In the present paper the effectiveness of biochar-aided phytostabilization of metal/metalloid-contaminated soil under freezing-thawing conditions and using the metal tolerating test plant Lolium perenne L. is comprehensively studied. The vegetative experiment consisted of plants cultivated for over 52 days with no exposure to freezing-thawing in a glass greenhouse, followed by 64 days under freezing-thawing in a temperature-controlled apparatus and was carried out in initial soil derived from a post-industrial urban area, characterized by the higher total content of Zn, Pb, Cu, Cr, As and Hg than the limit values included in the classification provided by the Regulation of the Polish Ministry of Environment. According to the substance priority list published by the Toxic Substances and Disease Registry Agency, As, Pb, and Hg are also indicated as being among the top three most hazardous substances. The initial soil was modified by biochar obtained from willow chips. The freeze-thaw effect on the total content of metals/metalloids (metal(-loid)s) in plant materials (roots and above-ground parts) and in phytostabilized soils (non- and biochar-amended) as well as on metal(-loid) concentration distribution/redistribution between four BCR (community bureau of reference) fractions extracted from phytostabilized soils was determined. Based on metal(-loid)s redistribution in phytostabilized soils, their stability was evaluated using the reduced partition index (Ir). Special attention was paid to investigating soil microbial composition. In both cases, before and after freezing-thawing, biochar increased plant biomass, soil pH value, and metal(-loid)s accumulation in roots, and decreased metal(-loid)s accumulation in stems and total content in the soil, respectively, as compared to the corresponding non-amended series (before and after freezing-thawing, respectively). In particular, in the phytostabilized biochar-amended series after freezing-thawing, the recorded total content of Zn, Cu, Pb, and As in roots substantially increased as well as the Hg, Cu, Cr, and Zn in the soil was significantly reduced as compared to the corresponding non-amended series after freezing-thawing. Moreover, exposure to freezing-thawing itself caused redistribution of examined metal(-loid)s from mobile and/or potentially mobile into the most stable fraction, but this transformation was favored by biochar presence, especially for Cu, Pb, Cr, and Hg. While freezing-thawing greatly affected soil microbiome composition, biochar reduced the freeze-thaw adverse effect on bacterial diversity and helped preserve bacterial groups important for efficient soil nutrient conversion. In biochar-amended soil exposed to freezing-thawing, psychrotolerant and trace element-resistant genera such as Rhodococcus sp. or Williamsia sp. were most abundant.

Agricultural Research Ltd Zahradni 400 1 66441 Troubsko Czech Republic

Department of Agrochemistry Soil Science Microbiology and Plant Nutrition Faculty of AgriSciences Mendel University in Brno Zemedelska 1 61300 Brno Czech Republic

Department of Botany Government Degree College Ramban 182144 India

Faculty of Geoengineering University of Warmia and Mazury in Olsztyn Słoneczna St 45G 10 719 Olsztyn Poland

Institute of Chemistry and Technology of Environmental Protection Faculty of Chemistry Brno University of Technology Purkynova 118 61200 Brno Czech Republic

Institute of Civil Engineering Warsaw University of Life Sciences Nowoursynowska 159 02 776 Warsaw Poland

Institute of Environmental Engineering Warsaw University of Life Sciences Nowoursynowska 159 02 776 Warsaw Poland

Zobrazit více v PubMed

Khalid S., Shahid M., Niazi N.K., Murtaza B., Bibi I., Dumat C. A comparison of technologies for remediation of heavy metal contaminated soils. J. Geochem. Explor. 2017;182:247–268. doi: 10.1016/j.gexplo.2016.11.021. DOI

Pourret O., Bollinger J.C., Hursthouse A. Heavy metal: A misused term? Acta Geochim. 2021;40:466–471. doi: 10.1007/s11631-021-00468-0. DOI

Khan S., Naushad M., Lima E.C., Zhang S., Shaheen S.M., Rinklebe J. Global soil pollution by toxic elements: Current status and future perspectives on the risk assessment and remediation strategies—A review. J. Hazard. Mat. 2021;417:126039. doi: 10.1016/j.jhazmat.2021.126039. PubMed DOI

Zhang J., Li C., Li G., He Y., Yang J., Zhang J. Effects of biochar on heavy metal bioavailability and uptake by tobacco (Nicotiana tabacum) in two soils. Agric. Ecosyst. Environ. 2021;317:107453. doi: 10.1016/j.agee.2021.107453. DOI

Thakare M., Sarma H., Datar S., Roy A., Pawar P., Gupta K., Pandit S., Prasad R. Understanding the holistic approach to plant-microbe remediation technologies for removing heavy metals and radionuclides from soil. Curr. Res. Biotechnol. 2021;3:84–98. doi: 10.1016/j.crbiot.2021.02.004. DOI

Palansooriya K.N., Shaheen S.M., Chene S.S., Tsange D.C.W., Hashimotof Y., Houg D., Bolanh N.S., Rinklebeb J., Oka Y.S. Soil amendments for immobilization of potentially toxic elements in contaminated soils: A critical review. Environ. Int. 2020;134:105046. doi: 10.1016/j.envint.2019.105046. PubMed DOI

Wyszkowski M., Radziemska M. Influence of chromium (III) and (VI) on the concentration of mineral elements in oat (Avena sativa L.) Fres. Environ. Bull. 2013;22:979–986.

