Nitrate (NO3−) is the second preferred terminal electron acceptor after oxygen (O2), as it plays an essential role as the main electron acceptor for respiration under oxygen-depleted conditions. Dissimilatory nitrate reduction to ammonium (DNRA) is an increasingly important process of microbial-driven nitrate reduction in wetland ecosystems, making it necessary to study the biogeographical distribution and structure of the DNRA community, and to identify the factors governing DNRA in global wetlands.
Materials and methods
We collected samples from 15 wetland sites around the world and used qPCR assay analysis to quantify the DNRA functional gene nrfA. High-throughput sequencing was conducted to analyze the microbial diversity and community structure of DNRA bacteria. The most connected genera were derived from molecular ecological network analysis. Principal coordinates analysis (PCoA), redundancy analysis (RDA), and Pearson’s correlation analysis were used to explore the relationship between microbial structure and environmental factors.
Results and discussion
The environmental conditions of the wetlands varied largely with the latitude. At the phylum level, Proteobacteria was dominant, and Anaerolinea was the key genus. Pearson’s correlation analysis also illustrated that the annual average temperature, as a factor of latitude, most significantly affected DNRA abundance, followed by total organic matter (TOM) and C/N ratio.
For the first time, we summarized the characteristics of DNRA bacteria at the molecular level, along with the influencing factors, in wetlands with a wide biogeographical distribution. This study provides a scientific foundation for the future study of DNRA bacteria in wetlands around the world.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Price excludes VAT (USA)
Tax calculation will be finalised during checkout.
Akunna JC, Bizeau C, Moletta R (1994) Nitrate reduction by anaerobic sludge using glucose at various nitrate concentrations—ammonification, denitrification and methanogenic activities. Environ Technol 15:41–49
Ardon M, Morse JL, Colman BP, Bernhardt ES (2013) Drought-induced saltwater incursion leads to increased wetland nitrogen export. Glob Chang Biol 19:2976–2985
Arrigoni A, Findlay S, Fischer D, Tockner K (2008) Predicting carbon and nutrient transformations in tidal freshwater wetlands of the Hudson River. Ecosystems 11:790–802
Bao S (2000) Soil and agricultural chemistry analysis. China Agriculture Press, Beijing
Barbier EB, Hacker SD, Kennedy C, Koch EW, Stier AC, Silliman BR (2011) The value of estuarine and coastal ecosystem services. Ecol Monogr 81:169–193
Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. International AAAI conference on weblogs and social media, San Jose
Bernhard AE, Dwyer C, Idrizi A, Bender G, Zwick R (2015) Long-term impacts of disturbance on nitrogen-cycling bacteria in a New England salt marsh. Front Microbiol 6:46
Berry D, Widder S (2014) Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front Microbiol 5:219
Burgin AJ, Hamilton SK (2007) Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways. Front Ecol Environ 5:89–96
Canfield DE, Glazer AN, Falkowski PG (2010) The evolution and future of earth’s nitrogen cycle. Science 330:192–196
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336
Chen Y, Korkeala H, Linden J, Lindstrom M (2008) Quantitative real-time reverse transcription-PCR analysis reveals stable and prolonged neurotoxin cluster gene activity in a Clostridium botulinum type E strain at refrigeration temperature. Appl Environ Microbiol 74:6132–6137
Csa’rdi G, Nepusz T (2006) The igraph software package for complex network research. InterJournal Complex Systems 1695(5):1–9
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
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461
Fang YY, Babourina O, Rengel Z, Yang XE, Pu PM (2007) Ammonium and nitrate uptake by the floating plant Landoltia punctata. Ann Bot 99:365–370
