Abstract
Enhancement of dissimilatory nitrate/nitrite reduction to ammonium (DNRA) in agricultural soils has recently gained attention as a means to decelerate nitrogen loss. Here, the potential effects of plant root exudates on the DNRA activity of a model organism Shewanella loihica and agricultural soil consortia were examined. The chemical composition of the root exudate collected from Arabidopsis thaliana (Col-0) plant was analyzed by gas chromatography time-of-flight mass spectrometry (GC TOF-MS) and applied to S. loihica cultures grown on lactate and \({\text{NO}}_{3}^{{^{ - } }}\) to examine the effects on the \({\text{NO}}_{3}^{{^{ - } }}\) fate. Additionally, artificial root exudate was synthesized consisting of the major root exudate constituents, and its impacts on denitrification vs. DNRA competition in agricultural soil extracts, as well as S. loihica cultures, were investigated. Incubation of S. loihica in media amended with A. thaliana root exudates or artificial root exudates both resulted in a significant enhancement of DNRA activity. The agricultural soil consortia amended with root exudates did not exhibit significant DNRA enhancement; however, artificial root exudates addition had significant DNRA enhancement effect, which was confirmed with \(^{{{15}}} {\text{NH}}_{4}^{ + }\) production from added \(^{{{15}}} {\text{NO}}_{3}^{{^{ - } }}\). The findings of this study suggest that plants’ root exudates may have stimulatory impact on the environmentally beneficial DNRA pathway.
Both authors contributed equally to this work.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
References
Ahmad E, Sharma PK, Khan MS, (2021) Roles of root exudates in different processes in the nitrogen cycle in the Rhizosphere. In: Cruz C, Vishwakarma K, Choudhary DK, Varma A (eds) Soil nitrogen ecology. Springer International Publishing, Cham, pp 179–200. https://doi.org/10.1007/978-3-030-71206-8_8
Andresen L C, Bode S, Tietema A, Boeckx P, Rütting T (2015) Amino acid and N mineralization dynamics in heathland soil after long-term warming and repetitive drought. Soil 1, 341–349.https://doi.org/10.5194/soil-1-341-2015
Barnard R, Leadley PW, Hungate BA (2005) Global change, nitrification, and denitrification: a review. Global Biogeochem. Cycles 19. https://doi.org/10.1029/2004GB002282
Bateman EJ, Baggs EM (2005) Contributions of nitrification and denitrification to N2O emissions from soils at different water-filled pore space. Biol Fertil Soils 41:379–388. https://doi.org/10.1007/s00374-005-0858-3
Beeckman F, Motte H, Beeckman T (2018) Nitrification in agricultural soils: impact, actors and mitigation. Curr Opin Biotechnol 50, 166–173. https://doi.org/10.1016/j.copbio.2018.01.014
Bremer C, Braker G, Matthies D, Reuter A, Engels C, Conrad R (2007) Impact of plant functional group, plant species, and sampling time on the composition of nirK-typt denitrifier communities in soil. Appl Environ Microbiol 73:6876–6884. https://doi.org/10.1128/AEM.01536-07
Bulgarelli D, Rott M, Schlaeppi K, van Themaat E, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E, Peplies J, Gloeckner FO, Amann R, Eickhorst T, Schulze-Lefert P (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95. https://doi.org/10.1038/nature11336
Bürgmann 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
Chaparro JM, Badri DV, Bakker MG, Sugiyama A, Manter DK, Vivanco JM (2013) Root exudation of phytochemicals in Arabidopsis follows specific patterns that are developmentally programmed and correlate with soil microbial functions. Plos One 8.https://doi.org/10.1371/journal.pone.0055731
Cheng Y, Wang J, Wang J, Chang SX, Wang S (2017) The quality and quantity of exogenous organic carbon input control microbial NO3− immobilization: A meta-analysis. Soil Biol Biochem 115, 357–363. https://doi.org/10.1016/j.soilbio.2017.09.006
Coskun D, Britto DT, Shi W, Kronzucker HJ (2017) How plant root exudates shape the nitrogen cycle. Trends Plant Sci 22:661–673. https://doi.org/10.1016/j.tplants.2017.05.004
Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47. https://doi.org/10.1023/A:1020809400075
Dimkpa C, Weinand T, Asch F (2009) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32:1682–1694. https://doi.org/10.1111/j.1365-3040.2009.02028.x