U.S. Environmental Protection Agency (USEPA) Risk Assessment Guidance for Superfund (Rags). Human Health Evaluation Manual (Part E, Supplemental Guidance for Dermal Risk Assessment) Interim. I. [(accessed on 2 April 2022)];2004 Available online: http://www.epa.gov/oswer/riskassessment/ragse/

ATSDR Substance Priority List. Agency for Toxic Substance and Disease Registry, U.S . Toxicological Profile for Cadmium. Department of Health and Humans Services, Public Health Service, Centers for Disease Control; Atlanta, GA, USA: 2019.

Nsanganwimana F., Souki K.S.A., Waterlot C., Douay F., Pelfrêne A., Ridošková A., Louvel B., Pourrut B. Potentials of Miscanthus x giganteus for phytostabilization of trace element-contaminated soils: Ex situ experiment. Ecotox. Environ. Safe. 2021;214:112125. doi: 10.1016/j.ecoenv.2021.112125. PubMed DOI

Trippe K.M., Manning V.A., Reardon C.L., Klein A.N., Weidman C., Ducey T.F., Novak J.M., Watts D.W., Rushmiller H., Spokas K.A., et al. Phytostabilization of acidic mine tailings with biochar, biosolids, lime, and locally-sourced microbial inoculum: Do amendment mixtures influence plant growth, tailing chemistry, and microbial composition? Appl. Soil Ecol. 2021;165:103962. doi: 10.1016/j.apsoil.2021.103962. PubMed DOI PMC

Green C., Hoffnagle A. Phytoremediation Field Studies Database for Chlorinated Solvents, Pesticides, Explosives and Metals. U.S. Environmental Protection Agency Office of Superfund Remediation and Technology Innovation Washington, DC, August 2004. [(accessed on 2 April 2022)]. Available online: https://clu-in.org/download/techdrct/td_hoffnagle-phytoremediation.pdf.

Garau N., Castaldi P., Diquattro S., Pinna M.V., Senette C., Roggero P.P., Garau G. Combining grass and legume species with compost for assisted phytostabilization of contaminated soils. Environ. Technol. Innov. 2021;22:101387. doi: 10.1016/j.eti.2021.101387. DOI

Wang J., Shi L., Zhai L., Zhang H., Wang S., Zou J., Shen Z., Lian C., Chen Y. Analysis of the long-term effectiveness of biochar immobilization remediation on heavy metal contaminated soil and the potential environmental factors weakening the remediation effect: A review. Ecotox. Environ. Safe. 2021;207:111261. doi: 10.1016/j.ecoenv.2020.111261. PubMed DOI

Radziemska M., Gusiatin Z.M., Cydzik-Kwiatkowska A., Cerdà A., Pecina V., Bęś A., Datta R., Majewski G., Mazur Z., Dzięcioł J., et al. Insight into metal immobilization and microbial community structure in soil from a steel disposal dump that was phytostabilized with composted, pyrolyzed or gasified wastes. Chemosphere. 2021;272:129576. doi: 10.1016/j.chemosphere.2021.129576. PubMed DOI

Fan J., Cai C., Chi H., Reid B.J., Coulon F., Zhang Y., Hou Y. Remediation of cadmium and lead polluted soil using thiol modified biochar. J. Hazard. Mat. 2020;388:22037. doi: 10.1016/j.jhazmat.2020.122037. PubMed DOI

Liu B., Ma R., Fan H. Evaluation of the impact of freeze-thaw cycles on pore structure characteristics of black soil using X-ray computed tomography. Soil Till. Res. 2021;206:104810. doi: 10.1016/j.still.2020.104810. DOI

Sorensen P.O., Finzi A.C., Giasson M.A., Reinmann A.B., Sanders-DeMott R., Templer P.H. Winter soil freeze-thaw cycles lead to reductions in soil microbial biomass and activity not compensated for by soil warming. Soil Biol. Biochem. 2018;116:39–47. doi: 10.1016/j.soilbio.2017.09.026. DOI

Kreyling J., Beierkuhnlein C., Jentsch A. Effects of soil freeze–thaw cycles differ between experimental plant communities. Basic Appl. Ecol. 2010;11:65–75. doi: 10.1016/j.baae.2009.07.008. DOI

Zhao Q., Li P., Stagnitti F., Ye J., Dong D., Zhang Y., Li P. Effects of aging and freeze-thawing on extractability of pyrene in soil. Chemosphere. 2009;76:447–452. doi: 10.1016/j.chemosphere.2009.03.068. PubMed DOI

Güllü H., Khudir A. Effect of freeze-thaw cycles on unconfined compressive strength of fine-grained soil treated with jute fiber, steel fiber and lime. Cold Reg. Sci. Technol. 2014;106–107:55–65. doi: 10.1016/j.coldregions.2014.06.008. DOI

Xie S.B., Qu J.J., Lai Y.M., Zhou Z.W., Xu X.T. Effects of freeze-thaw cycles on soil mechanical and physical properties in the Qinghai-Tibet Plateau. J. Mt. Sci. Engl. 2015;12:999–1009. doi: 10.1007/s11629-014-3384-7. DOI

Muehe E.M., Weigold P., Adaktylou I.J., Planer-Friedrich B., Kraemer U., Kappler A., Behrens S. Rhizosphere microbial community composition affects cadmium and zinc uptake by the metal-hyperaccumulating plant Arabidopsis helleri. ASM J. Appl. Environ. Microbiol. 2015;81:2173–2181. doi: 10.1128/AEM.03359-14. PubMed DOI PMC

Ministry of Environment . Regulation of the Minister of Environment on the Standards of the Soil Quality and Ground Quality of 1.09.2016. Ministry of Environment; Warsaw, Poland: 2016. Dziennik Ustaw No 165, Pos. 1359.

