Research progress of rhizosphere effect in the remediation of heavy metal contaminated soil
-
摘要: 由根际分泌物介导的根际效应表现为根际土壤中微生物种类和活性、土壤理化性质(如酶、pH、有机质等)显著不同于非根际土壤。根际效应受土壤类型、植物种类等影响较大,在农业生产、林业防护等领域被广泛研究,并被投入到实际应用中。近年来,根际效应在土壤修复领域的研究取得了一定进展,但对其修复机制、影响因素等尚缺乏系统性的认识。综述了受重金属污染土壤中根际效应的修复机制、影响因素,并提出加强修复效果的措施,以期利用根际效应提高土壤生物修复效率。根际效应驱动根际土壤与非根际土壤中重金属的形态和分布差异显著,受土壤类型、植物功能性状、重金属性质等因素影响,土壤改良、接种外源微生物等措施可强化植物根际对重金属污染土壤的修复效果。然而目前相关研究时间较短、规模较小,忽略了多年生植物不同生长阶段的根际效应对重金属修复效果的影响,植物生长发育周期长导致筛选特异性修复植物也存在一定的挑战。随着根际效应在土壤修复领域研究的深入,建议展开更系统、全面、长期的指标监测研究,从而明确影响根际效应修复重金属的主次因素,同时筛选出针对不同重金属污染土壤的特异性修复植物,以便于建立土壤生物修复的植物资源库。Abstract: The rhizosphere effect mediated by rhizosphere exudates shows that the species and activities of microorganisms, and soil physicochemical properties such as enzymes, pH and organic matter in rhizosphere soil are significantly different from those in non-rhizosphere soil. Rhizosphere effect is greatly affected by soil types and plant species, etc., and has been widely studied and used in agricultural production and forestry protection. In recent years, some progress had been made in the research of rhizosphere effect on soil remediation, but systematic understanding of its remediation mechanism and influencing factors still needed to be further improved. In this study, the remediation mechanism and influencing factors of rhizosphere effect in heavy metal contaminated soil were reviewed and analyzed, and the measures to strengthen the remediation effect were proposed to improve the soil bioremediation efficiency by rhizosphere effect. The review indicated that the rhizosphere effects drove the significant differences in the form and distribution of heavy metals between the rhizosphere and non-rhizosphere soils. Affected by soil types, plant functional traits, heavy metal properties and other factors, soil improvement and inoculation of exogenous microorganisms could enhance the remediation effect of plant rhizosphere on heavy metals contaminated soil. However, current studies were in short term and small scale, and had neglected the rhizosphere effects at different growth stages of perennial plants on heavy metal remediation, and the long cycle of plant growth and development set a challenge for screening of specific remediation plants. With the deeper study of rhizosphere effect in the field of soil remediation, it was necessary to carry out more systematic, comprehensive and long-term index monitoring researches to identify the primary and secondary factors affecting the restoration of heavy metals by rhizosphere effect. At the same time, specific remediation plants of different heavy metal contaminated soil types were needed to be selected to facilitate the establishment of soil bioremediation plant resource bank.
