Influence of cadmium and copper mixtures to rhizosphere bacterial communities

Highlights

• The relative abundance of rhizosphere soil bacteria has significantly positive correlation with BCF of Cd and Cu.

• Obvious variations of predominant species of bacterial communities in rhizosphere soil would emerge in the additions with different concentrations of Cd-Cu mixtures.

• In the additions with Cd and Cu, the mean of rhizosphere soil bacterial community diversity index was ranked as: Cu alone>Cd-Cu mixtures>Cd pollution.

• The PCA and PERMANOVA analysis showed that Cu may be the main factor changing the composition of rhizosphere soil bacteria.

Abstract

To study the effects of combined Cd and Cu pollution on rhizosphere bacterial community. High-throughput sequencing was used to examine the response of rhizosphere bacterial communities to heavy-metal stress under single and mixed pollution of cadmium (Cd) and copper (Cu). With additions of Cd and Cu, the mean diversity index of rhizosphere bacterial community was in the order Cu alone>Cd-Cu mixtures>Cd alone. In all Cd and Cu treatments, the dominant phyla were Proteobacteria, Actinobacteria, Chloroflexi and Acidobacteria. In the additions with different concentrations of Cd-Cu mixtures, LEfSe indicated that there were differences in the predominant species of rhizosphere bacterial communities. Some genera such as Streptomyces and Microbacterium belonging to Actinobacteria as biomarkers were significantly enriched in both control and treatments, while some genera such as Pseudoxanthomonas and Rhodopseudomonas belonging to Proteobacteria as biomarkers were observed to be enriched in the additions with single and mixture of Cd and Cu. According to the Nonmetric multidimensional scaling (NMDS) analysis, the structure of rhizosphere bacterial community was different between treatments and the CK. Principal Component Analysis (PCA) and permutational multivariate analysis of variance (PERMANOVA) showed that there were significant differences among treatments (p<0.01), and that the addition of Cu might be the primary factor affecting the composition of rhizosphere bacterial communities.

Graphical abstract

Keywords

Cadmium / Copper / High-throughput sequencing / Bacterial community structure

References

[1] An, Y.J., Kim, Y.M., Kwon, T.I., Jeong, S.W., 2004. Combined effect of copper, cadmium, and lead upon Cucumis sativus growth and bioaccumulation. Science of the Total Environment 326, 85–93

[2] Anjum, S.A., Tanveer, M., Hussain, S., Bao, M., Wang, L., Khan, I., Ullah, E., Tung, S.A., Samad, R.A., Shahzad, B., 2015. Cadmium toxicity in Maize (Zea mays L.): consequences on antioxidative systems, reactive oxygen species and cadmium accumulation. Environmental Science and Pollution Research International 22, 17022–17030

[3] Cai, Y., Xu, W., Wang, M., Chen, W., Li, X., Li, Y., Cai, Y., 2019. Mechanisms and uncertainties of Zn supply on regulating rice Cd uptake. Environmental Pollution 253, 959–965

[4] Chaudhuri, D., Tripathy, S., Veeresh, H., Powell, M.A., Hart, B.R., 2003. Relationship of chemical fractions of heavy metals with microbial and enzyme activities in sludge and ash-amended acid lateritic soil from India. Environmental Geology 45, 115–123

[5] Chodak, M., Gołebiewski, M., Morawska-Płoskonka, J., Kuduk, K., Niklińska, M., 2013. Diversity of microorganisms from forest soils differently polluted with heavy metals. Applied Soil Ecology 64, 7–14

[6] Chu, L., Liu, D.Y., Wang, Y.B., 2006. Separated and combined effects of Cu and Cd on seeding growth and active oxygen metaolism system of Trifolium repens L. Frontiers in Broscience Landmark 11, 2861–2867

[7] Edgar, R.C., 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics (Oxford, England) 26, 2460–2461

[8] Feng, J., Lin, Y., Yang, Y., Shen, Q., Huang, J., Wang, S., Zhu, X., Li, Z., 2018. Tolerance and bioaccumulation of Cd and Cu in Sesuvium portulacastrum. Ecotoxicology and Environmental Safety 147, 306–312.