Bis Z., Nowak W. Method and Appliance for Auto-Thermal Valorization of Waste Solid Fuels as Well as the Biomass Used for Pure Generation of Electric Power and Heat. PL204294 (B1). 31 December 2009. [(accessed on 2 April 2022)]. Available online: https://pl.espacenet.com/publicationDetails/description?locale=pl_PL&CC=PL&date=20091231&NR=204294B1&ND=5&KC=B1&rnd=1640378047723&FT=D&DB=;

Mitchell K.J. Growth of pasture species under controlled environment. I. Growth at various levels of constant temperature. N. Z. J. Sci. Tech. 1956;38:203–216.

Cool M., Hannaway D.B., Larson C., Myers D. Perennial Ryegrass (Lolium perenne L.) Oregon State University; Corvallis, OR, USA: 2004. [(accessed on 2 April 2022)]. Forage Fact Sheet. Available online: https://www.cabi.org/isc/datasheet/31166#F4A5D70D-10CB-4516-8089-2E8BA501F206.

Hannaway D., Fransen S., Cropper J., Teel M., Chaney M., Griggs T., Halse R., Hart J., Cheeke P., Hansen D., et al. Perennial Ryegrass (Lolium perenne L.) PNW 503. 1999:1–20.

Santibáñez C., Verdugo C., Ginocchio R. Phytostabilization of copper mine tailings with biosolids: Implications for metal uptake and productivity of Lolium perenne. Sci. Total Environ. 2008;395:1–10. doi: 10.1016/j.scitotenv.2007.12.033. PubMed DOI

Arienzo M., Adamo P., Cozzolino V. The potential of Lolium perenne for revegetation of contaminated soils from a metallurgical site. Sci. Total Environ. 2004;319:13–25. doi: 10.1016/S0048-9697(03)00435-2. PubMed DOI

Pichtel J., Salt C.A. Vegetative growth and trace metal accumulation in metalliferous waste. J. Environ. Qual. 1998;27:618–624. doi: 10.2134/jeq1998.00472425002700030020x. DOI

van der Ent A., Baker A.J.M., Reeves R.D., Pollard A.J., Schat H. Hyperaccumulators of metal and metalloid trace elements: Facts and fiction. Plant Soil. 2013;362:319–334. doi: 10.1007/s11104-012-1287-3. DOI

Lambrechts T., Couder E., Bernal M.P., Faz Á., Iserentant A., Lutts S. Assessment of heavy metal bioavailability in contaminated soils from a former mining area (La Union, Spain) using a rhizospheric test. Water Air Soil Pollut. 2011;217:333–346. doi: 10.1007/s11270-010-0591-x. DOI

Boyd R.S. Ecology of metal hyperaccumulation. New Phytol. 2004;162:563–567. doi: 10.1111/j.1469-8137.2004.01079.x. PubMed DOI

Hou R., Wang L., O’Connor D., Tsang D.C.W., Rinklebe J., Hou D. Effect of immobilizing reagents on soil Cd and Pb lability under freeze-thaw cycles: Implications for sustainable agricultural management in seasonally frozen land. Environ. Int. 2020;144:106040. doi: 10.1016/j.envint.2020.106040. PubMed DOI

Pueyo M., Mateu J., Rigol A., Vidal M., López-Sánchez J.F., Rauret G. Use of the modified BCR three-step sequential ex-traction procedure for the study of trace element dynamics in contaminated soils. Environ. Pollut. 2008;152:330–341. doi: 10.1016/j.envpol.2007.06.020. PubMed DOI

Caporaso J.G., Lauber C.L., Walters W.A., Berg-Lyons D., Lozupone C.A., Turnbaugh P.J., Fierer N., Knight R. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. USA. 2011;108:4516–4522. doi: 10.1073/pnas.1000080107. PubMed DOI PMC

Edgar R.C., Haas B.J., Clemente J.C., Quince C., Knight R. UCHIME improves sensitivity and speed of chimera detection. Oxford J. Bioinform. 2011;27:2194–2200. doi: 10.1093/bioinformatics/btr381. PubMed DOI PMC

Edgar R.C. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Meth. 2013;10:996–998. doi: 10.1038/nmeth.2604. PubMed DOI

Bokulich N.A., Rideout J.R., Kopylova E., Bolyen E., Patnode J., Ellett Z., McDonald D., Wolfe B., Maurice C.F., Dutton R.J., et al. A standardized, extensible framework for optimizing classification improves marker-gene taxonomic assignments. PeerJ Prepr. 2015;3:e934v2.