-
Key words:
- rhizosphere effect /
- heavy metal /
- soil /
- rhizoremediation
-
表 1 重金属污染土壤植物修复案例
Table 1. Case of phytoremediation of heavy metal contaminated soil
重金属 修复植物 修复机制 影响因素 铜(Cu) 蓖麻(Castor bean) 增加酸交换性Cu浓度[34] 土壤pH[34] 小麦(Triticum aestivum) 降低Cu的有效性[35] 溶解性有机质浓度[35] 多瑙淫羊藿(Epilobium dodonaei) 固定重金属[32] 共存重金属类型[32] 埃塞俄比亚油菜(Brassica carinata) 提高重金属有效性[36] 种植模式[36] 锌(Zn) 芥菜(Brassica juncea) 分泌半胱氨酸、组氨酸螯合Zn离子[37] 混栽植物、外源微生物[37] 刺槐(Robinia pseudoacacia) 改变重金属有效性[5] 土壤理化性质、重金属性质[5] 铅(Pb) 芥菜(Brassica juncea) 添加生物炭,降低Pb的有效态浓度,固定Pb[38];
增加重金属有效性,促进植物吸收[39]生物炭含量[38]、外源微生物[39] 刺槐(Robinia pseudoacacia) 改变重金属有效性[5] 土壤理化性质、重金属性质[5] 碱蓬(Suaeda glauca) 增加pH,降低重金属离子浓度[40] 重金属浓度、植物种类[40] 萝卜(Raphanus sativus) 增加可溶性Pb浓度[41] 溶解性有机碳浓度[41] 东南景天(Sedum alfredii) 根系分泌物与重金属反应[23] 重金属浓度[23] 镉(Cd) 碱蓬(Suaeda glauca) 增加pH,降低重金属离子浓度[40] 重金属浓度、植物种类[40] 芥菜(Brassica juncea) 增加重金属有效性,促进植物吸收[39] 外源微生物[39] 叶用红菾菜(Beta vulgaris) 固定重金属[42] 植物类型[42] 黑麦草(Lolium perene) 固定重金属[42] 植物类型[42] 油菜(Brassica campestris) 固定重金属[43] 外源微生物、改良剂[43] 甘蓝型油菜(Brassica napus) 影响根际pH,促进植物对Cd的吸收和提取[44] 重金属浓度、改良剂的酸碱性[44] 砷(As) 蜈蚣草(Pteris vittata) 促进植物生长,活化重金属[45] 外源微生物[45] 玉米(Zea mays) 促进重金属解析[46] 外源微生物、改良剂[46] 锰(Mn) 碱蓬(Suaeda glauca) 增加pH,降低重金属离子浓度[40] 重金属浓度、植物种类[40] 铀(U) 黑麦草(Lolium perenne) pH降低促进根部惰性U的活化[47] 重金属浓度[47] -
[1] RILEY D, BARBER S A. Bicarbonate accumulation and pH changes at the soybean (Glycine max (L. ) merr. ) root-soil interface[J]. Soil Science Society of America Journal,1969,33(6):905-908. doi: 10.2136/sssaj1969.03615995003300060031x [2] 刘芷宇, 李良谟, 施卫明, 等. 根际研究法[M]. 南京: 江苏科学技术出版社, 1997: 308-327. [3] 贺纪正, 陆雅海, 傅伯杰. 土壤生物学前言[M]. 北京: 科学出版社, 2015: 291-326. [4] GUO M X, GONG Z Q, MIAO R H, et al. Microbial mechanisms controlling the rhizosphere effect of ryegrass on degradation of polycyclic aromatic hydrocarbons in an aged-contaminated agricultural soil[J]. Soil Biology and Biochemistry,2017,113:130-142. doi: 10.1016/j.soilbio.2017.06.006 [5] YANG Y R, DONG M, CAO Y P, et al. Comparisons of soil properties, enzyme activities and microbial communities in heavy metal contaminated bulk and rhizosphere soils of Robinia pseudoacacia L. in the northern foot of Qinling Mountain[J]. Forests,2017,8(11):430. doi: 10.3390/f8110430 [6] 王凯, 宋立宁, 张成龙, 等.科尔沁沙地典型林分土壤有机碳储量与根际效应的关系[J]. 水土保持学报,2013,27(6):221-225.WANG K, SONG L N, ZHANG C L, et al. Relationship between soil organic carbon storage and rhizosphere effect of typical forests in horqin sandy land[J]. Journal of Soil and Water Conservation,2013,27(6):221-225. [7] BOURCERET A, LEYVAL C, THOMAS F, et al. Rhizosphere effect is stronger than PAH concentration on shaping spatial bacterial assemblages along centimetre-scale depth gradients[J]. Canadian Journal of Microbiology,2017,63(11):881-893. [8] LIU Y X, LUO M, YE R Z, et al. Impacts of the rhizosphere effect and plant species on organic carbon mineralization rates and pathways, and bacterial community composition in a tidal marsh[J]. FEMS Microbiology Ecology,2019,95(9):fiz120. doi: 10.1093/femsec/fiz120 [9] MAPELLI F, MARASCO R, FUSI M, et al. The stage of soil development modulates rhizosphere effect along a high arctic desert chronosequence[J]. The ISME Journal,2018,12(5):1188-1198. doi: 10.1038/s41396-017-0026-4 [10] GUO Z B, LIU H, WAN S X, et al. Fertilisation practice changes rhizosphere microbial community structure in the agroecosystem[J]. Annals of Applied Biology,2019,174(2):123-132. doi: 10.1111/aab.12478 [11] 孙福红, 周启星, 陈艳卿.