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Dissimilatory nitrate reduction and functional genes in two subtropical rivers, China

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Abstract

Dissimilatory nitrate reduction processes, including denitrification, anaerobic ammonium oxidation (anammox), and dissimilatory nitrate reduction to ammonium (DNRA), are important pathways of nitrate transformation in the aquatic environments. In this study, we investigated potential rates of denitrification, anammox, and DNRA in the sediments of two subtropical rivers, Jinshui River and Qi River, with different intensities of human activities in their respective catchment, China. Our objectives were to assess the seasonality of dissimilatory nitrate reduction rates, quantify their respective contributions to nitrate reduction, and reveal the relationship between dissimilatory nitrate reduction rates, functional gene abundances, and physicochemicals in the river ecosystems. Our results showed higher rates of denitrification and anammox in the intensively disturbed areas in autumn and spring, and higher potential DNRA in the slightly disturbed areas in summer. Generally, denitrification, anammox, and DNRA were higher in summer, autumn, and spring, respectively. Relative contributions of nitrate reduction from denitrification, anammox, and DNRA were quite different in different seasons. Dissimilatory nitrate reduction rates and gene abundances correlated significantly with water temperature, dissolved organic carbon (DOC), sediment total organic carbon (SOC), NO3-, NH4+, DOC/NO3-, iron ions, and sulfide. Understanding dissimilatory nitrate reduction is essential for restoring nitrate reduction capacity and improving and sustaining ecohealth of the river ecosystems.

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References

  • An S, Gardner WS (2002) Dissimilatory nitrate reduction to ammonium (DNRA) as a nitrogen link, versus denitrification as a sink in a shallow estuary (Laguna Madre/Baffin Bay, Texas). Mar Ecol Prog Ser 237:41–50

  • An S, Gardner WS, Kana T (2001) Simultaneous measurement of denitrification and nitrogen fixation using isotope pairing with membrane inlet mass spectrometry analysis. Appl Environ Microbiol 67:1171–1178

  • Baeseman JL, Smith RL, Silverstein J (2006) Denitrification potential in stream sediments impacted by acid mine drainage: effects of pH, various electron donors, and iron. Microb Ecol 51(2):232–241

  • Bernard RJ, Mortazavi B, Kleinhuizen AA (2015) Dissimilatory nitrate reduction to ammonium (DNRA) seasonally dominates NO3- reduction pathways in an anthropogenically impacted sub-tropical coastal lagoon. Biogeochemistry 125(1):47–64

  • Bohlen L, Dale AW, Sommer S, Mosch T, Hensen C, Noffke A, Scholz F, Wallmann K (2011) Benthic nitrogen cycling traversing the peruvian oxygen minimum zone. Geochim Cosmochim Acta 75(20):6094–6111

  • Boldea O, Magnus JR (2009) Maximum likelihood estimation of the multivariate normal mixture model. J Am Stat Assoc 104:1539–1549

  • Braker G, Zhou JZ, Wu LY, Devol AH, Tiedjen JM (2000) Nitrite reductase genes (nirK and nirS) as functional markers to investigate diversity of denitrifying bacteria in Pacific Northwest marine sediment communities. Appl Environ Microbiol 66(5):2096–2104

  • Brin LD, Giblin AE, Rich JJ (2015) Effects of experimental warming and carbon addition on nitrate reduction and respiration in coastal sediments. Biogeochemistry 125:81–95

  • Brunet RC, Garcia-Gil LJ (1996) Sulfide-induced dissimilatory nitrate reduction to ammonia in anaerobic freshwater sediments, FEMS Microbiol. Ecol. 21(2):131–138

  • Bu C, Wang Y, Ge C, Ahmad HA, Gao B, Ni SQ (2017) Dissimilatory nitrate reduction to ammonium in the Yellow River Estuary: rates, abundance, and community diversity. Sci Rep 7(1). https://doi.org/10.1038/s41598-017-06404-8

  • Burgin AJ, Hamilton SK (2007) Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways. Front EcolEnviron 5(2):89–96

  • Cavari BZ, Phelps G (1977) Denitrification in Lake Kinneret in the presence of oxygen. Freshw Biol 7(4):385–391

  • Chen NW, Wu JZ, Hong HS (2011) Preliminary results concerning summer-time denitrification in the Jiulong River Estuary. Environ Sci 32(11):3229–3234

  • Chen LM, Liu ST, Chen Q, Zhu GB, Wu X, Wang JW, Li XF, Hou LJ, Ni JR (2019) Anammox response to natural and anthropogenic impact over the Yangtze river. Sci Total Environ 665(2019):171–180