Dhariwal A., Chong J., Habib S., King I., Agellon L.B., Xia J. Microbiome Analyst—A web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data. Nucleic Acids Res. 2017;45:180–188. doi: 10.1093/nar/gkx295. PubMed DOI PMC

Chong J., Liu P., Zhou G., Xia J. Using Microbiome Analyst for comprehensive statistical, functional, and meta-analysis of microbiome data. Nat. Protoc. 2020;15:799–821. doi: 10.1038/s41596-019-0264-1. PubMed DOI

McMurdie P.J., Holmes S. Waste not, want not: Why rarefying microbiome data is inadmissible. PLoS Comput. Biol. 2014;10:e1003531. doi: 10.1371/journal.pcbi.1003531. PubMed DOI PMC

Guo X., Han W., Zhang G., Yang Y., Wei Z., He Q., Wu Q. Effect of inorganic and organic amendments on maize bio-mass, heavy metals uptake and their availability in calcareous and acidic washed soil. Environ. Technol. Innov. 2020;19:101038. doi: 10.1016/j.eti.2020.101038. DOI

Kurzemann F.R., Juárez N.F.D., Probst M., Gómez-Brandón M., Partl C., Insam H. Effect of biomass fly ashes from fast pyrolysis bio-oil production on soil properties and plant yield. J. Environ. Manag. 2021;298:113479. doi: 10.1016/j.jenvman.2021.113479. PubMed DOI

Feng Z., Ji S., Ping J., Cui D. Recent advances in metabolomics for studying heavy metal stress in plants. TracTrends Anal. Chem. 2021;143:116402. doi: 10.1016/j.trac.2021.116402. DOI

Tripathi S., Sharma P., Singh K., Purchase D., Chandra R. Translocation of heavy metals in medicinally important herbal plants growing on complex organometallic sludge of sugarcane molasses-based distillery waste. Environ. Tech. Inn. 2021;22:101434. doi: 10.1016/j.eti.2021.101434. DOI

Gonzaga M.I.S., Silva P.S.O., Santos J.C.J., Junior L.F.G.O. Biochar increases plant water use efficiency and biomass production while reducing Cu concentration in Brassica juncea L. in a Cu-contaminated soil. Ecotox. Env. Saf. 2020;183:109557. doi: 10.1016/j.ecoenv.2019.109557. PubMed DOI

Palva E.T., Thtiharju S., Tamminen I., Puhakainen T., Laitinen R., Svensson J., Flelenius E., Heino P. Biological Mechanisms of Low Temperature Stress Response: Cold Acclimation and Development of Freezing Tolerance in Plants. JIRCAS; Tsukuba, Japan: 2002. pp. 9–15. JIRCAS Working Report.

Fitzhugh R.D., Driscoll C.T., Groman P.M., Tierney G.L., Hardy F.J.P. Effects of soil freezing disturbance on soil solution nitrogen, phosphorus, and carbon chemistry in a northern hardwood ecosystem. Biogeochemistry. 2001;56:215–238. doi: 10.1023/A:1013076609950. DOI

Feng R.W., Wang Z., Yang J.G., Zhao P.P., Zhu Y.M., Li Y.P., Yu Y.S., Liu H., Rensing C., Wu Z.Y., et al. Underlying mechanisms responsible for restriction of uptake and translocation of heavy metals (metalloids) by selenium via root application in plants. J. Hazard. Mat. 2020;402:123570. doi: 10.1016/j.jhazmat.2020.123570. PubMed DOI

Moon D.H., Park J.W., Chang Y.Y., Ok Y.S., Lee S.S., Ahmad M., Koutsospyros A., Park J.H., Baek K. Immobilization of lead in contaminated firing range soil using biochar. Environ. Sci. Pollut. Res. 2013;20:8464. doi: 10.1007/s11356-013-1964-7. PubMed DOI

Ok Y.S., Kim S.C., Kim D.K., Skousen J.G., Lee J.S., Cheong Y.W., Kim S.J., Yang J.E. Ameliorants to immobilize Cd in rice paddy soils contaminated by abandoned metal mines in Korea. Environ. Geochem. Health. 2011;33:23. doi: 10.1007/s10653-010-9364-0. PubMed DOI

Bashir M.A., Naveed M., Ahmad Z., Gao B., Mustafa A., Núnez-Delgado A. Combined application of biochar and sulfur regulated growth, physiological, antioxidant responses and Cr removal capacity of maize (Zea mays L.) in tannery polluted soils. J. Environ. Manag. 2020;259:110051. doi: 10.1016/j.jenvman.2019.110051. PubMed DOI

Beesley L., Inneh O.S., Norton G.J., Jimenez E.M., Pardo T., Clemente R., Dawson J.J.C. Assessing the influence of com-post and biochar amendments on the mobility and toxicity of metals and arsenic in a naturally contaminated mine soil. Environ. Pollut. 2014;186:195–202. doi: 10.1016/j.envpol.2013.11.026. PubMed DOI

Hart J.J., Welch R.M., Norvell W.A., Clarke J.M., Kochian L.V. Zinc effects on cadmium accumulation and partitioning in near-isogenic lines of durum wheat that differ in grain cadmium concentration. New Phytol. 2005;167:391–401. doi: 10.1111/j.1469-8137.2005.01416.x. PubMed DOI

Namgay T., Singh B., Singh B.P. Influence of biochar application to soil on the availability of As, Cd, Cu, Pb, and Zn to maize (Zea mays L.) Aust. J. Soil Res. 2010;48:638–647. doi: 10.1071/SR10049. DOI

Vapaavuori E.M., Rikala R., Ryyppo A. Effects of root temperature on growth and photosynthesis in conifer seedlings during shoot elongation. Tree Physiol. 1992;10:217–230. doi: 10.1093/treephys/10.3.217. PubMed DOI