Fisk LM, Barton L, Jones DL, Glanville HC, Murphy DV (2015) Root exudate carbon mitigates nitrogen loss in a semi-arid soil. Soil Biol Biochem 88:380–389. https://doi.org/10.1016/j.soilbio.2015.06.011
Giles M, Morley N, Baggs EM, Daniell TJ (2012) Soil nitrate reducing processes—drivers, mechanisms for spatial variation, and significance for nitrous oxide production. Front Microbiol 3.https://doi.org/10.3389/fmicb.2012.00407
Haichar FEZ, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, Heulin T, Achouak W (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230. https://doi.org/10.1038/ismej.2008.80
Hamonts K, Clough TJ, Stewart A, Clinton PW, Richardson AE, Wakelin SA, O’Callaghan M, Condron LM (2013) Effect of nitrogen and waterlogging on denitrifier gene abundance, community structure and activity in the rhizosphere of wheat. FEMS Microbiol Ecol 83:568–584. https://doi.org/10.1111/1574-6941.12015
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 N2 production. Geochim Cosmochim Acta 164, 146–160. https://doi.org/10.1016/j.gca.2015.04.049
Henry A, Doucette W, Norton J, Bugbee B (2007) Changes in crested wheatgrass root exudation caused by flood, drought, and nutrient stress. J Environ Qual 36:904–912. https://doi.org/10.2134/jeq2006.0425sc
Henry S, Texier S, Hallet S, Bru D, Dambreville C, Chèneby D, Bizouard F, Germon JC, Philippot L (2008) Disentangling the rhizosphere effect on nitrate reducers and denitrifiers: insight into the role of root exudates. Environ Microbiol 10:3082–3092. https://doi.org/10.1111/j.1462-2920.2008.01599.x
Hinsinger P, Gobran GR, Gregory PJ, Wenzel WW (2005) Rhizosphere geometry and heterogeneity arising from root-mediated physical and chemical processes. New Phytol 168:293–303. https://doi.org/10.1111/j.1469-8137.2005.01512.x
Kim H, Park D, Yoon S (2017) pH Control Enables Simultaneous Enhancement of Nitrogen Retention and N2O Reduction in Shewanella loihica Strain PV-4. Front Microbiol 8:1820. https://doi.org/10.3389/fmicb.2017.01820
Li B, Li Y-Y, Wu H-M, Zhang F-F, Li C-J, Li X-X, Lambers H, Li L (2016) Root exudates drive interspecific facilitation by enhancing nodulation and N2 fixation. Proc Natl Acad Sci 113:6496–6501. https://doi.org/10.1073/pnas.1523580113
Matilla MA, Ramos JL, Bakker PAHM, Doornbos R, Badri DV, Vivanco JM, Ramos-González MI (2010) Pseudomonas putida KT2440 causes induced systemic resistance and changes in Arabidopsis root exudation. Environ Microbiol Rep 2:381–388. https://doi.org/10.1111/j.1758-2229.2009.00091.x
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Naher U, Othman R, Shamsuddin ZHJ, Mohd Saud H, Ismail MR, Rahim K (2011) Effect of root exuded specific sugars on biological nitrogen fixation and growth promotion in rice (Oryza sativa). Aust J Crop Sci 5:1210–1217
Narula N, Kothe E, Behl R (2009) Role of root exudates in plant-microbe interactions. J Appl Bot Food Qual 82:122–130
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, 2715–2724. https://doi.org/10.1016/j.watres.2010.02.002
Pajares S, Bohannan BJM (2016) Ecology of nitrogen fixing, nitrifying, and denitrifying microorganisms in tropical forest soils. Front Microbiol 7:1045. https://doi.org/10.3389/fmicb.2016.01045
Pariasca Tanaka J, Nardi P, Wissuwa M (2010) Nitrification inhibition activity, a novel trait in root exudates of rice. AoB Plants 2010, plq014–plq014. https://doi.org/10.1093/aobpla/plq014
Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789
Rütting T, Boeckx P, Müller C, Klemedtsson L (2011) Assessment of the importance of dissimilatory nitrate reduction to ammonium for the terrestrial nitrogen cycle. Biogeosciences 8.https://doi.org/10.5194/bg-8-1779-2011
Silver WL, Herman DJ, Firestone MK (2001) Dissimilatory nitrate reduction to ammonium in upland tropical forest soils. Ecology 82:2410–2416. https://doi.org/10.1890/0012-9658(2001)082[2410:DNRTAI]2.0.CO;2
ŠImek M, Cooper JE (2002) The influence of soil pH on denitrification: progress towards the understanding of this interaction over the last 50 years. Eur J Soil Sci 53, 345–354. https://doi.org/10.1046/j.1365-2389.2002.00461.x
Ståhl M (2000) The Influence of Organic Carbon on Nitrogen Transformation in Five Wetland Soil. Soil Sci Soc Am J SSSAJ 64. https://doi.org/10.2136/sssaj2000.6431129x
Stevens RJ, Laughlin RJ, Malone JP (1998) Soil pH affects the processes reducing nitrate to nitrous oxide and di-nitrogen. Soil Biol Biochem 30, 1119–1126. https://doi.org/10.1016/S0038-0717(97)00227-7