[9] Feris, K., Ramsey, P., Frazar, C., Moore, J.N., Gannon, J.E., Holben, W.E., 2003. Differences in hyporheic-zone microbial community structure along a heavy-metal contamination gradient. Applied and Environmental Microbiology 69, 5563–5573

[10] Fernández-Calviño, D., Arias-Estévez, M., Díaz-Raviña, M., Bååth, E., 2012. Assessing the effects of Cu and pH on microorganisms in highly acidic vineyard soils. European Journal of Soil Science 63, 571–578

[11] Ferreira, R., Gaspar, H., Gonzalez, J.M., Clara, M.I., Santana, M.M., 2015. Copper and temperature modify microbial communities, ammonium and sulfate release in soil. Journal of Plant Nutrition and Soil Science 178, 953–962

[12] Gan, Y., Wang, L., Yang, G., Dai, J., Wang, R., Wang, W., 2017. Multiple factors impact the contents of heavy metals in vegetables in high natural background area of China. Chemosphere 184, 1388–1395

[13] Giller, K.E., Witter, E., McGrath, S.P., 2009. Heavy metals and soil microbes. Soil Biology & Biochemistry 41, 2031–2037

[14] Gołebiewski, M., Deja-Sikora, E., Cichosz, M., Tretyn, A., Wróbel, B., 2014. 16S rDNA pyrosequencing analysis of bacterial community in heavy metals polluted soils. Microbial Ecology 67, 635–647

[15] Gong, Q., Wang, L., Dai, T., Zhou, J., Kang, Q., Chen, H., Li, K., Li, Z., 2019. Effects of copper on the growth, antioxidant enzymes and photosynthesis of spinach seedlings. Ecotoxicology and Environmental Safety 171, 771–780

[16] Greco, M., Sáez, C.A., Contreras, R.A., Rodríguez-Rojas, F., Bitonti, M.B., Brown, M.T., 2019. Cadmium and/or copper excess induce interdependent metal accumulation, DNA methylation, induction of metal chelators and antioxidant defences in the seagrass Zostera marina. Chemosphere 224, 111–119

[17] Guan, Y., Shao, C., Ju, M., 2014. Heavy metal contamination assessment and partition for industrial and mining gathering areas. International Journal of Environmental Research and Public Health 11, 7286–7303

[18] Guo, B., Hong, C., Tong, W., Xu, M., Huang, C., Yin, H., Lin, Y., Fu, Q., 2020. Health risk assessment of heavy metal pollution in a soil- rice system : a case study in the Jin- Qu Basin of China. Scientific Reports 10, 1–11

[19] Hansda, A., Kumar, V., Anshumali., 2017. Cu-resistant Kocuria sp. CRB15: a potential PGPR isolated from the dry tailing of Rakha copper mine. 3 Biotech, 7, 1–11.

[20] He, H., Li, W., Yu, R., Ye, Z., 2017. Illumina-based analysis of bulk and rhizosphere soil bacterial communities in paddy fields under mixed heavy metal contamination. Pedosphere 27, 569–578

[21] He, P.P., Lv, X.Z., Wang, G.Y., 2004. Effects of Se and Zn supplementation on the antagonism against Pb and Cd in vegetables. Environment International 30, 167–172

[22] Hou, S., Zheng, N., Tang, L., Ji, X., 2018. Effects of cadmium and copper mixtures to carrot and pakchoi under greenhouse cultivation condition. Ecotoxicology and Environmental Safety 159, 172–181

[23] Huang, G., Liao, J., Han, Z., Li, J., Zhu, L., Lyu, G., Lu, L., Xie, Y., Ma, J., 2020. Interaction between fungal communities, soil properties, and the survival of invading E. coli o157:H7 in soils. International Journal of Environmental Research and Public Health 17, 1–17

[24] Idris, R., Trifonova, R., Puschenreiter, M., Wenzel, W.W., Sessitsch, A., 2004. Bacterial communities associated with flowering plants of the Ni hyperaccumulator Thlaspi goesingense. Applied and Environmental Microbiology 70, 2667–2677

[25] Jiang, B., Adebayo, A., Jia, J., Xing, Y., Deng, S., Guo, L., Liang, Y., Zhang, D., 2019. Impacts of heavy metals and soil properties at a Nigerian e-waste site on soil microbial community. Journal of Hazardous Materials 362, 187–195

[26] Jiao, Y., Zhou, Z., Chen, T., Wei, Y., Zheng, J., Gao, R., Chen, H., 2018. Biomarkers of antibiotic resistance genes during seasonal changes in wastewater treatment systems. Environmental Pollution 234, 79–87

[27] Ju, W., Liu, L., Fang, L., Cui, Y., Duan, C., Wu, H., 2019. Impact of co-inoculation with plant-growth-promoting rhizobacteria and rhizobium on the biochemical responses of alfalfa-soil system in copper contaminated soil. Ecotoxicology and Environmental Safety, 167, 218–226.