  • Cheng L, Li XF, Lin XB, Hou LJ, Liu M, Li Y, Liu S, Hu XT (2016) Dissimilatory nitrate reduction processes in sediments of urban river networks: spatiotemporal variations and environmental implications. Environ Pollut 219(DEC):545–554

  • Cole JJ, Prairie YT, Caraco NF, Mcdowell WH, Tranvik LJ, Striegl RG, Duarte CM, Kortelainen P, Downing JA, Middelburg JJ, Melack J (2007) Plumbing the global carbon cycle: integrating inland waters into the terrestrial carbon budget. Ecosystems 10(1):171–184

  • Dale AW, Sommer S, Bohlen L, Treude T, Bertics VJ, Bange HW, Pfannkuche O, Schorp T, Mattsdotter M, Wallmann K (2011) Rates and regulation of nitrogen cycling in seasonally hypoxic sediments during winter (boknis eck, sw baltic sea): sensitivity to environmental variables. Estuar Coast Shelf Sci 95(1):14–28

  • Dalsgaard T, Thamdrup B (2002) Factors controlling anaerobic ammonium oxidation with nitrite in marine sediments. Appl Environ Microbiol 68(8):3802–3808

  • Davidsson TE, Ståhl M (2000) The influence of organic carbon on nitrogen transformations in five wetland soils. Soil Sci Soc Am J 64(3):1129–1136

  • 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

  • Deng F, Hou LJ, Liu M, Zheng YL, Yin GY, Li XF, Lin XB, Chen F, Gao J, Jiang XF (2015) Dissimilatory nitrate reduction processes and associated contribution to nitrogen removal in sediments of the Yangtze Estuary. J Geophys Res Biogeosci 120:1521–1531

  • Dong LF, Smith CJ, Papaspyrou S, Stott A, Osborn AM, Nedwell DB (2009) Changes in benthic denitrification, nitrate ammonification, and anammox process rates and nitrate and nitrite reductase gene abundances along an estuarine nutrient gradient (the colne estuary, united kingdom). Appl Environ Microbiol 75(10):3171–3179

  • 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(1):279–291

  • Enwall K, Philippot L, Hallin S (2005) Activity and composition of the denitrifying bacterial community respond differently to long-term fertilization. Appl Environ Microbiol 71(12):8335–8343. https://doi.org/10.1128/aem.71.12.8335-8343.2005

  • Feng J, Xu X, Wu JJ, Zhang Q, Zhang DD, Li QX, Long CY, Chen Q, Chen JW, Cheng XL (2018) Inhibited enzyme activities in soil macroaggregates contribute to enhanced soil carbon sequestration under afforestation in central china. Sci Total Environ 640-641(NOV.1):653–661. https://doi.org/10.1016/j.scitotenv.2018.05.332

  • Friedl J, De Rosa D, Rowlings DW, Grace PR, Müller C, Scheer C (2018) Dissimilatory nitrate reduction to ammonium (DNRA), not denitrification dominates nitrate reduction in subtropical pasture soils upon rewetting. Soil Biol Biochem 125:340–349. https://doi.org/10.1016/j.soilbio.2018.07.024

  • Gao SJ, Cao WD, Bai JS, Gao JS, Huang J, Zeng NH, Chang DN, Zhi SSH (2017a) Abundances of AOA-amoA, narG, nosZ genes and their relationships with soil environment factors in red paddy soils in south hunan province. Soil and Fertilizer Sciences in China. 21–27

  • Gao D, Li X, Lin X, Wu D, Chen X (2017b) Soil dissimilatory nitrate reduction processes in the spartina alterniflora invasion chronosequences of a coastal wetland of southeastern china: dynamics and environmental implications. Plant Soil 421:383–399

  • Gardner WS, Mccarthy MJ, An S, Sobolev D, Sell KS, Brock D (2006) Nitrogen fixation and dissimilatory nitrate reduction to ammonium (DNRA) support nitrogen dynamics in Texas estuaries. Limnol Oceanogr 51:558–568

  • Garzanti E, Andó S, Francelanord C, Censi P, Vignola P, Galy V, Lupker M (2011) Mineralogical and chemical variability of fluvial sediments 2. Suspended-load silt (Ganga-Brahmaputra, Bangladesh). Earth Planet. Sci Lett 302:107–120

  • Geets J, De Cooman M, Wittebolle L, Heylen K, Vanparys B, De Vos P, Verstraete W, Boon N (2007) Real-time PCR assay for the simultaneous quantification of nitrifying and denitrifying bacteria in activated sludge. Appl Microbiol Biotechnol 75:211–221