对二氯苯与Cd复合污染对毫米级根际微域土壤酶活性的联合毒性效应评价[J]. 环境工程技术学报,2016,6(6):571-578.SUN F H, ZHOU Q X, CHEN Y Q. Assessment on joint toxic effects of combined pollution of 1, 4-DCB and Cd on enzyme activities in millimeter rhizosphere[J]. Journal of Environmental Engineering Technology,2016,6(6):571-578. [12] MASSACCESI L, BENUCCI G M N, GIGLIOTTI G, et al. Rhizosphere effect of three plant species of environment under periglacial conditions (Majella Massif, central Italy)[J]. Soil Biology and Biochemistry,2015,89:184-195. doi: 10.1016/j.soilbio.2015.07.010 [13] 肖列, 刘国彬, 李鹏, 等.短期CO2浓度升高和干旱胁迫对白羊草土壤碳氮和微生物根际效应的影响[J]. 应用生态学报,2017,28(10):3251-3259.XIAO L, LIU G B, LI P, et al. Effects of short-term elevated CO2 concentration and drought stress on the rhizosphere effects of soil carbon, nitrogen and microbes of Bothriochloa ischaemum[J]. Chinese Journal of Applied Ecology,2017,28(10):3251-3259. [14] 马志良, 赵文强, 刘美, 等.增温对高寒灌丛根际和非根际土壤微生物生物量碳氮的影响[J]. 应用生态学报,2019,30(6):1893-1900.MA Z L, ZHAO W Q, LIU M, et al. Effects of warming on microbial biomass carbon and nitrogen in the rhizosphere and bulk soil in an alpine scrub ecosystem[J]. Chinese Journal of Applied Ecology,2019,30(6):1893-1900. [15] ZVEREV A O, PERSHINA E V, PROVOROV N A, et al. Metagenomic characteristic of rhizosphere effect on cereals in black and sod-podzolic soils[J]. Sel'Skokhozyaistvennaya Biologiya,2016,51(5):654-663. [16] 刘菊梅, 曹博, 石春芳, 等.紫花苜蓿根际效应对河套灌区土壤盐分和养分的影响[J]. 南方农业学报,2018,49(2):246-252.LIU J M, CAO B, SHI C F, et al. Rhizosphere effects of alfalfa on soil salt and nutrient in Hetao irrigation area[J]. Journal of Southern Agriculture,2018,49(2):246-252. [17] SCHOUTEDEN N, de WAELE D, PANIS B, et al. Arbuscular mycorrhizal fungi for the biocontrol of plant-parasitic Nematodes: a review of the mechanisms involved[J]. Frontiers in Microbiology,2015,6:1280. [18] 刘顺, 刘喜帅, 朱新传, 等.陈山红心杉土壤养分、酶活性的根际效应及肥力评价[J]. 植物营养与肥料学报,2017,23(2):492-501.LIU S, LIU X S, ZHU X C, et al. Rhizosphere effects of nutrients and enzyme activities of Cunninghania lanceolata and soil fertility assessment[J]. Journal of Plant Nutrition and Fertilizer,2017,23(2):492-501. [19] FINZI A C, ABRAMOFF R Z, SPILLER K S, et al. Rhizosphere processes are quantitatively important components of terrestrial carbon and nutrient cycles[J]. Global Change Biology,2015,21(5):2082-2094. doi: 10.1111/gcb.12816 [20] DOTANIYA M L, MEENA V D. Rhizosphere effect on nutrient availability in soil and its uptake by plants: a review[J]. Proceedings of the National Academy of Sciences, India Section B:Biological Sciences,2015,85(1):1-12. doi: 10.1007/s40011-013-0297-0 [21] 王晓婷, 陈瑞蕊, 井忠旺, 等.水稻和小麦根际效应及细菌群落特征的比较研究[J]. 土壤学报,2019,56(2):443-453.WANG X T, CHEN R R, JING Z W, et al. Comparative study on rhizosphere effects and bacterial communities in the rhizospheres of rice and wheat[J]. Acta Pedologica Sinica,2019,56(2):443-453. [22] 王雪峰, 毛之夏, 徐济责, 等.根际效应对大豆田土壤线虫群落组成及多样性的影响[J]. 