[28] Kidd, P., Barceló, J., Bernal, M.P., Navari-Izzo, F., Poschenrieder, C., Shilev, S., Clemente, R., Monterroso, C., 2009. Trace element behaviour at the root-soil interface: Implications in phytoremediation. Environmental and Experimental Botany 67, 243–259

[29] Lanier, C., Bernard, F., Dumez, S., Leclercq-Dransart, J., Lemière, S., Vandenbulcke, F., Nesslany, F., Platel, A., Devred, I., Hayet, A., Cuny, D., Deram, A., 2019. Combined toxic effects and DNA damage to two plant species exposed to binary metal mixtures (Cd/Pb). Ecotoxicology and Environmental Safety,167, 278–287.

[30] Lauber, C.L., Strickland, M.S., Bradford, M.A., Fierer, N., 2008. The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biology & Biochemistry 40, 2407–2415

[31] Li, H., Liu, L., Luo, L., Liu, Y., Wei, J., Zhang, J., Yang, Y., Chen, A., Mao, Q., Zhou, Y., 2018. Response of soil microbial communities to red mud-based stabilizer remediation of cadmium-contaminated farmland. Environmental Science and Pollution Research International 25, 11661–11669

[32] Li, J., Zheng, Y.M., Liu, Y.R., Ma, Y.B., Hu, H.W., He, J.Z., 2014. Initial copper stress strengthens the resistance of soil microorganisms to a subsequent copper stress. Microbial Ecology 67, 931–941

[33] Lin, H., Liu, C., Li, B., Dong, Y., 2021. Trifolium repens L. regulated phytoremediation of heavy metal contaminated soil by promoting soil enzyme activities and beneficial rhizosphere associated microorganisms. Journal of Hazardous Materials 402, 123829.

[34] Liu, C., Lin, H., Dong, Y., Li, B., Liu, Y., 2018. Ecotoxicology and environmental safety investigation on microbial community in remediation of lead-contaminated soil by Trifolium repens L. Ecotoxicology and Environmental Safety 165, 52–60

[35] Liu, J., He, X.X., Lin, X.R., Chen, W.C., Zhou, Q.X., Shu, W.S., Huang, L.N., 2015. Ecological effects of combined pollution associated with e-waste recycling on the composition and diversity of soil microbial communities. Environmental Science & Technology 49, 6438–6447

[36] Liu, X., Song, Q., Tang, Y., Li, W., Xu, J., Wu, J., Wang, F., Brookes, P.C., 2013. Human health risk assessment of heavy metals in soil-vegetable system: A multi-medium analysis. Science of the Total Environment 463–464, 530–540

[37] Mani, D., Sharma, B., Kumar, C., Balak, S., 2012. Cadmium and lead bioaccumulation during growth stages alters sugar and vitamin C content in dietary vegetables. Proceedings of the National Academy of Sciences. India. Section B, Biological Sciences 82, 477–488

[38] Nacke, H., Thürmer, A., Wollherr, A., Will, C., Hodac, L., Herold, N., Schöning, I., Schrumpf, M., Daniel, R., 2011. Pyrosequencing-based assessment of bacterial community structure along different management types in German forest and grassland soils. PLoS One 6, e17000

[39] Narendrula-Kotha, R., Nkongolo, K.K., 2017. Bacterial and fungal community structure and diversity in a mining region under long-term metal exposure revealed by metagenomics sequencing. Ecological Genetics and Genomics 2, 13–24

[40] Roy, M., Mcdonald, L.M., 2015. Metal uptake in plants and health risk assessments in metal-contaminated smelter soils. Land Degradation & Development 26, 785–792

[41] Sánchez-Moreno, S., Navas, A., 2007. Nematode diversity and food web condition in heavy metal polluted soils in a river basin in southern Spain. European Journal of Soil Biology 43, 166–179

[42] Schneider, A.R., Gommeaux, M., Duclercq, J., Fanin, N., Conreux, A., Alahmad, A., Lacoux, J., Roger, D., Spicher, F., Ponthieu, M., Cancès, B., Morvan, X., Marin, B., 2017. Response of bacterial communities to Pb smelter pollution in contrasting soils. Science of the Total Environment 605–606, 436–444

