Adsorption of herring sperm DNA onto pine sawdust biochar: Thermodynamics and site energy distribution

Highlights

● Adsorption of environmental deoxyribonucleic acid on biochar was studied.

● π−π interaction and electrostatic repulsion worked in the adsorption.

● Thermodynamics indicated the adsorption was spontaneous and endothermic.

Abstract

Environmental deoxyribonucleic acid (eDNA), which includes antibiotic resistance genes, is ubiquitous in the environment. The interactions between eDNA and biochar, a promising material widely used in soil amendment and water treatment, greatly affect the environmental behavior of eDNA. Hitherto few experimental evidences are available yet, especially on the information of thermodynamics and energy distribution to explains the interactions between biochar and eDNA. This study investigated the adsorption of herring sperm DNA (hsDNA) on pine sawdust biochar, with a specific emphasis on the adsorption thermodynamics and site energy distribution. The adsorption of hsDNA on biochar was enhanced by an increase in the pyrolysis and adsorption temperatures. The higher surface area, stronger π−π interaction, and weaker electrostatic repulsion between hsDNA and biochars prepared at high pyrolysis temperatures facilitated the adsorption of hsDNA. The thermodynamics indicated that the adsorption of hsDNA on biochar was spontaneous and endothermic. Therefore, higher temperature was beneficial for the adsorption of hsDNA on biochar; this was well explained by the increase in E^* and F(E^*) with the adsorption temperature. These results are useful for evaluating the migration and transformation of eDNA in the presence of biochar.

Graphical abstract

Keywords

Environmental deoxyribonucleic acid / Antibiotic resistance genes / Biochar / Adsorption thermodynamics

References

[1] AhmadA, LohM, AzizJ. (2007). Preparation and characterization of activated carbon from oil palm wood and its evaluation on methylene blue adsorption. Dyes and Pigments, 75( 2): 263– 272

[2] BounaasM, BouguettouchaA, ChebliD, GaticaJ M, VidalH. (2021). Role of the wild carob as biosorbent and as precursor of a new high-surface-area activated carbon for the adsorption of methylene blue. Arabian Journal for Science and Engineering, 46( 1): 325– 341

[3] CaiP Huang Q LiM LiangW ( 2008). Binding and degradation of DNA on montmorillonite coated by hydroxyl aluminum species. Colloids and Surfaces. B, Biointerfaces, 62( 2): 299− 306

[4] ChenB, ZhouD, ZhuL. (2008). Transitional adsorption and partition of nonpolar and polar aromatic contaminants by biochars of pine needles with different pyrolytic temperatures. Environmental Science & Technology, 42( 14): 5137– 5143

[5] ChenH, ZhangY, LiJ, ZhangP, LiuN. (2019). Preparation of pickling-reheating activated alfalfa biochar with high adsorption efficiency for p-nitrophenol: characterization, adsorption behavior, and mechanism. Environmental Science and Pollution Research International, 26( 15): 15300– 15313

[6] ChenY, LiuJ, ZengQ, LiangZ, YeX, LvY, LiuM. (2021). Preparation of Eucommia ulmoides lignin-based high-performance biochar containing sulfonic group: Synergistic pyrolysis mechanism and tetracycline hydrochloride adsorption. Bioresource Technology, 329 : 124856

[7] DingZ, WanY, HuX, WangS, ZimmermanA R, GaoB. (2016). Sorption of lead and methylene blue onto hickory biochars from different pyrolysis temperatures: Importance of physicochemical properties. Journal of Industrial and Engineering Chemistry, 37 : 261– 267

[8] DongX, SinghB P, LiG, LinQ, ZhaoX. (2019). Biochar increased field soil inorganic carbon content five years after application. Soil & Tillage Research, 186 : 36– 41

[9] FangJ, JinL, MengQ, WangD, LinD. (2021). Interactions of extracellular DNA with aromatized biochar and protection against degradation by DNAse I. Journal of Environmental Sciences (China), 101 : 205– 216

[10] GaoN, LiA, QuanC, DuL, DuanY. (2013). TG–FTIR and Py–GC/MS analysis on pyrolysis and combustion of pine sawdust. Journal of Analytical and Applied Pyrolysis, 100 : 26– 32

[11] GardnerC M, GunschC K. (2017). Adsorption capacity of multiple DNA sources to clay minerals and environmental soil matrices less than previously estimated. Chemosphere, 175 : 45– 51

[12] HongM, ZhangL, TanZ, HuangQ. (2019). Effect mechanism of biochar’s zeta potential on farmland soil’s cadmium immobilization. Environmental Science and Pollution Research International, 26( 19): 19738– 19748

[13] HouY, WuP, ZhuN. (2014). The protective effect of clay minerals against damage to adsorbed DNA induced by cadmium and mercury. Chemosphere, 95 : 206– 212

[14] JelavićS, StippS L S, BovetN. (2018). Adsorption of organic ligands on low surface charge clay minerals: the composition in the aqueous interface region. Physical Chemistry Chemical Physics, 20( 25): 17226– 17233