Wang L., O’Connor D., Rinklebe J., Ok Y.S., Tsang D.C., Shen Z., Hou D. Biochar aging: Mechanisms, physicochemical changes, assessment, and implications for field applications. Environ. Sci. Tech. 2020;54:14797–14814. doi: 10.1021/acs.est.0c04033. PubMed DOI

Garbuz S., Mackay A., Camps-Arbestain M., DeVantier B., Minor M. Biochar amendment improves soil physico-chemical properties and alters root biomass and the soil food web in grazed pastures. Agric. Ecosyst. Environ. 2021;319:107517. doi: 10.1016/j.agee.2021.107517. DOI

Yang K., Wang X., Cheng H., Tao S. Effect of aging on stabilization of Cd and Ni by biochars and enzyme activities in a historically contaminated alkaline agricultural soil simulated with wet–dry and freeze–thaw cycling. Environ. Pollut. 2021;268:115846. doi: 10.1016/j.envpol.2020.115846. PubMed DOI

He L., Zhong H., Liu G., Dai Z., Brookes P.C., Xu J. Remediation of heavy metal contaminated soils by biochar: Mechanisms, potential risks and applications in China. Environ. Pollut. 2019;252:846–855. doi: 10.1016/j.envpol.2019.05.151. PubMed DOI

Islam M.N., Taki G., Nguyen X.P., Jo Y.T., Kim J., Park J.H. Heavy metal stabilization in contaminated soil by treatment with calcined cockle shell. Environ. Sci. Pollut. Res. 2017;24:7177–7183. doi: 10.1007/s11356-016-8330-5. PubMed DOI

Li H., Ye X., Geng Z., Zhou H., Guo X., Zhang Y., Zhao H., Wang G. The influence of biochar type on long-term stabili-zation for Cd and Cu in contaminated paddy soils. J. Hazard. Mater. 2016;304:40–48. doi: 10.1016/j.jhazmat.2015.10.048. PubMed DOI

Wang Z., Li T., Liu D., Fu Q., Hou R., Li Q., Cui S., Li M. Research on the adsorption mechanism of Cu and Zn by bio-char under freeze-thaw conditions. Sci. Tot. Environ. 2021;774:145194. doi: 10.1016/j.scitotenv.2021.145194. PubMed DOI

Lucchini P., Quilliam R.S., DeLuca T.H., Vamerali T., Jones D.L. Does biochar application alter heavy metal dynamics in agricultural soil? Agric. Ecosys. Environ. 2014;184:149–157. doi: 10.1016/j.agee.2013.11.018. DOI

Chen D., Guo H., Li R., Li L., Pan G., Chang A., Joseph S. Low uptake affinity cultivars with biochar to tackle Cd-tainted rice—a field study over four rice seasons in Hunan, China. Sci. Tot. Environ. 2016;541:1489–1498. doi: 10.1016/j.scitotenv.2015.10.052. PubMed DOI

Shaheen S.M., El-Naggar A., Wang J., Hassan N.E., Niazi N.K., Wang H., Tsang D.C.W., Ok Y.S., Bolan N., Rinklebe J. Biochar from Biomass and Waste. Elsevier; Amsterdam, The Netherlands: 2019. Biochar as an (Im) mobilizing agent for the potentially toxic elements in contaminated soils; pp. 255–274.

Li L., Zhu C., Liu X., Li F., Li H., Ye J. Biochar amendment immobilizes arsenic in farmland and reduces its bioavailability. Environ. Sci. Poll. Res. 2018;25:34091–34102. doi: 10.1007/s11356-018-3021-z. PubMed DOI

Awad M., Liu Z., Skalicky M., Dessoky E.S., Brestic M., Mbarki S., Rastogi A., El Sabagh A. Fractionation of heavy met-als in multi-contaminated soil treated with biochar using the sequential extraction procedure. Biomolecules. 2021;11:448. doi: 10.3390/biom11030448. PubMed DOI PMC

Zhao B., O’Connor D., Shen Z., Tsang D.C., Rinklebe J., Hou D. Sulfur-modified biochar as a soil amendment to stabilize mercury pollution: An accelerated simulation of long-term aging effects. Environ. Poll. 2020;264:114687. doi: 10.1016/j.envpol.2020.114687. PubMed DOI

Chen X., Ji H., Yang W., Zhu B., Ding H. Speciation and distribution of mercury in soils around gold mines located up-stream of Miyun Reservoir, Beijing, China. J. Geochem. Explor. 2016;163:1–9. doi: 10.1016/j.gexplo.2016.01.015. DOI

Ferraro G., Pecori G., Rosi L., Bettucci L., Fratini E., Casini D., Rozzo A.M., Chiaramonti D. Biochar from lab-scale pyrolysis: Influence of feedstock and operational temperature. Biomass Conv. Bioref. 2021:1–11. doi: 10.1007/s13399-021-01303-5. DOI

Rui D., Wu Z., Ji M., Liu J., Wang S., Ito Y. Remediation of Cd-and Pb-contaminated clay soils through combined freeze-thaw and soil washing. J. Hazard. Mat. 2019;369:87–95. doi: 10.1016/j.jhazmat.2019.02.038. PubMed DOI

Yang J., Li X., Huang L., Jiang H. Actinobacterial diversity in the sediments of five cold springs on the Qinghai-Tibet Plateau. Front. Microbiol. 2015;6:1345. doi: 10.3389/fmicb.2015.01345. PubMed DOI PMC

