Abstract
Graphene nanofertilizers have demonstrated immense potential in improving agricultural productivity and nitrogen management. However, how those nanomaterials interact with soil microbial communities related to N cycle remain unclear. The present study assessed the impact of four different graphitic nanomaterials (i.e., GO, graphene oxide; rGO, reduced graphene oxide; GNP, graphene nanoplatelet; GNA, graphite nanoadditive) and biochar at two different doses (5 and 1000 mg kg−1 soil) on soil respiration, nitrification potential, and microbial N cycling functional genes over 28 days of incubation of sandy agricultural soil. Basal respiration indicated a transient increase of microbial activity with all treatments, while substrate induced respiration (SIR) revealed an enhancement of microbial respiration rate with some treatments that sustained at the end of the incubation. No significant differences in the maximum nitrification potential were observed when treated with GNMs or biochar. However, decreased abundances of amoA genes and increased abundance of denitrifying genes (nirK, nirS, nosZ) in all treated soils suggested a decreased potential for nitrification and boosted denitrification after 28-day exposure. In addition, GNMs showed minimum impact on nifH population in this incubation study. Together, the results suggest that graphitic nanomaterials might suppress nitrification and potentially reduce losses by nitrate leaching in agricultural soils.
Graphical abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Azad N, Behmanesh J, Rezaverdinejad V, Abbasi F, Navabian M (2020) An analysis of optimal fertigation implications in different soils on reducing environmental impacts of agricultural nitrate leaching. Sci Rep 10(1):1–5. https://doi.org/10.1038/s41598-020-64856-x
Azziz G, Monza J, Etchebehere C, Irisarri P (2017) nirS-and nirK-type denitrifier communities are differentially affected by soil type, rice cultivar and water management. Eur J Soil Biol 78:20–28. https://doi.org/10.1016/j.ejsobi.2016.11.003
Banach-Wiśniewska A, Tomaszewski M, Hellal MS, Ziembińska-Buczyńska A (2021) Effect of biomass immobilization and reduced graphene oxide on the microbial community changes and nitrogen removal at low temperatures. Sci Rep 11(1):1–12. https://doi.org/10.1038/s41598-020-80747-7
Bárta J, Melichová T, Vaněk D, Picek T, Šantrůčková H (2010) Effect of pH and dissolved organic matter on the abundance of nirK and nirS denitrifiers in spruce forest soil. Biogeochemistry 101(1):123–132. https://doi.org/10.1007/s10533-010-9430-9
Bianco A, Cheng HM, Enoki T, Gogotsi Y, Hurt RH, Koratkar N, Kyotani T, Monthioux M, Park CR, Tascon JM, Zhang J (2013) All in the graphene family–A recommended nomenclature for two-dimensional carbon materials. Carbon 65:1–6. https://doi.org/10.1016/j.carbon.2013.08.038
Blagodatskaya E, Yuyukina T, Blagodatsky S, Kuzyakov Y (2011) Three-source-partitioning of microbial biomass and of CO2 efflux from soil to evaluate mechanisms of priming effects. Soil Biol Biochem 43(4):778–786. https://doi.org/10.1016/j.soilbio.2010.12.011
Carniel FC, Fortuna L, Nepi M, Cai G, Del Casino C, Adami G, Bramini M, Bosi S, Flahaut E, Martín C, Vázquez E (2020) Beyond graphene oxide acidity: Novel insights into graphene related materials effects on the sexual reproduction of seed plants. J Hazard Mater 393:122380. https://doi.org/10.1016/j.jhazmat.2020.122380