  • Gibbons SM, Jones E, Bearquiver A, Blackwolf F, Roundstone W, Scott N, Hooker J, Madsen R, Coleman ML, Gilbert JA (2014) Human and environmental impacts on river sediment microbial communities. PLoS One 9:e97435

  • Gilbert F, Souchu P, Bianchi M, Bonin P (1997) Influence of shellfish farming activities on nitrification, nitrate reduction to ammonium and denitrification at the water-sediment interface of the thau lagoon, france. Mar Ecol Prog Ser 151(1-3):143–153

  • Graham DW, Trippett C, Dodds WK, O’Brien JM, Banner EBK, Head IM, Smithd MS, Yang RK, Knapp CW (2010) Correlations between in situ denitrification activity and nir-gene abundances in pristine and impacted prairie streams. Environ Pollut 158(10):3225–3229

  • Gregory L, Philppot L, David J, Spiro S (2003) Characterization of a nitrate respiring bacteria community using the nitrate reductase gene (narG) as a functional marker. Microbiol 149:229–237

  • Gruber N, Galloway JN (2008) An Earth-system perspective of the global nitrogen cycle. Nature 451:293–296

  • Hahmann AN, Dickinson RE (1997) RCCM2-BATS model over tropical South America: Applications to tropical deforestation. J Clim 10(8):1944–1964

  • Henry S, Baudoin E, López-Gutiérrez JC, Martin-Laurent F, Brauman A, Philippot L (2004) Quantification of denitrifying bacteria in soils by nirK gene targeted real-time PCR. J Microbiol Methods 59(3):327–335. https://doi.org/10.1016/j.mimet.2004.07.002

  • Henry S, Bru D, Stres B, Hallet S, Philippot L (2006) Quantitative detection of the nosZ gene, encoding nitrous oxide reductase, and comparison of the abundances of 16S rRNA, narG, nirK, and nosZ genes in soils. Appl Environ Microbiol 72:5181–5189

  • Hernández-del Amo E, Menció A, Gich F, Mas-Pla J, Bañeras L (2018) Isotope and microbiome data provide complementary information to identify natural nitrate attenuation processes in groundwater. Sci Total Environ 613-614:579–591. https://doi.org/10.1016/j.scitotenv.2017.09.018

  • Hernández-del Amo E, Ramió-Pujol S, Gich F, Trias R, Bañeras L (2020) Changes in the potential activity of nitrite reducers and the microbial community structure after sediment dredging and plant removal in the Empuriabrava FWS-CW. Microbial Ecology 79(3).

  • Hirsch MD, Long ZT, Song B (2011) Anammox bacterial diversity in various aquatic ecosystems based on the detection of hydrazine oxidase genes (hzoA/hzoB). Microb Ecol 61(2):264–276

  • Hong YG, Li M, Cao H, Gu JD (2011) Residence of habitat-specific anammox bacteria in the deep-sea subsurface sediments of the south china sea: analyses of marker gene abundance with physical chemical parameters. Microb Ecol 62(1):36–47

  • Hou LJ, 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

  • 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 Biogeosci 118:1237–1246. https://doi.org/10.1002/jgrg.20108

  • Hou LJ, Zheng YL, Liu M, Li XF, Lin XB, Yin GY, Gao J, Deng FY, Chen F, Jiang XF (2015) Anaerobic ammonium oxidation and its contribution to nitrogen removal in China’s coastal wetlands. Sci Rep 5:15,621

  • Hu XT, Cheng L, Lin XB, Liu M, Hou LJ (2016) Temperature sensitivity and controlling factors of dissimilatory nitrate reduction processes in sediments of qingcaosha reservoir, yangtze estuary. China Environ Sci 36(9):2624–2632

  • Huang BQ, Liu Q, Li RF, Cao WH, Zhong JF (2012) Impacts of land use and land cover change on river. J Anhui Agric Sci 40(21):11073–11076 11136

  • Huang X, Li W, Zhang D, Qin W (2013) Ammonium removal by a novel oligotrophic Acinetobacter sp. Y16 capable of heterotrophic nitrification–aerobic denitrification at low temperature. Bioresour Technol 146:44–50. https://doi.org/10.1016/j.biortech.2013.07.046

  • Ikeda E, Andou S, Iwama U, Kato C, Horikoshi K, Tamegai H (2009) Physiological roles of two dissimilatory nitrate reductases in the deep-sea denitrifier Pseudomonas sp. strain MT-1. Biosci Biotechnol Biochem 73:896–900