Wang J., Fu R., Xu Z. Stabilization of heavy metals in municipal sewage sludge by freeze–thaw treatment with a blend of diatomite, FeSO4, and Ca(OH)2. J. Air Waste Manag. Assoc. 2017;67:847–853. doi: 10.1080/10962247.2017.1281175. PubMed DOI

Cui H., Li D., Liu X., Fan Y., Zhang X., Zhang S., Zhou J., Gang G., Zhoum J. Dry-wet and freeze-thaw aging activate endogenous copper and cadmium in biochar. J. Clean. Prod. 2021;288:125605. doi: 10.1016/j.jclepro.2020.125605. DOI

Klik B.K., Gusiatin Z.M., Kulikowska D. Suitability of environmental indices in assessment of soil remediation with con-ventional and next generation washing agents. Sci. Rep. 2020;10:1–14. doi: 10.1038/s41598-020-77312-7. PubMed DOI PMC

Fu Q., Yan J., Li H., Li T., Hou R., Liu D., Ji Y. Effects of biochar amendment on nitrogen mineralization in black soil with different moisture contents under freeze-thaw cycles. Geoderma. 2019;353:459–467. doi: 10.1016/j.geoderma.2019.07.027. DOI

Shen Y., Tang T., Zuo R., Tian Y., Zhang Z., Wang Y. The effect and parameter analysis of stress release holes on decreasing frost heaves in seasonal frost areas. Cold Reg. Sci. Tech. 2020;169:102898. doi: 10.1016/j.coldregions.2019.102898. DOI

Amin A.E.E.A.Z. Carbon sequestration, kinetics of ammonia volatilization and nutrient availability in alkaline sandy soil as a function on applying calotropis biochar produced at different pyrolysis temperatures. Sci. Tot. Environ. 2020;726:138489. doi: 10.1016/j.scitotenv.2020.138489. PubMed DOI

Lehmann J., Rillig M.C., Thies J., Masiello C.A., Hockaday W.C., Crowley D. Biochar effects on soil biota—A review. Soil Biol. Biochem. 2011;43:1812–1836. doi: 10.1016/j.soilbio.2011.04.022. DOI

Li X., Wang T., Chang S.X., Jiang X., Song Y. Biochar increases soil microbial biomass but has variable effects on micro-bial diversity: A meta-analysis. Sci. Total Environ. 2020;749:141593. doi: 10.1016/j.scitotenv.2020.141593. PubMed DOI

Xie Y., Fan J., Zhu W., Amombo E., Lou Y., Chen L., Fu J. Effect of heavy metal pollution on soil microbial diversity and bermudagrass genetic variation. Front. Plant Sci. 2016;7:755. doi: 10.3389/fpls.2016.00755. PubMed DOI PMC

Ayangbenro A.S., Babalola O.O. A new strategy for heavy metal polluted environments: A review of microbial bio-sorbents. Int. J. Environ. Res. Public Health. 2017;14:94. doi: 10.3390/ijerph14010094. PubMed DOI PMC

Jacquiod S., Cyriaque V., Riber L., Abu Al-Soud W., Gillan D.C., Ruddy W., Sørensen S.J. Long-term industrial metal contamination unexpectedly shaped diversity and activity response of sediment microbiome. J. Hazard. Mater. 2018;344:299–307. doi: 10.1016/j.jhazmat.2017.09.046. PubMed DOI

Moriwaki H., Koide R., Yoshikawa R., Warabino Y., Yamamoto H. Adsorption of rare earth ions onto the cell walls of wild-type and lipoteichoic acid-defective strains of Bacillus subtilis. Appl. Microbiol. Biotechnol. 2013;97:3721–3728. doi: 10.1007/s00253-012-4200-3. PubMed DOI

Azarbad H., van Gestel C.A.M., Niklinska M., Laskowski R., Reoling W.F.M., van Straalen N.M. Resilience of soil mi-crobial communities to metals and additional stressors: DNA-based approaches for assessing “stress-on-stress” responses. Int. J. Mol. Sci. 2016;17:933. doi: 10.3390/ijms17060933. PubMed DOI PMC

González Henao S., Ghneim-Herrera T. Heavy metals in soils and the remediation potential of bacteria associated with the plant microbiome. Front. Environ. Sci. 2021;9:15. doi: 10.3389/fenvs.2021.604216. DOI

Sorensen P.O., Templer P.H., Finzi A.C. Contrasting effects of winter snowpack and soil frost on growing season microbial biomass and enzyme activity in two mixed-hardwood forests. Biogeochem. 2016;128:141–154. doi: 10.1007/s10533-016-0199-3. DOI

Stres B., Philippot L., Faganeli J., Tiedje J.M. Frequent freeze-thaw cycles yield diminished yet resistant and responsive microbial communities in two temperate soils: A laboratory experiment. FEMS Microbiol. Ecol. 2010;74:323–335. doi: 10.1111/j.1574-6941.2010.00951.x. PubMed DOI

Luo G., Li L., Friman V.-P., Guo J., Guo S., Shen Q., Ling N. Organic amendments increase crop yields by improving microbe-mediated soil functioning of agroecosystems: A meta-analysis. Soil Biol. Biochem. 2018;124:105–115. doi: 10.1016/j.soilbio.2018.06.002. DOI