Carpio IE, Santos CM, Wei X, Rodrigues DF (2012) Toxicity of a polymer–graphene oxide composite against bacterial planktonic cells, biofilms, and mammalian cells. Nanoscale 4(15):4746–4756. https://doi.org/10.1039/c2nr30774j
Chen Q, Wang H, Yang B, He F, Han X, Song Z (2015) Responses of soil ammonia-oxidizing microorganisms to repeated exposure of single-walled and multi-walled carbon nanotubes. Sci Total Environ 505:649–657. https://doi.org/10.1016/j.scitotenv.2014.10.044
Chen D, Wang X, Yang K, Wang H (2016) Response of a three dimensional bioelectrochemical denitrification system to the long-term presence of graphene oxide. Biores Technol 214:24–29. https://doi.org/10.1016/j.biortech.2016.04.082
Chen S, Yang M, Ba C, Yu S, Jiang Y, Zou H, Zhang Y (2018) Preparation and characterization of slow-release fertilizer encapsulated by biochar-based waterborne copolymers. Sci Total Environ 615:431–437. https://doi.org/10.1016/j.scitotenv.2017.09.209
Chung H, Kim MJ, Ko K, Kim JH, Kwon HA, Hong I, Park N, Lee SW, Kim W (2015) Effects of graphene oxides on soil enzyme activity and microbial biomass. Sci Total Environ 514:307–313. https://doi.org/10.1016/j.scitotenv.2015.01.077
Clark CM, Bell MD, Boyd JW, Compton JE, Davidson EA, Davis C, Fenn ME, Geiser L, Jones L, Blett TF (2017) Nitrogen-induced terrestrial eutrophication: cascading effects and impacts on ecosystem services. Ecosphere 8(7):e01877. https://doi.org/10.1002/ecs2.1877
Cui P, Fan F, Yin C, Song A, Huang P, Tang Y, Zhu P, Peng C, Li T, Wakelin SA, Liang Y (2016) Long-term organic and inorganic fertilization alters temperature sensitivity of potential N2O emissions and associated microbes. Soil Biol Biochem 93:131–141. https://doi.org/10.1016/j.soilbio.2015.11.005
Ducey TF, Ippolito JA, Cantrell KB, Novak JM, Lentz RD (2013) Addition of activated switchgrass biochar to an aridic subsoil increases microbial nitrogen cycling gene abundances. Appl Soil Ecol 65:65–72. https://doi.org/10.1016/j.apsoil.2013.01.006
Fan F, Yang Q, Li Z, Wei D, Cui XA, Liang Y (2011) Impacts of organic and inorganic fertilizers on nitrification in a cold climate soil are linked to the bacterial ammonia oxidizer community. Microb Ecol 62(4):982–990. https://doi.org/10.1007/s00248-011-9897-5
Forstner C, Orton TG, Skarshewski A, Wang P, Kopittke PM, Dennis PG (2019) Effects of graphene oxide and graphite on soil bacterial and fungal diversity. Sci Total Environ 671:140–148. https://doi.org/10.1016/j.scitotenv.2019.03.360
Ge Y, Schimel JP, Holden PA (2011) Evidence for negative effects of TiO2 and ZnO nanoparticles on soil bacterial communities. Environ Sci Technol 45(4):1659–1664. https://doi.org/10.1021/es103040t
Ge Y, Priester JH, Mortimer M, Chang CH, Ji Z, Schimel JP, Holden PA (2016) Long-term effects of multiwalled carbon nanotubes and graphene on microbial communities in dry soil. Environ Sci Technol 50(7):3965–3974. https://doi.org/10.1021/acs.est.5b05620
Ge Y, Shen C, Wang Y, Sun YQ, Schimel JP, Gardea-Torresdey JL, Holden PA (2018) Carbonaceous nanomaterials have higher effects on soybean rhizosphere prokaryotic communities during the reproductive growth phase than during vegetative growth. Environ Sci Technol 52(11):6636–6646. https://doi.org/10.1021/acs.est.8b00937