  • Jäntti H, Stange F, Leskinen E, Hietanen S (2011) Seasonal variation in nitrification and nitrate-reduction pathways in coastal sediments in the Gulf of Finland. Baltic Sea Aquat Microb Ecol 63:171–181

  • Jensen MM, Kuyoers MMM, Lavik G, Thamdrup B (2008) Rates and regulation of anaerobic ammonium oxidation and denitrification in the Black Sea. Limnol Oceanogr 53:23–36

  • Jensen MM, Lam P, Revsbech NP (2011) Intensive nitrogen loss over the Omani shelf due to anammox coupled with dissimilatory nitrite reduction to ammonium. ISME J 5:1660–1670

  • Jousset A, Schmid B, Scheu S, Eisenhauer N (2011) Genotypic richness and dissimilarity opposingly affect ecosystem functioning. Ecol Lett 14(6):537–545

  • Jung SP, Kim YJ, Kang H (2014) Denitrification rates and their controlling factors in streams of the Han river basin with different land-use patterns. Pedosphere 24(4):516–528

  • Kana TM, Darkangelo C, Hunt MD, Oldham JB, Bennett GE, Cornwell JC (1994) Membrane inlet mass spectrometer for rapid high-precision determination of N2, O2, and Ar in environmental water samples. Anal Chem 66:4166–4170

  • Kandeler E, Deiglmayr K, Tscherko D, Bru D, Philippot L (2006) Abundance of narG, nirS, nirK, and nosZ genes of denitrifying bacteria during primary successions of a glacier foreland. Appl Environ Microbiol 72:5957–5962

  • Kartal B, Rattray J, van Niftrik LA, van de Vossenberg J, Schmid MC, Schouten S, Fuerst JA, Damsté JS, Jetten MS, Strous M (2007a) Candidatus ‘Anammoxoglobus propionicus’ a new propionate oxidizing species of anaerobic ammonium oxidizing bacteria. Syst Appl Microbiol 30:39–49

  • Kartal B, Kuypers MMM, Lavik G, Schalk J, Op den Camp HJM, Jetten MSM, Strous M (2007b) Anammox bacteria disguised as denitrifiers: nitrate reduction to dinitrogen gas via nitrate and ammonium. Environ Microbiol 9:635–642

  • Kartal, B., W. J. Maalcke, N. M. De Almeida, I. Cirpus, J. Gloerich,W. Geerts, , H. J. M. Op den Camp, H. R. Harhangi, E. M. Janssen-Megens, K.J. Francoijs, H.G. Stunnenberg, J. T. Keltjens, M.S.M. Jetten and M. Strous(2011), Molecular mechanism of anaerobic ammonium oxidation. Nature, 479(7371), 127-130.

  • Kim IN, Lee K, Gruber N, Karl DM, Bullister JL, Yang S, Kim TW (2014) Increasing anthropogenic nitrogen in the North Pacific Ocean. Science 346:1102–1106

  • Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol 55(1):485–529. https://doi.org/10.1146/annurev.micro.55.1.485

  • Lam P, Lavik G, Jensen MM, van de Vossenberg J, Schmid M, Woebken D, Gutiérrez D, Amann R, Jetten MSM, Kuypers MMM (2009) Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proc Natl Acad Sci U S A 106:4752–4757

  • Li L, Davis AP (2014) Urban stormwater runoff nitrogen composition and fate in bioretention systems. Environ Sci Technol 48(6):3403–3410

  • Li M, Hong YG, Cao HL, Gu JD (2011) Mangrove trees affect the community structure and distribution of anammox bacteria at an anthropogenic-polluted mangrove in the pearl river delta reflected by 16s rRNA and hydrazine oxido reductase (hzo) encoding gene analyses. Ecotoxicology 20(8):1780–1790

  • Liu B, Mørkved PT, Frostegård Å, Bakken LR (2010) Denitrification gene pools, transcription and kinetics of NO, N2O and N2 production as affected by soil pH. FEMS Microbiol Ecol 72:407–417

  • Liu W, Yao L, Wang Z, Xiong Z, Liu G (2015) Human land uses enhance sediment denitrification and n2o production in Yangtze lakes primarily by influencing lake water quality. Biogeosciences 12:6059–6070

  • Liu C, Hou LJ, Liu M, Zheng YL, Yin GY, Han P, Dong HP, Gao DZ, Chang YK, Zhang ZX (2019) Coupling of denitrification and anaerobic ammonium oxidation with nitrification in sediments of the yangtze estuary: importance and controlling factors. Estuar Coast Shelf Sci 220:64–72