生态学报,2016,36(16):5256-5262.WANG X F, MAO Z X, XU J Z, et al. Responses of soil nematode community composition and diversity to rhizosphere effects in a soybean field[J]. Acta Ecologica Sinica,2016,36(16):5256-5262. [23] LUO Q, WANG S Y, SUN L N, et al. Identification of root exudates from the Pb-accumulator Sedum alfredii under Pb stresses and assessment of their roles[J]. Journal of Plant Interactions,2017,12(1):272-278. doi: 10.1080/17429145.2017.1339837 [24] AHEMAD M. Enhancing phytoremediation of chromium-stressed soils through plant-growth-promoting bacteria[J]. Journal of Genetic Engineering and Biotechnology,2015,13(1):51-58. doi: 10.1016/j.jgeb.2015.02.001 [25] ZHAI X Q, LI Z W, HUANG B, et al. Remediation of multiple heavy metal-contaminated soil through the combination of soil washing and in situ immobilization[J]. Science of the Total Environment,2018,635:92-99. doi: 10.1016/j.scitotenv.2018.04.119 [26] HE L Z, ZHONG H A, LIU G X, et al. Remediation of heavy metal contaminated soils by biochar: mechanisms, potential risks and applications in China[J]. Environmental Pollution,2019,252:846-855. doi: 10.1016/j.envpol.2019.05.151 [27] EMENIKE C U, JAYANTHI B, AGAMUTHU P, et al. Biotransformation and removal of heavy metals: a review of phytoremediation and microbial remediation assessment on contaminated soil[J]. Environmental Reviews,2018,26(2):156-168. doi: 10.1139/er-2017-0045 [28] FASANI E, MANARA A, MARTINI F, et al. The potential of genetic engineering of plants for the remediation of soils contaminated with heavy metals[J]. Plant, Cell & Environment,2018,41(5):1201-1232. [29] SHARMA S, TIWARI S, HASAN A, et al. Recent advances in conventional and contemporary methods for remediation of heavy metal-contaminated soils[J]. Biotech,2018,8(4):1-18. [30] WAN X M, LEI M, CHEN T B. Cost-benefit calculation of phytoremediation technology for heavy-metal-contaminated soil[J]. Science of the Total Environment,2016,563/564:796-802. doi: 10.1016/j.scitotenv.2015.12.080 [31] GERHARDT K E, GERWING P D, GREENBERG B M. Opinion: taking phytoremediation from proven technology to accepted practice[J]. Plant Science,2017,256:170-185. doi: 10.1016/j.plantsci.2016.11.016 [32] RANĐELOVIĆ D, GAJIĆ G, MUTIĆ J, et al. Ecological potential of Epilobium dodonaei Vill. for restoration of metalliferous mine wastes[J]. Ecological Engineering,2016,95:800-810. doi: 10.1016/j.ecoleng.2016.07.015 [33] ZHAN J, SUN Q Y. Diversity of free-living nitrogen-fixing microorganisms in wastelands of copper mine tailings during the process of natural ecological restoration[J]. Journal of Environmental Sciences,2011,23(3):476-487. doi: 10.1016/S1001-0742(10)60433-0 [34] HUANG G Y, ZHOU X P, GUO G, et al. Variations of dissolved organic matter and Cu fractions in rhizosphere soil induced by the root activities of Castor bean[J]. Chemosphere,2020,254:126800. doi: 10.1016/j.chemosphere.2020.126800 [35] MOTAGHIAN H R, HOSSEINPUR A R. Rhizosphere effects on Cu availability and fractionation in sewage sludge-amended calcareous soils[J]. Journal of Plant Nutrition and Soil Science,2015,178(5):713-721. doi: 10.1002/jpln.201400513 [36] QUARTACCI M