Gogos A, Knauer K, Bucheli TD (2012) Nanomaterials in plant protection and fertilization: current state, foreseen applications, and research priorities. J Agric Food Chem 60(39):9781–9792. https://doi.org/10.1021/jf302154y
Guo GX, Deng H, Qiao M, Yao HY, Zhu YG (2013) Effect of long-term wastewater irrigation on potential denitrification and denitrifying communities in soils at the watershed scale. Environ Sci Technol 47(7):3105–3113. https://doi.org/10.1021/es304714a
Hagemann N, Harter J, Kaldamukova R, Guzman-Bustamante I, Ruser R, Graeff S, Kappler A, Behrens S (2017) Does soil aging affect the N2O mitigation potential of biochar? A combined microcosm and field study. GCB Bioenergy 9(5):953–964. https://doi.org/10.1111/gcbb.12390
Hallin S, Lindgren PE (1999) PCR detection of genes encoding nitrite reductase in denitrifying bacteria. Appl Environ Microbiol 65(4):1652–1657. https://doi.org/10.1007/BF01644071
Hao Y, Ma C, Zhang Z, Song Y, Cao W, Guo J, Zhou G, Rui Y, Liu L, Xing B (2018) Carbon nanomaterials alter plant physiology and soil bacterial community composition in a rice-soil-bacterial ecosystem. Environ Pollut 232:123–136. https://doi.org/10.1016/j.envpol.2017.09.024
Hart SC, Stark JM, Davidson EA, Firestone MK (1994) Nitrogen mineralization, immobilization, and nitrification. In: Weaver RW, Angle S, Bottomley P, Bezdicek D, Smith S, Ali (ed). Methods of Soil Analysis: Part 2 Microbiological and Biochemical Properties. SSSA, pp 985–1018. https://doi.org/10.2136/sssabookser5.2.c42
He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, Xu MG, Di H (2007) Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ Microbiol 9(9):2364–2374. https://doi.org/10.1111/j.1462-2920.2007.01358.x
He F, Wang H, Chen Q, Yang B, Gao Y, Wang L (2015) Short-term response of soil enzyme activity and soil respiration to repeated carbon nanotubes exposure. Soil Sediment Contam 24(3):250–261. https://doi.org/10.1080/15320383.2015.948611
He L, Liu Y, Zhao J, Bi Y, Zhao X, Wang S, Xing G (2016) Comparison of straw-biochar-mediated changes in nitrification and ammonia oxidizers in agricultural oxisols and cambosols. Biol Fertil Soils 52(2):137–149. https://doi.org/10.1007/s00374-015-1059-3
Hendershot WH, Lalande H, Duquette M (1993) Soil reaction and exchangeable acidity. In: Gregorich EG (ed) Carter MR. Soil sampling and methods of analysis, CRC Press, pp 173–178
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(8):5181–5189. https://doi.org/10.1128/AEM.00231-06
Herold MB, Giles ME, Alexander CJ, Baggs EM, Daniell TJ (2018) Variable response of nirK and nirS containing denitrifier communities to long-term pH manipulation and cultivation. FEMS Microbiol Lett 365(7):1–6. https://doi.org/10.1093/femsle/fny035
Hofmann T, Lowry GV, Ghoshal S, Tufenkji N, Brambilla D, Dutcher JR, Gilbertson LM, Giraldo JP, Kinsella JM, Landry MP, Lovell W (2020) Technology readiness and overcoming barriers to sustainably implement nanotechnology-enabled plant agriculture. Nature Food 1(7):416–425. https://doi.org/10.1038/s43016-020-0110-1
Honer K, Kalfaoglu E, Pico C, McCann J, Baltrusaitis J (2017) Mechanosynthesis of magnesium and calcium salt–urea ionic cocrystal fertilizer materials for improved nitrogen management. ACS Sustain Chem Eng 5(10):8546–8550. https://doi.org/10.1021/acssuschemeng.7b02621
