Abstract
In recent years, graphene has been applied in all kinds of industries because of its unique advantages. Simultaneously, the influence of graphene on soil is becoming increasingly prominent, but little information is available regarding the effect of graphene on the soil microbial community, especially the situation related to plant growth. Our aim was to investigate the impact of grapheme upon bacterial community diversity and chemical properties in Haplic Cambisols of Larix olgensis rhizosphere. By adding graphene (0, 7.58, 15.15, 30.30, 75.76 and 151.52 mg kg−1, respectively expressed as CK, T1, T2, T3, T4 and T5) to Haplic Cambisols planted Larix olgensis seedlings, we identified bacterial community diversity, structure and metabolic function, and measured the pH, organic matter, hydrolytic nitrogen and available P and K contents of rhizospheric soil. Graphene could increase bacterial richness, and a certain concentration of graphene allowed for greater community diversity. Bacterial community structure did not change significantly with increasing graphene concentration in a certain range due to the resistance of bacteria to graphene. Proteobacteria and Acidobacteria were the dominant bacteria, accounting for an average of 40.4% and 20.2% of soil bacteria, respectively. Graphene significantly affected bacterial community composition and metabolic function and varied with its concentration. Several key soil properties, namely, pH, organic matter and hydrolytic nitrogen contents, characterized the graphene effect on soil bacteria, and the determination of rhizospheric soil biochemical processes and the expression analysis of nutrient uptake-related genes can be considered for further research in the future.
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References
Akhavan O, Ghaderi E (2010) Toxicity of graphene and graphene oxide nanowalls against bacteria. ACS Nano 4:5731–5736. https://doi.org/10.1021/nn101390x
Azam A, Ahmed AS, Oves M, Khan MS, Habib SS, Memic A (2012) Antimicrobial activity of metal oxide nanoparticles against Gram-positive and Gram-negative bacteria: a comparative study. Int J Nanomed 7:6003–6009. https://doi.org/10.2147/IJN.S35347
Bergmann GT, Bates ST, Eilers KG, Lauber CL, Caporaso JG, Walters WA, Knight R, Fierer N (2011) The under-recognized dominance of Verrucomicrobia in soil bacterial communities. Soil Biol Biochem 43:1450–1455. https://doi.org/10.1016/j.soilbio.2011.03.012
Bradford MA, Jones TH, Bardgett RD, Black HIJ, Boag B, Bonkowski M, Cook R, Eggers T, Gange AC, Grayston SJ, Kandeler E, McCaig AE, Newington JE, Prosser JI, Setala H, Staddon PL, Tordoff GM, Tscherko D, Lawton JH (2002) Impacts of soil faunal community composition on model grassland ecosystems. Science 298:615–618. https://doi.org/10.1126/science.1075805
Buckley DH, Schmidt TM (2003) Diversity and dynamics of microbial communities in soils from agro-ecosystems. Environ Microbiol 5:441–452. https://doi.org/10.1046/j.1462-2920.2003.00404.x
Buckley DH, Huangyutitham V, Nelson TA, Rumberger A, Thies JE (2006) Diversity of Planctomycetes in soil in relation to soil history and environmental heterogeneity. Appl Environ Microbiol 72:4522–4531. https://doi.org/10.1128/AEM.00149-06
Chakravarty D, Erande MB, Late DJ (2015) Graphene quantum dots as enhanced plant growth regulators: effects on coriander and garlic plants. J Sci Food Agric 95:2772–2778. https://doi.org/10.1002/jsfa.7106
Chen LX (2005) Soil experiment and practice course. Northeast Forestry University Press, Harbin
Chen M, Sun Y, Liang J, Zeng GM, Li ZW, Tang L, Zhu Y, Jiang D, Song B (2019) Understanding the influence of carbon nanomaterials on microbial communities. Environ Int 126:690–698. https://doi.org/10.1016/j.envint.2019.02.005
Chen XF, Wang JC, You YM, Wang RY, Chu SH, Chi YW, Hayat K, Hui N, Liu XX, Zhang D, Zhou P (2021) When nanoparticle and microbes meet: the effect of multi-walled carbon nanotubes on microbial community and nutrient cycling in hyperaccumulator system. J Hazard Mater 423:e126947. https://doi.org/10.1016/j.jhazmat.2021.126947
