM (2014) Increased rates of dissimilatory nitrate reduction to ammonium (DNRA) under oxic conditions in a periodically hypoxic estuary. Geochim Cosmochim Acta 133:313–324. https://doi.org/10.1016/j.gca.2014.02.042
Roland FAE, Darchambeau F, Borges AV, Morana C, De Brabandere L, Thamdrup B, Crowe SA (2018) Denitrification, anaerobic ammonium oxidation, and dissimilatory nitrate reduction to ammonium in an East African Great Lake (Lake Kivu). Limnol Oceanogr 63:687–701. https://doi.org/10.1002/lno.10660
Salas PM, Sujatha CH, Ratheesh Kumar CS, Cheriyan E (2018) Amino acids as indicators to elucidate organic matter degradation profile in the Cochin estuarine sediments, Southwest coast of India. Mar Pollut Bull 127:273–284. https://doi.org/10.1016/j.marpolbul.2017.12.010
Sheridan CC, Lee C, Wakeham SG, Bishop JKB (2002) Suspended particle organic composition and cycling in surface and midwaters of the equatorial Pacific Ocean. Deep Sea Res Part I 49:1983–2008. https://doi.org/10.1016/S0967-0637(02)00118-8
Smith CJ, Dong LF, Wilson J, Stott A, Osborn AM, Nedwell DB (2015) Seasonal variation in denitrification and dissimilatory nitrate reduction to ammonia process rates and corresponding key functional genes along an estuarine nitrate gradient. Front Microbiol 6:542. https://doi.org/10.3389/fmicb.2015.00542
Switzer T (2008) Urea loading from a spring storm—Knysna estuary, South Africa. Harmful Algae 8:66–69. https://doi.org/10.1016/j.hal.2008.08.005
Taillardat P, Marchand C, Friess DA, Widory D, David F, Ohte N, Nakamura T, Van Vinh T, Thanh-Nho N, Ziegler AD (2020) Respective contribution of urban wastewater and mangroves on nutrient dynamics in a tropical estuary during the monsoon season. Mar Pollut Bull 160:111652. https://doi.org/10.1016/j.marpolbul.2020.111652
Tan E, Zou W, Jiang X, Wan X, Hsu TC, Zheng Z, Chen L, Xu M, Dai M, Kao SJ (2019) Organic matter decomposition sustains sedimentary nitrogen loss in the Pearl River Estuary, China. Sci Total Environ 648:508–517. https://doi.org/10.1016/j.scitotenv.2018.08.109
Teixeira C, Magalhães C, Joye SB, Bordalo AA (2012) Potential rates and environmental controls of anaerobic ammonium oxidation in estuarine sediments. Aquat Microb Ecol 66:23–32. https://doi.org/10.3354/ame01548
Wang K, Chen J, Jin H, Li H, Zhang W (2018) Organic matter degradation in surface sediments of the Changjiang estuary: evidence from amino acids. Sci Total Environ 637-638:1004–1013. https://doi.org/10.1016/j.scitotenv.2018.04.242
Wang R, Li X, Hou L, Liu M, Zheng Y, Yin G, Yang Y (2018) Nitrogen fixation in surface sediments of the East China Sea: occurrence and environmental implications. Mar Pollut Bull 137:542–548. https://doi.org/10.1016/j.marpolbul.2018.10.063
Wang C, Liu D, Bai E (2018) Decreasing soil microbial diversity is associated with decreasing microbial biomass under nitrogen addition. Soil Biol Biochem 120:126–133. https://doi.org/10.1016/j.soilbio.2018.02.003
Wankel SD, Ziebis W, Buchwald C, Charoenpong C, de Beer D, Dentinger J, Xu Z, Zengler K (2017) Evidence for fungal and chemodenitrification based N2O flux from nitrogen impacted coastal sediments. Nat Commun 8:15595. https://doi.org/10.1038/ncomms15595
Wei H, Gao D, Liu Y, Lin X (2020) Sediment nitrate reduction processes in response to environmental gradients along an urban river-estuary-sea continuum. Sci Total Environ 718:137185. https://doi.org/10.1016/j.scitotenv.2020.137185
Xue J, Lee C, Wakeham SG, Armstrong RA (2011) Using principal components analysis (PCA) with cluster analysis to study the organic geochemistry of sinking particles in the ocean. Org Geochem 42:356–367. https://doi.org/10.1016/j.orggeochem.2011.01.012
Yang G, Peng Y, Olefeldt D, Chen Y, Wang G, Li F, Zhang D, Wang J, Yu J, Liu L, Qin S, Sun T, Yang Y (2018) Changes in methane flux along a permafrost thaw sequence on the Tibetan Plateau. Environ Sci Technol 52:1244–1252. https://doi.org/10.1021/acs.est.7b04979
Yin G, Hou L, Liu M, Liu Z, Gardner WS (2014) A novel membrane inlet mass spectrometer method to measure 15NH4+ for isotope-enrichment experiments in aquatic ecosystems. Environ Sci Technol 48:9555–9562. https://doi.org/10.1021/es501261s
Zheng Y, Hou L, Liu M, Liu Z, Li X, Lin X, Yin G, Gao J, Yu C, Wang R, Jiang X (2016) Tidal pumping facilitates dissimilatory nitrate reduction in intertidal marshes. Sci Rep 6:21338. https://doi.org/10.1038/srep21338
Acknowledgements
Thanks to Dr. Jianhong Xue for guidance and help in conducting the experiments. We also thank Dr. Jianli Guo for assistance with language editing on the earlier version of this draft. Thanks are given to the editors and anonymous reviewers for constructive comments and suggestions on this manuscript. We acknowledge the Department of Environmental & Geographical Science, University of Cape Town, for assistance with fieldwork and logistics. The work was conducted under the South African National Parks research permit number: MEAD-ME/2018-007.
Funding
This work was supported by the Natural Science Foundation of China (grant numbers: 41761144062, 41725002, 42030411, and 41730646) and by the National Research Foundation of South Africa (grant number: 110776). It was also funded by Chinese National Key Programs for Fundamental Research and Development (nos. 2016YFA0600904 and 2016YFE0133700) and Fundamental Research Funds for the Central Universities.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Responsible Editor: Hongbin Yin
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The original online version of this article was revised: Modifications have been made to the Acknowledgements and Funding sections. Full information regarding the corrections made can be found in the correction for this article.
Supplementary information
ESM 1
(DOCX 99 kb)
Rights and permissions
About this article
Cite this article
Chang, Y., Hou, L., Gao, D. et al. Organic matter degradation state affects dissimilatory nitrate reduction processes in Knysna estuarine sediment, South Africa. J Soils Sediments 21, 3202–3212 (2021). https://doi.org/10.1007/s11368-021-02925-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11368-021-02925-y