Hou S, Ai C, Zhou W, Liang G, He P (2018) Structure and assembly cues for rhizospheric nirK-and nirS-type denitrifier communities in long-term fertilized soils. Soil Biol Biochem 119(12):32–40. https://doi.org/10.1016/j.soilbio.2018.01.007
Jian LI, Yangde Z, Zhiming Z (2008) Study on application of nanometer biotechnology on the yield and quality of winter wheat. J Anhui Agric Sci 36:15578–15580
Jin L, Son Y, Yoon TK, Kang YJ, Kim W, Chung H (2013) High concentrations of single-walled carbon nanotubes lower soil enzyme activity and microbial biomass. Ecotoxicol Environ Saf 88:9–15. https://doi.org/10.1016/j.ecoenv.2012.10.031
Jin L, Son Y, DeForest JL, Kang YJ, Kim W, Chung H (2014) Single-walled carbon nanotubes alter soil microbial community composition. Sci Total Environ 466–467:533–538. https://doi.org/10.1016/j.scitotenv.2013.07.035
Jones CM, Hallin S (2010) Ecological and evolutionary factors underlying global and local assembly of denitrifier communities. ISME J 4(5):633–641. https://doi.org/10.1038/ismej.2009.152
Joseph S, Graber ER, Chia C, Munroe P, Donne S, Thomas T, Nielsen S, Marjo C, Rutlidge H, Pan GX, Li L (2013) Shifting paradigms: development of high-efficiency biochar fertilizers based on nano-structures and soluble components. Carbon Manag 4(3):323–343. https://doi.org/10.4155/cmt.13.23
Kabiri S, Degryse F, Tran DN, da Silva RC, McLaughlin MJ, Losic D (2017) Graphene oxide: a new carrier for slow release of plant micronutrients. ACS Appl Mater Interfaces 9(49):43325–43335. https://doi.org/10.1021/acsami.7b07890
Kah M, Kookana RS, Gogos A, Bucheli TD (2018) A critical evaluation of nanopesticides and nanofertilizers against their conventional analogues. Nat Nanotechnol 13(8):677–684. https://doi.org/10.1038/s41565-018-0131-1
Kalus K, Koziel JA, Opaliński S (2019) A review of biochar properties and their utilization in crop agriculture and livestock production. Appl Sci (switzerland) 9(17):3494. https://doi.org/10.3390/app9173494
Kumar A, Dixit CK (2017) Methods for characterization of nanoparticles. In: Nimesh S, Chandra R, Gupta N (ed). Advances in nanomedicine for the delivery of therapeutic nucleic acids, Woodhead Publishing 43–58. https://doi.org/10.1016/B978-0-08-100557-6.00003-1
Kuzyakov Y (2006) Sources of CO2 efflux from soil and review of partitioning methods. Soil Biol Biochem 38(3):425–448. https://doi.org/10.1016/j.soilbio.2005.08.020
Kuzyakov Y (2010) Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42(9):1363–1371. https://doi.org/10.1016/j.soilbio.2010.04.003
Lahiani MH, Dervishi E, Ivanov I, Chen J, Khodakovskaya M (2016) Comparative study of plant responses to carbon-based nanomaterials with different morphologies. Nanotechnology 27(26):265102. https://doi.org/10.1088/0957-4484/27/26/265102
Lan Z, Chen C, Rezaei Rashti M, Yang H, Zhang D (2018) High pyrolysis temperature biochars reduce nitrogen availability and nitrous oxide emissions from an acid soil. GCB Bioenergy 10(12):930–945. https://doi.org/10.1111/gcbb.12529
Lan ZM, Chen CR, Rashti MR, Yang H, Zhang DK (2019) Linking feedstock and application rate of biochars to N2O emission in a sandy loam soil: Potential mechanisms. Geoderma 337:880–892. https://doi.org/10.1016/j.geoderma.2018.11.007
Levy-Booth DJ, Prescott CE, Grayston SJ (2014) Microbial functional genes involved in nitrogen fixation, nitrification and denitrification in forest ecosystems. Soil Biol Biochem 75:11–25. https://doi.org/10.1016/j.soilbio.2014.03.021