F, MICAELLI F, SGHERRI C. Brassica carinata planting pattern influences phytoextraction of metals from a multiple contaminated soil[J]. Agrochimica,2014,58(1):77-89. [37] ADEDIRAN G A,NGWENYA B T,MOSSELMANS J F W,et al. Mixed planting with a leguminous plant outperforms bacteria in promoting growth of a metal remediating plant through histidine synthesis[J]. International Journal of Phytoremediation,2016,18(7):720-729. doi: 10.1080/15226514.2015.1131235 [38] 刘旻慧, 王震宇, 陈蕾, 等.花生壳及中药渣混合生物炭对铅污染土壤的修复研究[J]. 中国海洋大学学报(自然科学版),2016,46(1):101-107.LIU M H, WANG Z Y, CHEN L, et al. Application of peanut shell and Chinese medicine mixed biochar as soil amendment to lead contaminated soil[J]. Periodical of Ocean University of China,2016,46(1):101-107. [39] LIU X Y, GUO D, REN C Y, et al. Performance of Streptomyces pactum-assisted phytoextraction of Cd and Pb: in view of soil properties, element bioavailability, and phytoextraction indices[J]. Environmental Science and Pollution Research International,2020,27(35):43514-43525. doi: 10.1007/s11356-020-09842-6 [40] ZHANG X, LI M, YANG H H, et al. Physiological responses of Suaeda glauca and Arabidopsis thaliana in phytoremediation of heavy metals[J]. Journal of Environmental Management,2018,223:132-139. [41] LI X X, HUANG S, MCBRIDE M B. Rhizosphere effect on Pb solubility and phytoavailability in Pb-contaminated soils[J]. Environmental Pollution,2021,268:115840. doi: 10.1016/j.envpol.2020.115840 [42] LYU Y, YU Y Q, LI T, et al. Rhizosphere effects of Loliumperenne L. and Beta vulgaris var. cicla L. on the immobilization of Cd by modified nanoscale black carbon in contaminated soil[J]. Journal of Soils and Sediments,2018,18(1):1-11. doi: 10.1007/s11368-017-1724-2 [43] LIU W, ZUO Q Q, ZHAO C C, et al. Effects of Bacillus subtilis and nanohydroxyapatite on the metal accumulation and microbial diversity of rapeseed (Brassica campestris L. ) for the remediation of cadmium-contaminated soil[J]. Environmental Science and Pollution Research International,2018,25(25):25217-25226. doi: 10.1007/s11356-018-2616-8 [44] ZENG X Y, ZOU D S, WANG A D, et al. Remediation of cadmium-contaminated soils using Brassica napus: effect of nitrogen fertilizers[J]. Journal of Environmental Management,2020,255:109885. doi: 10.1016/j.jenvman.2019.109885 [45] YANG Q, TU S, WANG G, et al. Effectiveness of applying arsenate reducing bacteria to enhance arsenic removal from polluted soils by Pteris vittata L[J]. International Journal of Phytoremediation,2012,14(1):89-99. doi: 10.1080/15226510903567471 [46] WANG S, PAN S, SHAH G M, et al. Enhancement in arsenic remediation by maize (Zea mays L. ) using edta in combination with arbuscular mycorrhizal fungi[J]. Applied Ecology and Environmental Research,2018,16(5):5987-5999. doi: 10.15666/aeer/1605_59875999 [47] 廉欢. 黑麦草对铀污染土壤植物提取修复的根际效应研究[D]. 抚州: 东华理工大学, 2018. [48] KIM K R, OWENS G, KWON S L. Influence of Indian mustard (Brassica juncea) on rhizosphere soil solution chemistry in long-term contaminated soils: a rhizobox study[J]. Journal of Environmental Sciences,2010,22(1):98-105. doi: 10.1016/S1001-0742(09)60080-2 [49] 郑志林, 罗有发, 周佳佳, 等.铅锌废渣堆场4种先锋修复植物根际微域磷素赋存形态特征[J]. 