Boros-Lajszner E., Wyszkowska J., Borowik A., Kucharski J. Energetic value of Elymus elongatus L. and Zea mays L. grown on soil polluted with Ni2+, Co2+, Cd2+, and sensitivity of rhizospheric bacteria to heavy metals. Energies. 2021;14:4903. doi: 10.3390/en14164903. DOI

Mhete M., Eze P.N., Rahube T.O., Akinyemi F.O. Soil properties influence bacterial abundance and diversity under different land-use regimes in semi-arid environments. Sci. Afr. 2020;7:e00246. doi: 10.1016/j.sciaf.2019.e00246. DOI

Navas M., Pérez-Esteban J., Torres M.A., Hontoria C., Moliner A. Taxonomic and functional analysis of soil microbial communities in a mining site across a metal(loid) contamination gradient. Eur. J. Soil. Sci. 2021;72:1190–1205. doi: 10.1111/ejss.12979. DOI

Pereira S.I.A., Lima A.I.G., Figueira E.M.D.A.P. Screening possible mechanisms mediating cadmium resistance in Rhizobium leguminosarum bv viciae isolated from contaminated Portuguese soils. Microb. Ecol. 2006;52:176–186. doi: 10.1007/s00248-006-9057-5. PubMed DOI

Shivlata L., Satyanarayana T. Thermophilic and alkaliphilic Actinobacteria: Biology and potential applications. Front. Microbiol. 2015;6:1–29. doi: 10.3389/fmicb.2015.01014. PubMed DOI PMC

Makhalanyane T.P., Van Goethem M.W., Cowan D.A. Microbial diversity and functional capacity in polar soils. Curr. Opin. Biotechnol. 2016;38:159–166. doi: 10.1016/j.copbio.2016.01.011. PubMed DOI

Rippin M., Lange S., Sausen N., Becker B. Biodiversity of biological soil crusts from the Polar Regions revealed by metabarcoding. FEMS Microbiol. Ecol. 2018;94:fiy036. doi: 10.1093/femsec/fiy036. PubMed DOI

Juan Y., Jiang N., Tian L., Chen X., Sun W., Chen L. Effect of freeze-thaw on a midtemperate soil bacterial community and the correlation network of its members. BioMed Res. Int. 2018;2018:8412429. doi: 10.1155/2018/8412429. PubMed DOI PMC

Bhardwaj P., Singh K.R., Jadeja N.B., Phale P.S., Kapley A. Atrazine bioremediation and its influence on soil microbial diversity by metagenomics analysis. Indian J. Microbiol. 2020;60:388–391. doi: 10.1007/s12088-020-00877-4. PubMed DOI PMC

Zhou Y., Berruti F., Greenhalf C., Tian X., Henry H.A.L. Increased retention of soil nitrogen over winter by biochar ap-plication: Implications of biochar pyrolysis temperature for plant nitrogen availability. Agric. Ecosyst. Environ. 2017;236:61–68. doi: 10.1016/j.agee.2016.11.011. DOI

Shen C., Ge Y., Yang T., Chu H. Verrucomicrobial elevational distribution was strongly influenced by soil pH and car-bon/nitrogen ratio. J. Soils Sediments. 2017;17:2449–2456. doi: 10.1007/s11368-017-1680-x. DOI

Khadem A.F., Pol A., Jetten M.S.M., den Camp H.J.M.O. Nitrogen fixation by the verrucomicrobial methanotroph ‘Methylacidiphilum fumariolicum’ SolV. Microbiology. 2010;156:1052–1059. doi: 10.1099/mic.0.036061-0. PubMed DOI

Martinez-Garcia M., Brazel D.M., Swan B.K., Arnosti C., Chain P.S.G., Reitenga K.G., Xie G., Poulton N.J., Gomez M.L., Masland D.E.D., et al. Capturing single cell genomes of active polysaccharide degraders: An unexpected contribution of Verrucomicrobia. PLoS ONE. 2012;7:e35314. doi: 10.1371/journal.pone.0035314. PubMed DOI PMC

Park D., Kim H., Yoon S. Nitrous oxide reduction by an obligate aerobic bacterium, Gemmatimonas aurantiaca strain T-27. Appl. Environ. Microbiol. 2017;83:e00502–e00517. doi: 10.1128/AEM.00502-17. PubMed DOI PMC

Rezgui C., Trinsoutrot-Gattin I., Benoit M., Laval K., Riah-Anglet W. Linking changes in the soil microbial community to C and N dynamics during crop residue decomposition. J. Integr. Agric. 2021;20:3039–3059. doi: 10.1016/S2095-3119(20)63567-5. DOI

Castro-Silva C., Ruíz-Valdiviezo V.M., Valenzuela-Encinas C., Alcántara-Hernández R.J., Navarro-Noya Y.E., Vázquez-Núñez E., Luna-Guido M., Marsch R., Dendooven L. The bacterial community structure in an alkaline saline soil spiked with anthracene. Electron. J. Biotechnol. 2013;16:5.

Vertès A.A., Inui M., Yukawa H. The biotechnological potential of Corynebacterium glutamicum, from umami to chemurgy. In: Yukawa H., Inui M., editors. Corynebacterium glutamicum: Biology and Biotechnology Microbiology. Springer; Berlin/Heidelberg, Germany: 2013. pp. 1–49. Monographs, 23.