Li T, Gao B, Tong Z, Yang Y, Li Y (2019) Chitosan and graphene oxide nanocomposites as coatings for controlled-release fertilizer. Water Air Soil Pollut 230(7):1–9. https://doi.org/10.1007/s11270-019-4173-2
Li J, Wu F, Fang Q, Wu Z, Duan Q, Li X, Ye W (2020) The mutual effects of graphene oxide nanosheets and cadmium on the growth, cadmium uptake and accumulation in rice. Plant Physiol Biochem 147:289–294. https://doi.org/10.1016/j.plaphy.2019.12.034
Liao J, Liu X, Hu A, Song H, Chen X, Zhang Z (2020) Effects of biochar-based controlled release nitrogen fertilizer on nitrogen-use efficiency of oilseed rape (Brassica napus L.). Sci Rep 10(1):1–14. https://doi.org/10.1038/s41598-020-67528-y
Liu R, Lal R (2015) Potentials of engineered nanoparticles as fertilizers for increasing agronomic productions. Sci Total Environ 514(2015):131–139. https://doi.org/10.1016/j.scitotenv.2015.01.104
Liu L, Shen G, Sun M, Cao X, Shang G, Chen P (2014) Effect of biochar on nitrous oxide emission and its potential mechanisms. J Air Waste Manag Assoc 64(8):894–902. https://doi.org/10.1080/10962247.2014.899937
Liu J, Ma K, Ciais P, Polasky S (2016) Reducing human nitrogen use for food production. Sci Rep 6:1–14. https://doi.org/10.1038/srep30104
López-Gutiérrez JC, Henry S, Hallet S, Martin-Laurent F, Catroux G, Philippot L (2004) Quantification of a novel group of nitrate-reducing bacteria in the environment by real-time PCR. J Microbiol Methods 57(3):399–407. https://doi.org/10.1016/j.mimet.2004.02.009
Lowry GV, Avellan A, Gilbertson LM (2019) Opportunities and challenges for nanotechnology in the agri-tech revolution. Nat Nanotechnol 14(6):517–522. https://doi.org/10.1038/s41565-019-0461-7
Miao Y, Liao R, Zhang XX, Wang Y, Wang Z, Shi P, Liu B, Li A (2015) Metagenomic insights into Cr (VI) effect on microbial communities and functional genes of an expanded granular sludge bed reactor treating high-nitrate wastewater. Water Research 76(Vi):43–52. https://doi.org/10.1016/j.watres.2015.02.042
Mu X, Yuan B, Feng X, Qiu S, Song L, Hu Y (2016) The effect of doped heteroatoms (nitrogen, boron, phosphorus) on inhibition thermal oxidation of reduced graphene oxide. RSC Adv 6(107):105021–105029. https://doi.org/10.1039/c6ra21329d
Neff JC, Townsend AR, Gleixner G, Lehman SJ, Turnbull J, Bowman WD (2002) Variable effects of nitrogen additions on the stability and turnover of soil carbon. Nature 419(6910):915–917. https://doi.org/10.1038/nature01136
Okano Y, Hristova KR, Leutenegger CM, Jackson LE, Denison RF, Gebreyesus B, Lebauer D, Scow KM (2004) Application of real-time PCR to study effects of ammonium on population size of ammonia-oxidizing bacteria in soil. Appl Environ Microbiol 70(2):1008–1016. https://doi.org/10.1128/AEM.70.2.1008-1016.2004
Ouyang Y, Evans SE, Friesen ML, Tiemann LK (2018) Effect of nitrogen fertilization on the abundance of nitrogen cycling genes in agricultural soils: a meta-analysis of field studies. Soil Biol Biochem 127:71–78. https://doi.org/10.1016/j.soilbio.2018.08.024
Oyelami AO, Semple KT (2015) Impact of carbon nanomaterials on microbial activity in soil. Soil Biol Biochem 86:172–180. https://doi.org/10.1016/j.soilbio.2015.03.029