  • Llorens-Marès T, Yooseph S, Goll J, Hoffman J, Vila-Costa M, Borrego CM, Dupont CL, Casamayor EO (2015) Connecting biodiversity and potential functional role in modern euxinic environments by microbial metagenomics. The ISME Journal 9(7):1648–1661. https://doi.org/10.1038/ismej.2014.254

  • Lou HJ, Wang DQ, Chen ZL, Li YJ, Jiang H, Xu SY (2013) Main environmental factors affecting denitrification rate in sediment of Yangtze estuarine coast. Environ Sci Technol 36(4):114–118

  • Lovley DR, Phillips EJP (1987) Rapid assay for microbially reducible ferric iron in aquatic sediments. Appl Environ Microbiol 53:1536e1540

  • Lu WW, Zhang HL, Shi WM (2013) Dissimilatory nitrate reduction to ammonium in an anaerobic agricultural soil as affected by glucose and free sulfide. Eur J Soil Biol 58:98–104

  • Luvizotto DL, Araujo JE, Silva MDCP, Dias ACF, Kraft B, Tegetmeye H, Strous M, Andreote FD (2019) The rates and players of denitrification, dissimilatory nitrate reduction to ammonia (DNRA) and anaerobic ammonia oxidation (anammox) in mangrove soils. An Acad Bras Cienc 91(Suppl. 1):e20180373

  • Ma P, Li XY, Wang HX, Wang JN, Yan WJ (2014) Denitrification and its role in cycling and removal of nitrogen in river. Journal of Agro-Environment Science 33(4):623–633

  • Ma L, Jiang XL, Liu GH, Yao LG, Liu WZ, Pan YT, Zuo YX (2020) Environmental factors and microbial diversity and abundance jointly regulate soil nitrogen and carbon biogeochemical processes in Tibetan wetlands. Environ Sci Technol 54(6):3267–3277

  • 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

  • Meyer RL, Risgaard-Petersen N, Allen DE (2005) Correlation between anammox activity and microscale distribution of nitrite in a subtropical mangrove sediment. Appl Environ Microbiol 71:6142–6149

  • Minjeaud L, Michotey VD, Garcia N, Bonin PC (2009) Seasonal variation in dinitrogen fluxes and associated processes (denitrification, anammox and nitrogen fixation) in sediment subject to shellfish farming influences. Aquat Sci 71:425–435

  • Mulder A, Vandegraaf AA, Robertson LA, Kuenen JG (1995) Anaerobic ammonium oxidation discovered in a denitrifying fluidized-bed reactor. FEMS Microbiol Ecol 16(3):177–183

  • 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

  • Nijburg JW, Coolen M, Gerards S, Gunnewiek P, Laanbroek HJ (1997) Effects of nitrate availability and the presence of Glyceria maxima on the composition and activity of the dissimilatory nitrate-reducing bacterial community. Appl Environ Microbiol 63:931–937

  • Nishio T, Koike I, Hattori A (1982) Denitrification, nitrate reduction, and oxygen consumption in coastal and estuarine sediments. Appl Environ Microbiol 43(3):648–653

  • Nizzoli D, Carraro E, Nigro V, Viaroli P (2010) Effect of organic enrichment and thermal regime on denitrification and dissimilatory nitrate reduction to ammonium (dnra) in hypolimnetic sediments of two lowland lakes. Water Res 44(9):2724

  • Nogales B, Timmis KN, Nedwell DB, Osborn AM (2002) Detection and diversity of expressed denitrification genes in estuarine sediments after reverse transcription-PCR amplification from mRNA. Appl Environ Microbiol 68(10):5017–5025. https://doi.org/10.1128/aem.68.10.5017-5025.2002

  • Nogaro G, Burgin AJ (2014) Influence of bioturbation on denitrification and dissimilatory nitrate reduction to ammonium (dnra) in freshwater sediments. Biogeochemistry 120(1-3):279–294

  • Oshiki M, Ishii S, Yoshida K, Fujii N, Ishiguro M, Satoh H, Okabe S (2013) Nitrate-dependent ferrous iron oxidation by anaerobic ammonium oxidation (anammox) bacteria. Appl Environ Microbiol 79(13):4087–4093

  • Pang YM, Ji GD (2019) Biotic factors drive distinct DNRA potential rates and contributions in typical Chinese shallow lake sediments. Environ Pollut 254:112903

  • Philippot L, Højberg O (1999) Dissimilatory nitrate reductases in bacteria. Biochim Biophys Acta 1446:1–23

  • Philippot L, Spor A, Hénault C, Bru D, Bizouard F, Jones CM, Sarr A, Maron PA (2013) Loss in microbial diversity affects nitrogen cycling in soil. ISME J 7(8):1609–1619