[15] JiangS, NguyenT A, RudolphV, YangH, ZhangD, OkY S, HuangL. (2017). Characterization of hard- and softwood biochars pyrolyzed at high temperature. Environmental Geochemistry and Health, 39( 2): 403– 415

[16] LengL, XiongQ, YangL, LiH, ZhouY, ZhangW, JiangS, LiH, HuangH. (2021). An overview on engineering the surface area and porosity of biochar. Science of the Total Environment, 763 : 144204

[17] Levy-BoothD J, CampbellR G, GuldenR H, HartM M, PowellJ R, KlironomosJ N, Peter PaulsK, SwantonC J, TrevorsJ T, DunfieldK E. (2007). Cycling of extracellular DNA in the soil environment. Soil Biology & Biochemistry, 39( 12): 2977– 2991

[18] LianF, YuW, ZhouQ, GuS, WangZ, XingB. (2020). Size matters: Nano-biochar triggers decomposition and transformation inhibition of antibiotic resistance genes in aqueous environments. Environmental Science & Technology, 54( 14): 8821– 8829

[19] LiuF, WangS, FanJ, MaG. (2012). Adsorption of natural organic matter surrogates from aqueous solution by multiwalled carbon nanotubes. Journal of Physical Chemistry C, 116( 49): 25783– 25789

[20] LiuJ, ZhouB, ZhangH, MaJ, MuB, ZhangW. (2019). A novel Biochar modified by Chitosan-Fe/S for tetracycline adsorption and studies on site energy distribution. Bioresource Technology, 294 : 122152

[21] LiuT, WangY, ZangQ, ZhongG. (2018a). Hydrothermal synthesis, structural characterization, and interaction mechanism with DNA of Copper(II) complex containing 2,2′-bipyridine. Bioinorganic Chemistry and Applications, 2018 : 8459638

[22] LiuY Dai Q JinX DongX PengJ WuM Liang N PanB XingB( 2018b). Negative impacts of biochars on urease activity: High pH, heavy metals, polycyclic aromatic hydrocarbons, or free radicals? Environmental Science & Technology, 52( 21): 12740− 12747

[23] MinX Han P YangH KimH Tong M ( 2014). Influence of sulfate and phosphate on the deposition of plasmid DNA on silica and alumina-coated surfaces. Colloids and Surfaces. B, Biointerfaces, 118: 83− 89

[24] PanB, ZhangD, LiH, WuM, WangZ, XingB. (2013). Increased adsorption of sulfamethoxazole on suspended carbon nanotubes by dissolved humic acid. Environmental Science & Technology, 47( 14): 7722– 7728

[25] PietramellaraG, AscherJ, CeccheriniM T, NannipieriP, WenderothD. (2007). Adsorption of pure and dirty bacterial DNA on clay minerals and their transformation frequency. Biology and Fertility of Soils, 43( 6): 731– 739

[26] PolyF, ChenuC, SimonetP, RouillerJ, Jocteur MonrozierL. (2000). Differences between linear chromosomal and supercoiled plasmid DNA in their mechanisms and extent of adsorption on clay minerals. Langmuir, 16( 3): 1233– 1238

[27] PrasannamedhaG, KumarP S, MehalaR, SharumithaT J, SurendharD. (2021). Enhanced adsorptive removal of sulfamethoxazole from water using biochar derived from hydrothermal carbonization of sugarcane bagasse. Journal of Hazardous Materials, 407 : 124825

[28] PrudenA, PeiR, StorteboomH, CarlsonK H. (2006). Antibiotic resistance genes as emerging contaminants: studies in northern Colorado. Environmental Science & Technology, 40( 23): 7445– 7450

[29] QianL, ZhangW, YanJ, HanL, GaoW, LiuR, ChenM. (2016). Effective removal of heavy metal by biochar colloids under different pyrolysis temperatures. Bioresource Technology, 206 : 217– 224

[30] RajabiH, MoslehM H, MandalP, Lea-LangtonA, SedighiM. (2021). Sorption behaviour of xylene isomers on biochar from a range of feedstock. Chemosphere, 268 : 129310

[31] SchmidtM P, MartínezC E. (2017). Ironing out genes in the environment: An experimental study of the DNA-goethite interface. Langmuir, 33( 34): 8525– 8532

[32] ShengX, QinC, YangB, HuX, LiuC, WaigiM G, LiX, LingW. (2019). Metal cation saturation on montmorillonites facilitates the adsorption of DNA via cation bridging. Chemosphere, 235 : 670– 678

[33] ShiL, ZhangD, ZhaoJ, XueJ, YinM, LiangA, PanB. (2021). New insights into the different adsorption kinetics of gallic acid and tannic acid on minerals via ¹H NMR relaxation of bound water. Science of the Total Environment, 767 : 144447

[34] TeixidóM, PignatelloJ J, BeltránJ L, GranadosM, PecciaJ. (2011). Speciation of the ionizable antibiotic sulfamethazine on black carbon (biochar). Environmental Science & Technology, 45( 23): 10020– 10027