Padilla FM, Gallardo M, Manzano-Agugliaro F (2018) Global trends in nitrate leaching research in the 1960–2017 period. Sci Total Environ 643(2):400–413. https://doi.org/10.1016/j.scitotenv.2018.06.215
Pandey K, Lahiani MH, Hicks VK, Hudson MK, Green MJ, Khodakovskaya M (2018) Effects of carbon-based nanomaterials on seed germination, biomass accumulation and salt stress response of bioenergy crops. PLoS ONE 13(8):1–17. https://doi.org/10.1371/journal.pone.0202274
Pandorf M, Pourzahedi L, Gilbertson L, Lowry GV, Herckes P, Westerhoff P (2020) Graphite nanoparticle addition to fertilizers reduces nitrate leaching in growth of lettuce (Lactuca sativa). Environ Sci Nano 7(1):127–138. https://doi.org/10.1039/c9en00890j
Perreault F, De Faria AF, Elimelech M (2015) Environmental applications of graphene-based nanomaterials. Chem Soc Rev 44(16):5861–5896. https://doi.org/10.1039/c5cs00021a
Phillips CJ, Paul EA, Prosser JI (2000) Quantitative analysis of ammonia oxidising bacteria using competitive PCR. FEMS Microbiol Ecol 32(2):167–175. https://doi.org/10.1016/S0168-6496(00)00028-3
Ren W, Ren G, Teng Y, Li Z, Li L (2015) Time-dependent effect of graphene on the structure, abundance, and function of the soil bacterial community. J Hazard Mater 297:286–294. https://doi.org/10.1016/j.jhazmat.2015.05.017
Rösch C, Mergel A, Bothe H (2002) Biodiversity of denitrifying and dinitrogen-fixing bacteria in an acid forest soil. Appl Environ Microbiol 68(8):3818–3829. https://doi.org/10.1128/AEM.68.8.3818-3829.2002
Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63(12):4704–4712. https://doi.org/10.1128/aem.63.12.4704-4712.1997
Shi Y, Liu X, Zhang Q (2019) Effects of combined biochar and organic fertilizer on nitrous oxide fluxes and the related nitrifier and denitrifier communities in a saline-alkali soil. Sci Total Environ 686:199–211. https://doi.org/10.1016/j.scitotenv.2019.05.394
Shrestha B, Acosta-Martinez V, Cox SB, Green MJ, Li S, Cañas-Carrell JE (2013) An evaluation of the impact of multiwalled carbon nanotubes on soil microbial community structure and functioning. J Hazard Mater 261(2013):188–197. https://doi.org/10.1016/j.jhazmat.2013.07.031
Simonin M, Richaume A (2015) Impact of engineered nanoparticles on the activity, abundance, and diversity of soil microbial communities: a review. Environ Sci Pollut Res 22(18):13710–13723. https://doi.org/10.1007/s11356-015-4171-x
Song G, Pandorf M, Westerhoff P, Ma Y (2018a) Carbon nanomaterial-based fertilizers can improve plant growth. In: Bai JA, Rai R (eds) Nanotechnology Applications in the Food Industry, 1st edn. CRC Press, United States, pp 21–44
Song J, Duan C, Sang Y, Wu S, Ru J, Cui X (2018) Effects of graphene on bacterial community diversity and soil environments of haplic Cambisols in Northeast China. Forests 9(11):1–18. https://doi.org/10.3390/f9110677
Sun R, Guo X, Wang D, Chu H (2015) Effects of long-term application of chemical and organic fertilizers on the abundance of microbial communities involved in the nitrogen cycle. Appl Soil Ecol 95:171–178. https://doi.org/10.1016/j.apsoil.2015.06.010
Tan G, Wang H, Xu N, Liu H, Zhai L (2018) Biochar amendment with fertilizers increases peanut N uptake, alleviates soil N2O emissions without affecting NH3 volatilization in field experiments. Environ Sci Pollut Res 25(9):8817–8826. https://doi.org/10.1007/s11356-017-1116-6