  • Philppot L (2002) Denitrifying genes in bacterial and archaeal genomes. Biochim Biophys Acta 1577:355–376

  • Porubsky WP, Velasquez LE, Joye SB (2008) Nutrient-replete benthic microalgae as a source of dissolved organic carbon to coastal waters. Estuar Coasts 31:860–876

  • Quan ZX, Rhee SK, Zuo JE, Yang Y, Bae JW, Park JR, Lee ST, Park YH (2008) Diversity of ammonium-oxidizing bacteria in a granular sludge anaerobic ammonium-oxidizing (anammox) reactor. Environ Microbiol 10:3130–3139

  • Rahman MM, Roberts KL, Grace MR, Kessler AJ, Cook PLM (2019a) Role of organic carbon, nitrate and ferrous iron on the partitioning between denitrification and DNRA in constructed stormwater urban wetlands. Sci Total Environ 666:608–617

  • Rahman MM, Roberts KL, Warry F, Grace MR, Cook PLM (2019b) Factors controlling dissimilatory nitrate reduction processes in constructed stormwater urban wetlands. Biogeochemistry 142:375–393

  • Richardson DJ, Ferguson SJ (1992) The influence of carbon substrate on the activity of the periplasmic nitrate reductase in aerobically grown thiosphaera pantotropha. Arch Microbiol 157(6):535–537

  • 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(1):63–73

  • Roberts KL, Eate VM, Eyre BD, Holland DP, Cook PLM (2012) Hypoxic events stimulate nitrogen recycling in a shallow salt-wedge estuary: the Yarra River estuary. Australia Limnol Oceanogr 57:1427–1442

  • Roberts KL, Velasquez LE, Joye SB (2014) Increased rates of dissimilatory nitrate reduction to ammonium (DNRA) under oxic conditions in a periodically hypoxic estuary. Geochim Cosmochim Acta 133:313–324

  • Robertson EK, Roberts KL, Burdorf LD, Cook P, Thamdrup B (2016) Dissimilatory nitrate reduction to ammonium coupled to Fe (II) oxidation in sediments of a periodically hypoxic estuary. Limnol Oceanogr 61(1):365–381

  • Rocca JD, Hall EK, Lennon JT, Evans SE, Waldrop MP, Cotner JB, Nemergut DR, Graham EB, Wallenstein MD (2014) Relationships between protein-encoding gene abundance and corresponding process are commonly assumed yet rarely observed. ISME J 9:1693

  • Schermelleh-Engel K, Moosbrugger H, Müller H (2003) Evaluating the fit of structural equation models: tests of significance and descriptive goodness-of-fit measures. Method Psychol Res 8:23–74

  • Schmid, M. C., A. B. Hooper, M. G. Klotz, D. Woebken, P. Lam, M. M. M Kuypers, , A. Pommerening-Roeser, H. J. M. Op Den Camp, M. S. M. Jetten (2008), Environmental detection of octahaem cytochrome c hydroxylamine / hydrazine oxidoreductase genes of aerobic and anaerobic ammonium-oxidizing bacteria. Environ Microbiol, 10( 11) : 3140-3149.

  • Scott JT, McCarthy MJ, Gardner WS, Doyle RD (2008) Denitrification, dissimilatory nitrate reduction to ammonium, and nitrogen fixation along a nitrate concentration gradient in a created freshwater wetland. Biogeochemistry 87:99–111. https://doi.org/10.1007/s10533-007-9171-6

  • Sears K, Alleman JE, Barnard JL, Oleszkiewicz JA (2004) Impacts of reduced sulfur components on active and resting ammonia oxidizers. J Ind Microbiol Biotechnol 3:369–378

  • Shan J, Zhao X, Sheng R, Xia Y, Ti C, Quan X, Wang S, Wei W, Yan X (2016) Dissimilatory nitrate reduction processes in typical Chinese paddy soils: rates, relative contributions and influencing factors. Environ Sci Technol 50:9972–9980

  • Sigleo AC (2019) Denitrification rates across a temperate north pacific estuary, Yaquina bay. Oregon Estuaries and Coasts 42:655–664

  • Simon J, Kern M, Hermann B, Einsle O, Butt JN (2011) Physiological function and catalytic versatility of bacterial multihaem cytochromes c involved in nitrogen and sulfur cycling. Biochem Soc Trans 39:1864–1870

  • Smith CJ, Nedwell DB, Dong LF, Osborn AM (2007) Diversity and abundance of nitrate reductase genes (narG and napA), nitrite reductase genes (nirS and nrfA), and their transcripts in estuarine sediments. Appl Environ Microbiol 73:3612–3622