Faulwetter JL, Gagnon V, Sundberg C, Chazarenc F, Burr MD, Brisson J, Camper AK, Stein OR (2009) Microbial processes influencing performance of treatment wetlands: a review. Ecol Eng 35:987–1004
Faust K, Raes J (2012) Microbial interactions: from networks to models. Nat Rev Microbiol 10:538–550
Fernandes SO, Javanaud C, Michotey VD, Guasco S, Anschutz P, Bonin P (2016) Coupling of bacterial nitrification with denitrification and anammox supports N removal in intertidal sediments (Arcachon Bay, France). Estuar Coast Shelf Sci 179:39–50
Fitzhugh RD, Lovett GM, Venterea RT (2003) Biotic and abiotic immobilization of ammonium, nitrite, and nitrate in soils developed under different tree species in the Catskill Mountains, New York, USA. Glob Chang Biol 9:1591–1601
Greaver TL, Clark CM, Compton JE, Vallano D, Talhelm AF, Weaver CP, Band LE, Baron JS, Davidson EA, Tague CL, Felker-Quinn E, Lynch JA, Herrick JD, Liu L, Goodale CL, Novak KJ, Haeuber RA (2016) Key ecological responses to nitrogen are altered by climate change. Nat Clim Chang 6:836–843
Hardison AK, Algar CK, Giblin AE, Rich JJ (2015) Influence of organic carbon and nitrate loading on partitioning between dissimilatory nitrate reduction to ammonium (DNRA) and N-2 production. Geochim Cosmochim Acta 164:146–160
Huygens D, Ruetting T, Boeckx P, Van Cleemput O, Godoy R, Mueller C (2007) Soil nitrogen conservation mechanisms in a pristine south Chilean Nothofagus forest ecosystem. Soil Biol Biochem 39:2448–2458
Jetten MSM (2008) The microbial nitrogen cycle. Environ Microbiol 10:2903–2909
Kleinhuizen AA, Mortazavi B (2018) Denitrification capacity of a natural and a restored marsh in the Northern Gulf of Mexico. Environ Manag 62:584–594
Kuypers MMM, Lavik G, Woebken D, Schmid M, Fuchs BM, Amann R, Jorgensen BB, Jetten MSM (2005) Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc Natl Acad Sci U S A 102:6478–6483
Laima MJC, Girard MF, Vouve F, Blanchard GF, Gouleau D, Galois R, Richard P (1999) Distribution of adsorbed ammonium pools in two intertidal sedimentary structures, Marennes-Oleron Bay, France. Mar Ecol Prog Ser 182:29–35
Larsson MA, Baken S, Gustafsson JP, Hadialhejazi G, Smolders E (2013) Vanadium bioavailability and toxicity to soil microorganisms and plants. Environ Toxicol Chem 32:2266–2273
Lu WW, Riya S, Zhou S, Hosomi M, Zhang HL, Shi WM (2012) In situ dissimilatory nitrate reduction to ammonium in a paddy soil fertilized with liquid cattle waste. Pedosphere 22:314–321
Magoc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963
Martiny JBH, Eisen JA, Penn K, Allison SD, Horner-Devine MC (2011) Drivers of bacterial beta-diversity depend on spatial scale. Proc Natl Acad Sci U S A 108:7850–7854
Mohan SB, Schmid M, Jetten M, Cole J (2004) Detection and widespread distribution of the nrfA gene encoding nitrite reduction to ammonia, a short circuit in the biological nitrogen cycle that competes with denitrification. FEMS Microbiol Ecol 49:433–443
Oksanen J, Kindt R, Legendre P, O’ Hara B, Simpson G, Solymos P (2007) Vegan: community ecology package. R package version:8
Osborne RI, Bernot MJ, Findlay SEG (2015) Changes in nitrogen cycling processes along a salinity gradient in tidal wetlands of the Hudson River, New York, USA. Wetlands 35:323–334
Palacin-Lizarbe C, Camarero L, Hallin S, Jones CM, Caliz J, Casamayor EO, Catalan J (2019) The DNRA-denitrification dichotomy differentiates nitrogen transformation pathways in mountain lake benthic habitats. Front Microbiol 10:1229
Power ME, Tilman D, Estes JA, Menge BA, Bond WJ, Mills LS, Daily G, Castilla JC, Lubchenco J, Paine RT (1996) Challenges in the quest for keystones. Bioscience 46:609–620
Rehr B, Klemme JH (1989) Competition for nitrate between denitrifying pseudomonas-stutzeri and nitrate ammonifying enterobacteria. FEMS Microbiol Ecol 62:51–58