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 Microbiol Ecol 49(3):401–417. https://doi.org/10.1016/j.femsec.2004.04.011
Timilsena YP, Adhikari R, Casey P, Muster T, Gill H, Adhikari B (2015) Enhanced efficiency fertilisers: a review of formulation and nutrient release patterns. J Sci Food Agric 95(6):1131–1142. https://doi.org/10.1002/jsfa.6812
Tong Z, Bischoff M, Nies L, Applegate B, Turco RF (2007) Impact of fullerene (C60) on a soil microbial community. Environ Sci Technol 41(8):2985–2991. https://doi.org/10.1021/es061953l
Wakelin SA, Colloff MJ, Harvey PR, Marschner P, Gregg AL, Rogers SL (2007) The effects of stubble retention and nitrogen application on soil microbial community structure and functional gene abundance under irrigated maize. FEMS Microbiol Ecol 59(3):661–670. https://doi.org/10.1111/j.1574-6941.2006.00235.x
Wang J, Wang S (2019) Preparation, modification and environmental application of biochar: a review. J Clean Prod 227:1002–1022. https://doi.org/10.1016/j.jclepro.2019.04.282
Wang Y, Chang CH, Ji Z, Bouchard DC, Nisbet RM, Schimel JP, Gardea-Torresdey JL, Holden PA (2017) Agglomeration determines effects of carbonaceous nanomaterials on soybean nodulation, dinitrogen fixation potential, and growth in soil. ACS Nano 11(6):5753–5765. https://doi.org/10.1021/acsnano.7b01337
Wang YY, Lu SE, Xiang QJ, Yu XM, Ke ZH, Zhang XP, Tu SH, Gu YF (2017) Responses of N2O reductase gene (nosZ)-denitrifier communities to long-term fertilization follow a depth pattern in calcareous purplish paddy soil. J Integr Agric 16(11):2597–2611. https://doi.org/10.1016/S2095-3119(17)61707-6
Wei W, Isobe K, Nishizawa T, Zhu L, Shiratori Y, Ohte N, Koba K, Otsuka S, Senoo K (2015) Higher diversity and abundance of denitrifying microorganisms in environments than considered previously. ISME J 9(9):1954–1965. https://doi.org/10.1038/ismej.2015.9
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
Xiao Z, Rasmann S, Yue L, Lian F, Zou H, Wang Z (2019) The effect of biochar amendment on N-cycling genes in soils: a meta-analysis. Sci Total Environ 696:133984. https://doi.org/10.1016/j.scitotenv.2019.133984
Xiao X, Xie G, Yang Z, He N, Yang D, Liu M (2021) Variation in abundance, diversity, and composition of nirK and nirS containing denitrifying bacterial communities in a red paddy soil as affected by combined organic-chemical fertilization. Appl Soil Ecol 166:104001. https://doi.org/10.1016/j.apsoil.2021.104001
Xu HJ, Wang XH, Li H, Yao HY, Su JQ, Zhu YG (2014) Biochar impacts soil microbial community composition and nitrogen cycling in an acidic soil planted with rape. Environ Sci Technol 48(16):9391–9399. https://doi.org/10.1021/es5021058
Yang Y, Bi X, Westerhoff P, Hristovski K, McLain JE (2014) Engineered nanomaterials impact biological carbon conversion in soils. Environ Eng Sci 31(7):381–392. https://doi.org/10.1089/ees.2013.0421
Yang Y, Zhao J, Jiang Y, Hu Y, Zhang M, Zeng Z (2017) Response of bacteria harboring nirS and nirK genes to different N fertilization rates in an alkaline northern Chinese soil. Eur J Soil Biol 82:1–9. https://doi.org/10.1016/j.ejsobi.2017.05.006
Yang Y, Nie J, Wang S, Shi L, Li Z, Zeng Z, Zang H (2021) Differentiated responses of nirS-and nirK-type denitrifiers to 30 years of combined inorganic and organic fertilization in a paddy soil. Arch Agron Soil Sci 67(1):79–92. https://doi.org/10.1080/03650340.2020.1714032