  • 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

  • Song GD, Liu SM, H. low flow seasonant, Kuypers MMM (2013) Anaerobic ammonium oxidation, denitrification and dissimilatory nitrate reduction to ammonium in the East China Sea sediment. Biogeosciences 10:4671–4710

  • Sørensen J, Tiedje J, Firestone R (1980) Inhibition by sulfide of nitric and nitrous oxide reduction by denitrifying Pseudomonas fluorescens. Appl Environ Microbiol 39:105–108

  • Souza VF, Santoro AL, Weerelt MV, Prast AE (2012) Sediment denitrification, DNRA and ANAMMOX rates in tropical floodplain lake (Pantanal, Brazil). Oecol Aust 16:734–744

  • Sponseller RA, Benfield EF, Valett HM (2001) Relationships between land use, spatial scale and stream macroinvertebrate communities. Freshw Biol 46(10):1409–1424

  • Ståhl M, Davidsson TE (2000) The influence of organic carbon on nitrogen transformations in five wetland soils. Soil Sci Soc Am J 64:1129–1136

  • Stainforth DA, Aina T, Christensen C, Collins M, Faull N, Frame DJ, Kettleborough JA, Knight S, Martin A, Murphy JM, Piani C, Sexton D, Smith LA, Spicer RA, Thorpe AJ, Allen MR (2005) Uncertainty in predictions of the climate response to rising levels of greenhouse gases. Nature 433(7024):403–406. https://doi.org/10.1038/nature03301

  • Tan EH, Zou WB, Jiang XL, Wan XH, Hsu TC, Zheng ZZ, Chen L, Xu M, Dai MH, Kao SJ (2019) Organic matter decomposition sustains sedimentary nitrogen loss in the Pearl River Estuary. China Sci Total Environ 648:508–517

  • Throbäck IN, Enwall K, Jarvis Å, Hallin S (2004) Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE. FEMS Microbial Ecol 49:401–417

  • Tiedje JM (1988) Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Zehnder AJB (ed) Biology of Anaerobic Microorganisms. Wiley, New York, pp 179–244

    Google Scholar 

  • Tomasek A, Kozarek JL, Hondzo M, Lurndahl N, Sadowsky MJ, Wang P, Staley C (2017) Environmental drivers of denitrification rates and denitrifying gene abundances in channels and riparian areas. Water Resour Res 53(8):6523–6538. https://doi.org/10.1002/2016wr019566

  • Trimmer M, Nicholls JC (2009) Production of nitrogen gas via anammox and denitrification in intact sediment cores along a continental shelf to slope transect in the North Atlantic. Limnol Oceanogr 54:577–589

  • Tu Q, Lin L, Cheng L, Deng Y, He Z (2019) NCycDB: a curated integrative database for fast and accurate metagenomic profiling of nitrogen cycling genes. Bioinformatics 35(6):1040.1048

  • van de Graaf AA, deBruijn P, Robertson LA, Jetten MSM, Kuenen JG (1996) Autotrophic growth of anaerobic ammoniumoxidizing micro-organisms in a fluidized bed reactor. Microbiology 142(8):2187–2196

  • Wang YF, Gu JD (2014) Effects of allylthiourea, salinity, and pH on ammonia/ammonium-oxidizing prokaryotes in mangrove sediment incubated in laboratory microcosms. Appl Microbiol Biotechnol 98:3257–3274

  • Wang J, Yuan J, Tan X, Li SY, Zhang QF (2015) Stable isotope composition of particulate organic matters and dissolved nitrate in the Jinshui river, upper Han river basin. Acta Ecol Sin 35(22):7338–7346

  • Wang SY, Radny D, Huang SB, Zhuang LJ, Zhao SY, Berg M, Jetten MSM, Zhu GB (2017) Nitrogen loss by anaerobic ammonium oxidation in unconfined aquifer soils. Sci Rep 7:40173

  • Welsh A, Chee-Sanford JC, Connor LM, Loffler FE, Sanford RA (2014) Refined nrfa phylogeny improves PCR-based nrfA gene detection. Appl Environ Microbiol 80(7):2110–2119

  • Wyman M, Hodgson S, Bird C (2013) Denitrifying alphaproteo bacteria from the Arabian sea that express nosZ, the gene encoding nitrous oxide reductase, in oxic and suboxic waters. Appl Environ Microbiol 79(8):2670–2681

  • Xiong ZQ (2018) Vegetation characteristics and soil denitrification of reservoir shorelines and Riparian wetlands in the Han River, China. Wuhan Botanical Garden, Chinese Academy of Science, Wuhan