水土保持研究,2019,26(3):269-278.ZHENG Z L, LUO Y F, ZHOU J J, et al. The fraction characteristics of phosphorus in the rhizosphere of four pioneer restoration plants in lead-zinc waste slag yards[J]. Research of Soil and Water Conservation,2019,26(3):269-278. [50] 王甜甜, 闫冰, 陈彦君, 等.不同生育期转基因抗虫棉根际土壤细菌群落特征[J]. 环境科学研究,2021,34(7):1728-1736.WANG T T, YAN B, CHEN Y J, et al. Characteristics of bacterial community of rhizosphere soil of transgenic insect-resistant cotton at different growth stages[J]. Research of Environmental Sciences,2021,34(7):1728-1736. [51] 李廷强, 朱恩, 杨肖娥, 等.超积累植物东南景天根际可溶性有机质对土壤锌吸附解吸的影响[J]. 应用生态学报,2008,19(4):838-844.LI T Q, ZHU E, YANG X E, et al. Effects of dissolved organic matter derived from hyperaccumulator Sedum alfredii Hance rhizosphere on Zn adsorption and desorption in soil[J]. Chinese Journal of Applied Ecology,2008,19(4):838-844. [52] 朱佳文, 邹冬生, 向言词, 等.先锋植物对铅锌尾矿库重金属污染的修复作用[J]. 水土保持学报,2011,25(6):207-210.ZHU J W, ZOU D S, XIANG Y C, et al. Pioneer species on remediation of heavy metal contamination in lead/zinc mine tailings pond[J]. Journal of Soil and Water Conservation,2011,25(6):207-210. [53] NGUYEN T X T, AMYOT M, LABRECQUE M. Differential effects of plant root systems on nickel, copper and silver bioavailability in contaminated soil[J]. Chemosphere,2017,168:131-138. doi: 10.1016/j.chemosphere.2016.10.047 [54] GUO L, CUTRIGHT T J. Remediation of acid mine drainage (AMD)-contaminated soil by Phragmites australis and rhizosphere bacteria[J]. Environmental Science and Pollution Research,2014,21(12):7350-7360. doi: 10.1007/s11356-014-2642-0 [55] 刘智峰. 陕西凤县铅锌冶炼区土壤重金属污染特征及根际促生菌强化植物修复研究[D]. 杨凌: 西北农林科技大学, 2019. [56] PIZARRO R, FLORES J P, TAPIA J, et al. Forest species in the recovery of soils contaminated with copper due to mining activities[J]. Revista Chapingo, Serie Ciencias Forestales y del Ambiente,2016,22(1):29-43. [57] SARWAR N, IMRAN M, SHAHEEN M R, et al. Phytoremediation strategies for soils contaminated with heavy metals: odifications and future perspectives[J]. Chemosphere,2017,171:710-721. doi: 10.1016/j.chemosphere.2016.12.116 [58] SCHENKEVELD W D C, KRAEMER S M. Equilibrium and kinetic modelling of the dynamic rhizosphere[J]. Plant and Soil,2015,386(1/2):395-397. doi: 10.3969/j.issn.1674-991X.2016.06.082 [59] 王燕. 基于双同位素示踪法的根际土壤汞甲基化与去甲基化作用研究[D]. 重庆: 西南大学, 2020. [60] 龚贵清. 三峡库区消落带植物根际微域土壤汞形态及其与土壤性质的相关性[D]. 重庆: 西南大学, 2020. [61] ROSENVALD K, KUZNETSOVA T, OSTONEN I, et al. Rhizosphere effect and fine-root morphological adaptations in a chronosequence of silver birch stands on reclaimed oil shale post-mining areas[J]. Ecological Engineering,2011,37(7):1027-1034. doi: 10.1016/j.ecoleng.2010.05.011 [62] GUAN T X, HE H B, ZHANG X D, et al. Cu fractions, mobility and bioavailability in soil-wheat system after Cu-enriched livestock manure applications[J]. Chemosphere,2011,82(2):215-222. doi: 10.1016/j.chemosphere.2010.10.018 [63] 祖艳群, 卢鑫, 湛方栋, 等.丛枝菌根真菌在土壤重金属污染植物修复中的作用及机理研究进展[J]. 植物生理学报,2015,51(10):1538-1548.ZU Y Q, LU X, ZHAN F D, et al. A review on roles and mechanisms of arbuscular mycorrhizal fungi in phytoremediation of heavy metals-polluted soils[J]. Plant Physiology Journal,2015,51(10):1538-1548. □