Yao H, Gao Y, Nicol GW, Campbell CD, Prosser JI, Zhang L, Han W, Singh BK (2011) Links between ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Appl Environ Microbiol 77(13):4618–4625. https://doi.org/10.1128/AEM.00136-11
Yin C, Fan F, Song A, Cui P, Li T, Liang Y (2015) Denitrification potential under different fertilization regimes is closely coupled with changes in the denitrifying community in a black soil. Appl Microbiol Biotechnol 99(13):5719–5729. https://doi.org/10.1007/s00253-015-6461-0
Yu J, Deem LM, Crow SE, Deenik JL, Penton CR (2018) Biochar application influences microbial assemblage complexity and composition due to soil and bioenergy crop type interactions. Soil Biol Biochem 117:97–107. https://doi.org/10.1016/j.soilbio.2017.11.017
Yu J, Deem LM, Crow SE, Deenik J, Penton CR (2019) Comparative metagenomics reveals enhanced nutrient cycling potential after 2 years of biochar amendment in a tropical oxisol. Appl Environ Microbiol 85(11):1–17. https://doi.org/10.1128/AEM.02957-18
Yu J, Pavia MJ, Deem LM, Crow SE, Deenik JL, Penton CR (2020) DNA-stable isotope probing shotgun metagenomics reveals the resilience of active microbial communities to biochar amendment in Oxisol soil. Front Microbiol 11:1–16. https://doi.org/10.3389/fmicb.2020.587972
Zhang H, Hines D, Akins DL (2014) Synthesis of a nanocomposite composed of reduced graphene oxide and gold nanoparticles. Dalton Trans 43(6):2670–2675. https://doi.org/10.1039/c3dt52573b
Zhang M, Gao B, Chen J, Li Y, Creamer AE, Chen H (2014) Slow-release fertilizer encapsulated by graphene oxide films. Chem Eng J 255:107–113. https://doi.org/10.1016/j.cej.2014.06.023
Zhang M, Gao B, Chen J, Li Y (2015) Effects of graphene on seed germination and seedling growth. J Nanopart Res 17(2):1–8. https://doi.org/10.1007/s11051-015-2885-9
Zhang M, Bai SH, Tang L, Zhang Y, Teng Y, Xu Z (2017) Linking potential nitrification rates, nitrogen cycling genes and soil properties after remediating the agricultural soil contaminated with heavy metal and fungicide. Chemosphere 184:892–899. https://doi.org/10.1016/j.chemosphere.2017.06.081
Zhou N, Zhao Z, Wang H, Chen X, Wang M, He S, Liu W, Zheng M (2019) The effects of graphene oxide on nitrification and N2O emission: dose and exposure time dependent. Environ Pollut 252:960–966. https://doi.org/10.1016/j.envpol.2019.06.009
Acknowledgements
The authors appreciate the technical assistance of Dr. Yuanming Guo and Dr. Paul Dahlen in instrumental analysis at Arizona State University. The authors would also like to acknowledge Dr. Guixue Song at Shandong University and Mingdong Zhang at SinoPhene Novel Materials for providing GNA and GO materials for this study. Finally, the authors gratefully acknowledge the use of facilities within the Eyring Materials Center at Arizona State University in part by NNCI-ECCS-1542160.
Funding
This work is supported by AFRI A1511 Nanotechnology for Agriculture and Food Systems [grant no. 2020–67021-31377] from the USDA National Institute of Food and Agriculture.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Das, P., Davis, K., Penton, C.R. et al. Impacts of graphitic nanofertilizers on nitrogen cycling in a sandy, agricultural soil. J Nanopart Res 24, 120 (2022). https://doi.org/10.1007/s11051-022-05500-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11051-022-05500-9