Classen AT, Sundqvist MK, Henning JA, Newman GS, Moore JAM, Cregger MA, Moorhead LC, Patterson CN (2015) Direct and indirect effects of climate change on soil microbial and soil microbial-plant interactions: What lies ahead? Ecosphere 6:e130. https://doi.org/10.1890/ES15-00217.1
Du JJ, Hu XG, Zhou QX (2015) Graphene oxide regulates the bacterial community and exhibits property changes in soil. RSC Adv 5:27009–27017. https://doi.org/10.1039/c5ra01045d
Du ST, Zhang P, Zhang RR, Lu Q, Liu L, Bao XW, Liu HJ (2016) Reduced graphene oxide induces cytotoxicity and inhibits photosynthetic performance of the green alga Scenedesmus obliquus. Chemosphere 164:499–507. https://doi.org/10.1016/j.chemosphere.2016.08.138
Ehrenfeld JG, Ravit B, Elgersma K (2005) Feedback in the plant-soil system. Annu Rev Environ Resour 30:75–115. https://doi.org/10.1146/annurev.energy.30.050504.144212
Feng XY, Wang QL, Sun YH, Zhang SW, Wang FY (2022) Microplastics change soil properties, heavy metal availability and bacterial community in a Pb-Zn-contaminated soil. J Hazard Mater 424:e127364. https://doi.org/10.1016/j.jhazmat.2021.127364
Fierer N (2017) Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol 15:579–590. https://doi.org/10.1038/nrmicro.2017.87
Ge Y, Priester JH, van der Werfhorst LC, Walker SL, Nisbet RM, An YJ, Schimel JP, Gardea-Torresdey JL, Holden PA (2014) Soybean plants modify metal oxide nanoparticle effects on soil bacterial communities. Environ Sci Technol 48:13489–13496. https://doi.org/10.1021/es5031646
Geim AK, Novoselov KS (2007) The Rise of Graphene. Nat Mat 6:183–191. https://doi.org/10.1038/nmat1849
Gurunathan S, Han JW, Dayem AA, Eppakayala V, Kim JH (2012) Oxidative stress-mediated antibacterial activity of graphene oxide and reduced graphene oxide in Pseudomonas aeruginosa. Int J Nanomedicine 7:5901–5914. https://doi.org/10.2147/IJN.S37397
Hao Y, Ma CX, Zhang ZT, Song YH, Cao WD, Guo J, Zhou GP, Rui YK, Liu LM, Xing BS (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
Hug LA, Castelle CJ, Wrighton KC, Thomas BC, Sharon I, Frischkorn KR, Williams KH, Tringe SG, Banfield JF (2013) Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling. Microbiome 1:e22. https://doi.org/10.1186/2049-2618-1-22
Hugenholtz P, Stackebrandt E (2004) Reclassification of Sphaerobacter thermophilus from the subclass Sphaerobacteridae in the phylum Actinobacteria to the class Thermomicrobia (emended description) in the phylum Chloroflexi (emended description). Int J Syst Evol Microbiol 54:2049–2051. https://doi.org/10.1099/ijs.0.03028-0
Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72:1719–1728. https://doi.org/10.1128/AEM.72.3.1719-1728.2006
Ji YZ, Feng WZ, Chen LX, Duan WB, Zhang XG (2008) Soil nutrition, microorganisms and enzyme activity of the rhizosphere and non-rhizosphere soils of mixed plantation of Larix. Ecol Environ 17:339–343
Jin LX, Son YH, DeForest JL, Kang YJ, Kim W, Chung H (2014) Single-walled carbon nanotubes alter soil microbial community composition. Sci Total Environ 466:533–538. https://doi.org/10.1016/j.scitotenv.2013.07.035
Khodakovskaya MV, Kim BS, Kim JN, Alimohammadi M, Dervishi E, Mustafa T, Cerniglal CE (2013) Carbon nanotubes as plant growth regulators: effects on tomato growth, reproductive system, and soil microbial community. Small 9:115–123. https://doi.org/10.1002/smll.201201225
Kong W, Kum H, Bae SH, Shim J, Kim H, Kong LP, Meng Y, Wang KJ, Kim C, Kim J (2019) Path towards graphene commercialization from lab to market. Nat Nanotechnol 14:927–938. https://doi.org/10.1038/s41565-019-0555-2
Kuzyakov Y, Blagodatskaya E (2015) Microbial hotspots and hot moments in soil: concept & review. Soil Biol Biochem 83:184–199. https://doi.org/10.1016/j.soilbio.2015.01.025
Kuzyakov Y, Razavi BS (2019) Rhizosphere size and shape: temporal dynamics and spatial stationarity. Soil Biol Biochem 135:343–360. https://doi.org/10.1016/j.soilbio.2019.05.011
Lanphere JD, Luth CJ, Walker SL (2013) Effects of solution chemistry on the transport of graphene oxide in saturated porous media. Environ Sci Technol 47:4255–4261. https://doi.org/10.1021/es400138c