Riley WJ, Ortiz-Monasterio I, Matson PA (2001) Nitrogen leaching and soil nitrate, nitrite, and ammonium levels under irrigated wheat in Northern Mexico. Nutr Cycl Agroecosyst 61:223–236
Robertson EK, Roberts KL, Burdorf LDW, Cook P, Thamdrup B (2016) Dissimilatory nitrate reduction to ammonium coupled to Fe(II) oxidation in sediments of a periodically hypoxic estuary. Limnol Oceanogr 61:365–381
Ruamps LS, Nunan N, Chenu C (2011) Microbial biogeography at the soil pore scale. Soil Biol Biochem 43:280–286
Rutting T, Clough TJ, Muller C, Lieffering M, Newton PCD (2010) Ten years of elevated atmospheric carbon dioxide alters soil nitrogen transformations in a sheep-grazed pasture. Glob Chang Biol 16:2530–2542
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541
Sen IS, Peucker-Ehrenbrink B (2012) Anthropogenic disturbance of element cycles at the earth’s surface. Environ Sci Technol 46:8601–8609
Silver WL, Herman DJ, Firestone MK (2001) Dissimilatory nitrate reduction to ammonium in upland tropical forest soils. Ecology 82:2410–2416
Song B, Lisa JA, Tobias CR (2014) Linking DNRA community structure and activity in a shallow lagoonal estuarine system. Front Microbiol 5:460
Tiedje JM, Sexstone AJ, Myrold DD, Robinson JA (1982) Denitrification—ecological niches, competition and survival. Antonie Van Leeuwenhoek 48:569–583
Tylova-Munzarova E, Lorenzen B, Brix H, Votrubova O (2005) The effects of NH4+ and NO3- on growth, resource allocation and nitrogen uptake kinetics of Phragmites australis and Glyceria maxima. Aquat Bot 81:326–342
Wang Q, Quensen JF, Fish JA, Lee TK, Sun YN, Tiedje JM, Cole JR (2013) Ecological patterns of nifH genes in four terrestrial climatic zones explored with targeted metagenomics using FrameBot, a new informatics tool. Mbio 4:e00592–e00513
Welsh JP, Wood GA, Godwin RJ, Taylor JC, Earl R, Blackmore S, Knight SM (2003) Developing strategies for spatially variable nitrogen application in cereals, part II: wheat. Biosyst Eng 84:495–511
Welsh A, Chee-Sanford JC, Connor LM, Loffler FE, Sanford RA (2014) Refined nrfA phylogeny improves PCR-based nrfA gene detection. Appl Environ Microbiol 80:2110–2119
Woods DD (1938) The reduction of nitrate to ammonia by Clostridium welchii. Biochem J 32:2000–2012
Zaehle S, Friend AD, Friedlingstein P, Dentener F, Peylin P, Schulz M (2010) Carbon and nitrogen cycle dynamics in the O-CN land surface model: 2. Role of the nitrogen cycle in the historical terrestrial carbon balance. Glob Biogeochem Cycles 24:GB1005
Zhou MH, Butterbach-Bahl K, Vereecken H, Bruggemann N (2017) A meta-analysis of soil salinization effects on nitrogen pools, cycles and fluxes in coastal ecosystems. Glob Chang Biol 23:1338–1352
The author Guibing Zhu gratefully acknowledges the support of a Humboldt Research Fellowship (1152633) and Program of the Youth Innovation Promotion Association (CAS).
This research is financially supported by the National Natural Science Foundation of China (No.41671471, 41322012, and 21707155), China Postdoctoral Science Foundation (2017M620931), Strategic Priority Research Program of the Chinese Academy of Sciences (XDB15020303), National Key R&D Program (2016YFA0602303), Local Innovative and Research Teams Project of Guangdong Pearl River Talents Program (2017BT01Z176), and special fund from the State Key Joint Laboratory of Environment Simulation and Pollution Control.
Conflict of interest
The authors declare that they have no conflicts of interest.
This article does not contain any studies with human participants or animals performed by any of the authors.
Responsible editor: Terrence H. Bell
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Pan, H., Yuan, D., Liu, W. et al. Biogeographical distribution of dissimilatory nitrate reduction to ammonium (DNRA) bacteria in wetland ecosystems around the world. J Soils Sediments 20, 3769–3778 (2020). https://doi.org/10.1007/s11368-020-02707-y
- Biogeographical distribution
- High-throughput sequencing
- Wetland ecosystems