[35] WangB, ZhangY, ZhuD, LiH. (2020a). Assessment of bioavailability of biochar-sorbed tetracycline to Escherichia coli for activation of antibiotic resistance genes. Environmental Science & Technology, 54( 20): 12920– 12928

[36] WangC, WangT, LiW, YanJ, LiZ, AhmadR, HerathS K, ZhuN. (2014a). Adsorption of deoxyribonucleic acid (DNA) by willow wood biochars produced at different pyrolysis temperatures. Biology and Fertility of Soils, 50( 1): 87– 94

[37] WangP, LiuX, YuB, WuX, XuJ, DongF, ZhengY. (2020b). Characterization of peanut-shell biochar and the mechanisms underlying its sorption for atrazine and nicosulfuron in aqueous solution. Science of the Total Environment, 702 : 134767

[38] WangY, YinR, LiuR. (2014b). Characterization of biochar from fast pyrolysis and its effect on chemical properties of the tea garden soil. Journal of Analytical and Applied Pyrolysis, 110 : 375– 381

[39] WangZ, YuX, PanB, XingB. (2010). Norfloxacin sorption and its thermodynamics on surface-modified carbon nanotubes. Environmental Science & Technology, 44( 3): 978– 984

[40] WuJ, WangH, ZhuA, LongF. (2018). Adsorption kinetics of single-stranded DNA on functional silica surfaces and its influence factors: An evanescent-wave biosensor study. ACS Omega, 3( 5): 5605– 5614

[41] WuJ, WangT, ZhangY, PanW P. (2019). The distribution of Pb(II)/Cd(II) adsorption mechanisms on biochars from aqueous solution: Considering the increased oxygen functional groups by HCl treatment. Bioresource Technology, 291 : 121859

[42] WuW, YangM, FengQ, McgroutherK, WangH, LuH, ChenY. (2012). Chemical characterization of rice straw-derived biochar for soil amendment. Biomass and Bioenergy, 47 : 268– 276

[43] XiaoX, ChenB, ZhuL. (2014). Transformation, morphology, and dissolution of silicon and carbon in rice straw-derived biochars under different pyrolytic temperatures. Environmental Science & Technology, 48( 6): 3411– 3419

[44] YinD, WangX, ChenC, PengB, TanC, LiH. (2016). Varying effect of biochar on Cd, Pb and As mobility in a multi-metal contaminated paddy soil. Chemosphere, 152 : 196– 206

[45] YuW, LiN, TongD, ZhouC, LinC, XuC. (2013). Adsorption of proteins and nucleic acids on clay minerals and their interactions: A review. Applied Clay Science, 80−81 : 443– 452

[46] YuanL, ChenL, ChenX, LiuR, GeG. (2017). In situ measurement of surface functional groups on silica nanoparticles using solvent relaxation nuclear magnetic resonance. Langmuir, 33( 35): 8724– 8729

[47] YuanY, LiJ, DaiH. (2021). Microcystin-LR sorption and desorption by diverse biochars: Capabilities, and elucidating mechanisms from novel insights of sorption domains and site energy distribution. Science of the Total Environment, 754 : 141921

[48] ZhangL, LiH, ChenF, ZhangD, WuM, PanB, XingB. (2017). New insights provided by solvent relaxation NMR-measured surface area in liquids to explain phenolics sorption on silica nanoparticles. Environmental Science. Nano, 4( 3): 577– 584

[49] ZhangQ PengQ ShuX Mo D JiangD ( 2019). Spectroscopic analysis of tylosin adsorption on extracellular DNA reveals its interaction mechanism. Colloids and Surfaces. B, Biointerfaces, 183: 110431

[50] ZhaoR, MaX, XuJ, ZhangQ. (2018). Removal of the pesticide imidacloprid from aqueous solution by biochar derived from peanut shell. BioResources, 13( 3): 5656– 5669

[51] ZhongW, YuJ, LiangY. (2003). Chlorobenzylidine-herring sperm DNA interaction: Binding mode and thermodynamic studies. Spectrochimica Acta. Part A: Molecular and Biomolecular Spectroscopy, 59( 6): 1281– 1288

[52] ZhouG, QiuX, WuX, LuS. (2021). Horizontal gene transfer is a key determinant of antibiotic resistance genes profiles during chicken manure composting with the addition of biochar and zeolite. Journal of Hazardous Materials, 408 : 124883

Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 42167030), Yunnan Young and Middle-aged Academic and Technical Leaders Reserve Talents (No. 2018HB008), Yunnan Ten Thousand Talents Plan Young and Elite Talents Project (No. YNWR-QNBJ-2018-336), and Yunnan Provincial Scientific Innovation Team of Soil Environment and Ecological Safety (No. 2019HC008).

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11783-022-1579-7 and is accessible for authorized users.

RIGHTS & PERMISSIONS

2022 Higher Education Press