Li LN, Teng Y, Ren WJ, Li ZG, Luo YM (2016) Effects of graphene on soil enzyme activities and microbial communities. Soils 48:102–108
Liu SB, Zeng TH, Hofmann M, Burcombe E, Wei J, Jiang RR, Kong J, Chen Y (2011) Antibacterial activity of graphite, graphite oxide, graphene oxide, and reduced graphene oxide: membrane and oxidative stress. ACS Nano 5:6971–6980. https://doi.org/10.1021/nn202451x
Lj S, Nicol GW, Smith Z, Fear J, Prosser JI, Baggs EM (2006) Nitrosospira spp. can produce nitrous oxide via a nitrifier denitrification pathway. Environ Microbiol 8:214–222. https://doi.org/10.1111/j.1462-2920.2005.00882.x
Mai-Prochnow A, Clauson M, Hong JM, Murphy AB (2016) Gram positive and Gram negative bacteria differ in their sensitivity to cold plasma. Sci Rep 6:e38610. https://doi.org/10.1038/srep38610
Nielsen S, Minchin T, Kimber S, van Zwieten LV, Gilbert J, Munroe P, Munroe P, Joseph S, Thomas T (2014) Comparative analysis of the microbial communities in agricultural soil amended with enhanced biochars or traditional fertilisers. Agric Ecosyst Environ 191:73–82. https://doi.org/10.1016/j.agee.2014.04.006
Novoselov KS, Geim AK, Morozov SV, Jiang D, Zhang Y, Dubonos SV, Grigorieva IV, Firsov AA (2004) Electric field effect in atomically thin carbon films. Science 306:666–669. https://doi.org/10.1126/science.1102896
Pan FJ, Han XZ, Zou WX, Wang CL, Zhang ZM, Liu H, Xu YL (2021) Shifts of bacterial community structure and function in long-term soybean monoculture. Arch Agron Soil Sci 67:793–808. https://doi.org/10.1080/03650340.2020.1759797
Pankratov TA, Ivanova AO, Dedysh SN, Liesack W (2011) Bacterial populations and environmental factors controlling cellulose degradation in an acidic Sphagnum peat. Environ Microbiol 13:1800–1814. https://doi.org/10.1111/j.1462-2920.2011.02491.x
Park MVDZ, Bleeker EA, Brand W, Cassee FR, van Elk M, Gosens I, de Jong WH, Meesters JAJ, Peijnenburg WJGM, Quik JTK, Vandebriel RJ, Sips AJAM (2017) Considerations for safe innovation: the case of graphene. ACS Nano 11:9574–9593. https://doi.org/10.1021/acsnano.7b04120
Park S, Choi KS, Kim S, Gwon Y, Kim J (2020) Graphene oxide-assisted promotion of plant growth and stability. Nanomaterials 10:e758. https://doi.org/10.3390/nano10040758
Perreault F, de Faria AF, Nejati S, Elimelech M (2015) Antimicrobial properties of graphene oxide nanosheets: Why size matters. ACS Nano 9:7226–7736. https://doi.org/10.1021/acsnano.5b02067
Premanathan M, Karthikeyan K, Jeyasubramanian K, Manivannan G (2011) Selective toxicity of ZnO nanoparticles toward Gram-positive bacteria and cancer cells by apoptosis through lipid peroxidation. Nanomedicine 7:184–192. https://doi.org/10.1016/j.nano.2010.10.001
Rajapaksha RMCP, Tobor-Kaplon MA, Baath E (2004) Metal toxicity affects fungal and bacterial activities in soil differently. Appl Environ Microbiol 70:2966–2973. https://doi.org/10.1128/AEM.70.5.2966-2973.2004
Ren WJ, Ren GD, Teng Y, Li ZG, Li LN (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
Roesch LF, Fulthorpe RR, Riva A, Casella G, Hadwin AKM, Kent AD, Daroub SH, Camargo FAO, Farmerie WG, Triplett EW (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1:283–290. https://doi.org/10.1038/ismej.2007.53
Ruiz ON, Fernando KAS, Wang BJ, Brown NA, Luo PG, McNamara ND, Vangsness M, Sun YP, Bunker CE (2011) Graphene oxide: a nonspecific enhancer of cellular growth. ACS Nano 5:8100–8107. https://doi.org/10.1021/nn202699t
Shao YY, Zou L, Wang ZY, Wu SP (2011) Dynamics of soil nutrient and microbial community of larch plantation. J North-East For Univ 39:82–84
Shaw LJ, Nicol GW, Smith Z, Fear J, Prosser JI, Baggs EM (2006) Nitrosospira spp. can produce nitrous oxide via a nitrifier denitrification pathway. Environ Microbiol 8:214–222. https://doi.org/10.1111/j.1462-2920.2005.00882.x
Shrestha B, Acosta-Martinez V, Cox SB, Green MJ, Li S, Canas-Carrell JE (2013) An evaluation of the impact of multiwalled carbon nanotubes on soil microbial community structure and functioning. J Hazard Mater 261:188–197. https://doi.org/10.1016/j.jhazmat.2013.07.031