Strehmel N, Böttcher C, Schmidt S, Scheel D (2014) Profiling of secondary metabolites in root exudates of Arabidopsis thaliana. Phytochemistry 108, 35–46. https://doi.org/10.1016/j.phytochem.2014.10.003
Strohm TO, Griffin B, Zumft WG, Schink B (2007) Growth yields in bacterial denitrification and nitrate ammonification. Appl Environ Microbiol 73:1420–1424. https://doi.org/10.1128/AEM.02508-06
Subbarao GV, Yoshihashi T, Worthington M, Nakahara K, Ando Y, Sahrawat KL, Rao IM, Lata J-C, Kishii M, Braun H-J (2015) Suppression of soil nitrification by plants. Plant Sci 233, 155–164. https://doi.org/10.1016/j.plantsci.2015.01.012
Sun L, Lu Y, Yu F, Kronzucker HJ, Shi W (2016) Biological nitrification inhibition by rice root exudates and its relationship with nitrogen-use efficiency. New Phytol 212, 646–656. https://doi.org/10.1111/nph.14057
van den Berg EM, Boleij M, Kuenen JG, Kleerebezem R, van Loosdrecht MCM (2016) DNRA and denitrification coexist over a broad range of acetate/N-NO3- ratios, in a chemostat enrichment culture. Front Microbiol 7.https://doi.org/10.3389/fmicb.2016.01842
Vuono D, Read R, Hemp J, Sullivan B, Arnone J, Neveux I, Blank R, Loney E, Miceli D, Winkler M-K, Chakraborty R, Stahl D, Grzymski J (2019) Resource concentration modulates the fate of dissimilated nitrogen in a dual-pathway actinobacterium. Front Microbiol 10. https://doi.org/10.3389/fmicb.2019.00003
Walker TS, Bais HP, Halligan KM, Stermitz FR, Vivanco JM (2003) Metabolic profiling of root exudates of Arabidopsis thaliana. J Agric Food Chem 51:2548–2554. https://doi.org/10.1021/jf021166h
Wolin EA, Wolfe RS, Wolin MJ (1964) Viologen dye inhibition of methane formation by Methanobacillus omelianskii. J Bacteriol 87:993–998
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
Xuan TD, Chung IIIM, Khanh TD, Tawata S (2006) Identification of phytotoxic substances from early growth of barnyard grass (Echinochloa crusgalli) root exudates. J Chem Ecol 32:895. https://doi.org/10.1007/s10886-006-9035-x
Yi C, Park S, Yun HS, Kwon C (2013) Vesicle-associated membrane proteins 721 and 722 are required for unimpeded growth of Arabidopsis under ABA application. J Plant Physiol 170, 529–533. https://doi.org/10.1016/j.jplph.2012.11.001
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
Yoon S, Cruz-García C, Sanford R, Ritalahti KM, Löffler FE (2015a) Denitrification versus respiratory ammonification: environmental controls of two competing dissimilatory NO3-/NO2-reduction pathways in Shewanella loihica strain PV-4. ISME J 9:1093–1104. https://doi.org/10.1038/ismej.2014.201
Yoon S, Sanford RA, Löffler FE (2015b) Nitrite control over dissimilatory nitrate/nitrite reduction pathways in Shewanella loihica strain PV-4. Appl Environ Microbiol 81:3510–3517. https://doi.org/10.1128/AEM.00688-15
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, Lan T, Müller C, Cai Z (2014) Dissimilatory nitrate reduction to ammonium (DNRA) plays an important role in soil nitrogen conservation in neutral and alkaline but not acidic rice soil. J Soils Sediments 15:523–531. https://doi.org/10.1007/s11368-014-1037-7
Acknowledgements
This research was financially supported by the National Research Foundation of Korea (NRF) (Grant no. 2015M3D3A1A01064881). The authors were also financially supported by the Brain Korea 21 Plus Project (Grant no. 21A20132000003). Authors would like to also acknowledge Dr. Sukhwan Yoon at KAIST, South Korea, and Dr. Chian Kwon and Da Jeong Cho at Dankook University, South Korea, for providing support in various forms for this study.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2022 The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
Biswal, B.K., Chang, J. (2022). Impact of Arabidopsis thaliana Root Exudates on Dissimilatory Nitrate Reduction to Ammonium (DNRA) Activities in Shewanella loihica PV-4 and Agricultural Soil Enrichments. In: Kumar, M., Mohapatra, S. (eds) Impact of COVID-19 on Emerging Contaminants. Springer Transactions in Civil and Environmental Engineering. Springer, Singapore. https://doi.org/10.1007/978-981-19-1847-6_9
Download citation
DOI: https://doi.org/10.1007/978-981-19-1847-6_9
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-19-1846-9
Online ISBN: 978-981-19-1847-6
eBook Packages: Earth and Environmental ScienceEarth and Environmental Science (R0)