Thomas J.C., IV, Oladeinde A., Kieran T.J., Finger J.W., Bayona-Vásquez N.J., Cartee J.C., Beasley J.C., Seaman J.C., McArthur J.V., Rhodes O.E., et al. Co-occurrence of antibiotic, biocide, and heavy metal resistance genes in bacteria from metal and radionuclide contaminated soils at the Savannah River Site. Microb. Biotechnol. 2020;13:1179–1200. doi: 10.1111/1751-7915.13578. PubMed DOI PMC

Chellaiah E.R. Cadmium (heavy metals) bioremediation by Pseudomonas aeruginosa: A mini review. Appl. Water Sci. 2018;8:154. doi: 10.1007/s13201-018-0796-5. DOI

Zivkovic L.I., Rikalović M., Gojgić-Cvijović G., Kazazić S., Vrvić M., Brčeski I., Beškoski V., Lončarević B., Gopčevića K., Karadžić I. Cadmium specific proteomic responses of a highly resistant Pseudomonas aeruginosa san 814 ai. RSC Adv. 2018;8:10549–10560. doi: 10.1039/C8RA00371H. PubMed DOI PMC

Zhang X., Yang H., Cui Z. Assessment on cadmium and lead in soil based on a rhizosphere microbial community. Toxicol. Res. 2017;6:671–677. doi: 10.1039/C7TX00048K. PubMed DOI PMC

Shi L.-D., Chen Y.-S., Du J.-J., Hu Y.-Q., Shapleigh J.P., Zhao H.-P. Metagenomic evidence for a Methylocystis species capable of bioremediation of diverse heavy metals. Front. Microbiol. 2019;9:3297. doi: 10.3389/fmicb.2018.03297. PubMed DOI PMC

Delmotte N., Knief C., Chaffron S., Innerebner G., Roschitzki B., Schlapbach R., Mering C., Vorholt J.A. Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc. Natl. Acad. Sci. USA. 2009;106:16428–16433. doi: 10.1073/pnas.0905240106. PubMed DOI PMC

Armin E., Cernava T., Cardinale M., Soh J., Sensen C.W., Grube M., Berg G. Rhizobiales as functional and endosymbiontic members in the lichen symbiosis of Lobaria pulmonaria L. Front. Microbiol. 2015;6:53. PubMed PMC

Whalen J.K., Sampedro L. Soil microorganisms. In: Whalen J.K., Sampedro L., editors. Soil Ecology and Management. CABI; Wallingford, UK: 2009.

Mo S., Li J., Li B., Yu R., Nie S., Zhang Z., Liao J., Jiang Q., Yan B., Jiang C. Impacts of Desulfobacterales and Chromatiales on sulfate reduction in the subtropical mangrove ecosystem as revealed by SMDB analysis. BioRxiv. 2020 doi: 10.1101/2020.08.16.252635. DOI

Ming L., Wenxin Z., Xiuxiu C., Chunqin Z., Wei Z., Yan D., Feng Z., Peng Y., Xinping C. Soil microbial composition and phod gene abundance are sensitive to phosphorus level in a long-term wheat-maize crop system. Front. Microbiol. 2021;11:3547. PubMed PMC

Altimira F., Yáñez C., Bravo G., González M., Rojas L., Seeger M. Characterization of copper-resistant bacteria and bacterial communities from copper-polluted agricultural soils of central Chile. BMC Microbiol. 2012;12:e193. doi: 10.1186/1471-2180-12-193. PubMed DOI PMC

Thierry S., Macarie H., Iizuka T., Geißdörfer W., Assih E.A., Spanevello M., Verhe F., Thomas P., Fudou R., Monroy O., et al. Pseudoxanthomonas mexicana sp. nov. and Pseudoxanthomonas japonensis sp. nov., isolated from diverse environments, and emended descriptions of the genus Pseudoxanthomonas and of its type species. Int. J. Syst. Evol. Microbiol. 2004;54:2245–2255. doi: 10.1099/ijs.0.02810-0. PubMed DOI

Mahbub K.R., Krishnan K., Naidu R., Megharaj M. Mercury resistance and volatilization by Pseudoxanthomonas sp. SE1 isolated from soil. Environ. Technol. Innov. 2016;6:94–104. doi: 10.1016/j.eti.2016.08.001. DOI

Nayak A.S., Vijaykumar M.H., Karegoudar T.B. Characterization of biosurfactant produced by Pseudoxanthomonas sp. PNK-04 and its application in bioremediation. Int. Biodeterior. Biodegradat. 2009;63:73–79. doi: 10.1016/j.ibiod.2008.07.003. DOI

Guerrero L.D., Makhalanyane T.P., Aislabie J.M., Cowan D.A. Draft genome sequence of Williamsia sp. strain D3, isolated from the Darwin Mountains, Antarctica. Genome Announc. 2014;2:e01230-13. doi: 10.1128/genomeA.01230-13. PubMed DOI PMC

Kai E.X., Johari W.L.W., Habib S., Yasid N.A., Ahmad S.A., Shukor M.H. The growth of the Rhodococcus sp. on diesel fuel under the effect of heavy metals and different concentrations of zinc. Adv. Polar Sci. 2020;31:132–136.

Horn H., Keller A., Hildebrandt U., Kämpfer P., Riederer M., Hentschel U. Draft genome of the Arabidopsis thaliana phyllosphere bacterium, Williamsia sp. ARP1. Stand. Genomic Sci. 2016;11:8. doi: 10.1186/s40793-015-0122-x. PubMed DOI PMC