Song JF, Duan CW, Sang Y, Wu SP, Ru JX, Cui XY (2018) Effects of graphene on bacterial community diversity and soil environments of Haplic Cambisols in northeast China. Forests 9:e677. https://doi.org/10.3390/f9110677
Song A, Li ZM, Wang EZ, Xu DY, Wang S, Bi JJ, Wang HL, Jeyakumar P, Li ZY, Fan FL (2021) Supplying silicon alters microbial community and reduces soil cadmium bioavailability to promote health wheat growth and yield. Sci Total Environ 796:e148797. https://doi.org/10.1016/j.scitotenv.2021.148797
Spain AM, Krumholz LR, Elshahed MS (2009) Abundance, composition, diversity and novelty of soil Proteobacteria. ISME J 3:992–1000. https://doi.org/10.1038/ismej.2009.43
Sun TY, Gottschalk F, Hungerbuhler K, Nowack B (2014) Comprehensive probabilistic modelling of environmental emissions of engineered nanomaterials. Environ Pollut 185:69–76. https://doi.org/10.1016/j.envpol.2013.10.004
Sutcliffe IC (2011) Cell envelope architecture in the Chloroflexi: a shifting frontline in a phylogenetic turf war. Environ Microbiol 13:279–282. https://doi.org/10.1111/j.1462-2920.2010.02339.x
Tong ZH, Bischoff M, Nies LF, Myer P, Applegate B, Turco RF (2012) Response of soil microorganisms to As-produced and functionalized single-wall carbon nanotubes (SWNTs). Environ Sci Technol 46:13471–13479. https://doi.org/10.1021/es303251r
van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, Kardol P, Klironomos JN, Kulmatiski A, Schweitzer JA, Suding KN, van de Voorde TFJ, Wardle DA (2013) Plant-soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276. https://doi.org/10.1111/1365-2745.12054
Vetrovsky T, Steffen KT, Baldrian P (2014) Potential of cometabolic transformation of polysaccharides and lignin in lignocellulose by soil Actinobacteria. PLoS ONE 9:e89108. https://doi.org/10.1371/journal.pone.0089108
Wagg C, Bender SF, Widmer F, van der Heijden MGA (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci 111:5266–5270. https://doi.org/10.1073/pnas.1320054111
Wang QS, Qi XC, Shen TL, Li CL (2017) Effect of silver nanoparticles and graphene on soil microorganisms and enzyme activities. Acta Sci Circum 37:3149–3157
Wang C, Liu DW, 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
Wei DC, Liu YQ (2010) Controllable synthesis of graphene and its applications. Adv Mater 22:3225–3241. https://doi.org/10.1002/adma.200904144
Yan YY, Chen ZH, Zhu FX, Zhu CY, Wang C, Gu C (2020) Effect of polyvinyl chloride microplastics on bacterial community and nutrient status in two agricultural soils. Bull Environ Contam Toxicol 107:602–609. https://doi.org/10.1007/s00128-020-02900-2
Yang LB, Zhu DG, Cui FX, Li JB, Song RQ, Ni HW (2017) Soil microbial community characteristics of the different forest types of arix gmelini forest in cold temperate zone. J North-East For Univ 45:66–72
Yergeau E, Sanschagrin S, Beaumier D, Greer CW (2012) Metagenomic analysis of the bioremediation of diesel-contaminated Canadian high arctic soils. PLoS ONE 7:e30058. https://doi.org/10.1371/journal.pone.0030058
Yu ZH, Li YS, Wang GH, Tang CX, Wang YH, Liu JJ, Liu XB, Jin J (2018) Elevated CO2 alters the abundance but not the structure of diazotrophic community in the rhizosphere of soybean grown in a Mollisol. Biol Fert Soils 54:877–881. https://doi.org/10.1007/s00374-018-1311-8
Zhang ZM, Yan J, Han XZ, Zou WX, Wang E, Lu XC, Chen X (2020) Keystone microbiomes revealed by 14 years of field restoration of the degraded agricultural soil under distinct vegetation scenarios. Front Microbiol 11:e1915. https://doi.org/10.3389/fmicb.2020.01915
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This work was supported by Open Grant for Key Laboratory of Sustainable Forest Ecosystem Management (Northeast Forestry University), Ministry of Education (KFJJ2021YB01), and Natural Science Foundation of Heilongjiang Province (LH2021C008).
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Zhang, X., Luo, N., Sang, Y. et al. Graphene Changes Soil Chemical Properties and Bacterial Community of Haplic Cambisols in the Larix olgensis Rhizosphere. J Soil Sci Plant Nutr 22, 3157–3171 (2022). https://doi.org/10.1007/s42729-022-00874-0
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DOI: https://doi.org/10.1007/s42729-022-00874-0