  • Yang XR, Weng BS, Li H, Marshall CW, Li H, Chen YS, Yu S, Zhu GB, Zhu YG (2017a) An overlooked nitrogen loss linked to anaerobic ammonium oxidation in estuarine sediments in China. J. Soils Sediments 17:2537–2546

  • Yang S, Winkel M, Wagner D, Liebner S (2017b) Community structure of rare methanogenic archaea: insight from a single functional group. FEMS Microbiol Ecol 99(11):126

  • Yin GY, Hou LJ, Zong HB, Ding PX, Liu M, Zhang SF, Cheng XL, Zhou JL (2014a) Denitrification and anaerobic ammonium oxidization across the sediment-water interface in the hypereutrophic ecosystem, Jinpu Bay, in the Northeastern Coast of China. Estuar Coasts 38:211–219

  • Yin GY, Hou LJ, Liu M, Liu ZF, Gardner WS (2014b) A novel membrane inlet mass spectrometer method to measure (NH4+)-N-15 for isotope-enrichment experiments in aquatic ecosystems. Environ Sci Technol 48(16):9555–9562

  • Yin GY, Hou LJ, Liu M, Li XF, Zheng YL, Gao J, Jiang XF, Wang R, Yu CD, Lin XB (2017) DNRA in intertidal sediments of the Yangtze Estuary. J Geophys Res Biogeosci 122:1988–1998

  • Yin XJ, Chen LJ, Tang DQ, Zhang Y, Liu GL, Hua YM, Wan XQ, Zhou WB, Zhao JW, Zhu DW (2019) Seasonal and vertical variations in the characteristics of the nitrogen-related functional genes in sediments from urban eutrophic lakes. Appl Soil Ecol 143:80–88

  • Zhang JY, Dong WJ, Wu LY, Wei JF, Chen PY, Lee DH (2005) Impact of land use changes on surface warming in China. Adv Atmos Sci 22(3):343–348

  • Zhang KR, Dang HS, Tan SD, Wang ZX, Zhang QF (2010) Vegetation community and soil characteristics of abandoned agricultural land and pine plantation in the Qinling mountains, china. Glob Biogeochem Cycles 259(10):2036–2047

  • Zhao BJ, Wang X, Zhang J, Tan X, He R, Zhou Q, Shi H, Zhang QF (2020) Influence factors of potential nitrification rates and functional genes abundance in the Jinshui River and the Qihe River of the Han River basin. Environ Sci 41(12):5419–5427

  • Zheng LZ, Cardenas MB, Wang LC (2016a) Temperature effects on nitrogen cycling and nitrate removal-production efficiency in bed form-induced hyprorheic zones. J Geophys Res Biogeosci 121:1086–1103

  • Zheng YL, Jiang XF, Hou LJ, Liu M, Lin XB, Gao J, Li XF, Yin GY, Yu CD, Wang R (2016b) Shifts in the community structure and activity of anaerobic ammonium oxidation bacteria along an estuarine salinity gradient. J Geophys Res Biogeosci 121:1632–1645

  • Zheng YL, Hou LJ, Liu M, Yin GY (2019) Dynamics and environmental importance of anaerobic ammonium oxidation (anammox) bacteria in urban river networks. Environ Pollut 254

  • Zhuang S, Zhang Y, Zhou J, Chen M, Wang X (2013) Biological removal of nitrate and ammonium under aerobic atmosphere by paracoccus versutus lym. Bioresour Technol 148(Complete):144–148

  • Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61(4):533

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The datasets used and analyzed during the current study are available from the corresponding author on reasonable request.

Funding

This research was supported by the National Natural Science Foundation of China (Nos. 32030069, 31720103905).

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Conceptualization: Binjie Zhao and Quanfa Zhang; Sampling: Binjie Zhao, Xinshuai Li, and Yang Wang; Formal analysis and investigation: Binjie Zhao, Wenhua Qi, and Hongran Li; Writing—original draft preparation: Binjie Zhao, Xinshuai Li, Yang Wang, Xiang Tan, Wenhua Qi, Hongran Li, Junwei Wei, Yong You, and Wenjun Shi; Writing—review and editing: Binjie Zhao and Quanfa Zhang; Funding acquisition: Quanfa Zhang; Supervision: Quanfa Zhang. All authors read and approved the final manuscript.

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Correspondence to Quanfa Zhang.

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Zhao, B., Li, X., Wang, Y. et al. Dissimilatory nitrate reduction and functional genes in two subtropical rivers, China. Environ Sci Pollut Res 28, 68155–68173 (2021). https://doi.org/10.1007/s11356-021-15197-3

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