[43] Shi, Z., Zhang, Z., Yuan, M., Wang, S., Yang, M., Yao, Q., Ba, W., Zhao, J., Xie, B., 2020. Characterization of a high cadmium accumulating soil bacterium, Cupriavidus sp. WS2. Chemosphere 247, 125834

[44] Siripornadulsil, S., Siripornadulsil, W., 2013. Cadmium-tolerant bacteria reduce the uptake of cadmium in rice: Potential for microbial bioremediation. Ecotoxicology and Environmental Safety 94, 94–103

[45] Solioz, M., Abicht, H.K., Mermod, M., Mancini, S., 2010. Response of Gram-positive bacteria to copper stress. Journal of Biological Inorganic Chemistry 15, 3–14

[46] Song, J., Shen, Q., Wang, L., Qiu, G., Shi, J., Xu, J., Brookes, P.C., Liu, X., 2018a. Effects of Cd, Cu, Zn and their combined action on microbial biomass and bacterial community structure. Environmental Pollution 243, 510–518

[47] Sun, C., Liu, J., Wang, Y., Sun, L., Yu, H., 2013. Multivariate and geostatistical analyses of the spatial distribution and sources of heavy metals in agricultural soil in Dehui, Northeast China. Chemosphere 92, 517–523

[48] Sun, Y., Zhao, L., Li, X., Xu, H., Weng, L., Yang, L., Li, Y., 2020. Response of soil bacterial and fungal community structure succession to earthworm addition for bioremediation of metolachlor. Ecotoxicology and Environmental Safety, 189, 109926.

[49] Sunda, W. G., Huntsman, S. A., 1998. Processes regulating cellular metal accumulation and physiological effects : Phytoplankton as model systems. Science of The Total Environment 219, 165–181.

[50] Tang, J., Zhang, J., Ren, L., Zhou, Y., Gao, J., Luo, L., Yang, Y., Peng, Q., Huang, H., Chen, A., 2019. Diagnosis of soil contamination using microbiological indices: A review on heavy metal pollution. Journal of Environmental Management 242, 121–130

[51] Teste, F.P., Kardol, P., Turner, B.L., Wardle, D.A., Zemunik, G., Renton, M., Laliberté, E., 2017. Plant-soil feedback and the maintenance of diversity in Mediterranean-climate shrublands. Science 355, 173–176

[52] Tian, P., Razavi, B. S., Zhang, X., Wang, Q., Blagodatskaya, E., 2020. Microbial growth and enzyme kinetics in rhizosphere hotspots are modulated by soil organics and nutrient availability. Soil Biology and Biochemistry 141, 107662.

[53] Vig, K., Megharaj, M., Sethunathan, N., Naidu, R., 2003. Bioavailability and toxicity of cadmium to microorganisms and their activities in soil: A review. Advances in Environmental Research 8, 121–135

[54] Wang, Q., Hou, J., Yuan, J., Wu, Y., Liu, W., Luo, Y., Christie, P., 2020. Evaluation of fatty acid derivatives in the remediation of aged PAH-contaminated soil and microbial community and degradation gene response. Chemosphere 248, 125983

[55] Wang, Y., Chen, C., Qian, Y., Zhao, X., Wang, Q., Kong, X., 2015. Toxicity of mixtures of λ-cyhalothrin, imidacloprid and cadmium on the earthworm Eisenia fetida by combination index (CI)-isobologram method. Ecotoxicology and Environmental Safety 111, 242–247

[56] Wang, Y.P., Shi, J.Y., Wang, H., Lin, Q., Chen, X.C., Chen, Y.X., 2007. The influence of soil heavy metals pollution on soil microbial biomass, enzyme activity, and community composition near a copper smelter. Ecotoxicology and Environmental Safety 67, 75–81

[57] Wenzel, W.W., 2009. Rhizosphere processes and management in plant-assisted bioremediation (phytoremediation) of soils. Plant and Soil 321, 385–408

[58] Will, C., Thürmer, A., Wollherr, A., Nacke, H., Herold, N., Schrumpf, M., Gutknecht, J., Wubet, T., Buscot, F., Daniell, R., 2010. Horizon-specific bacterial community composition of german grassland soils, as revealed by pyrosequencing-based analysis of 16S rRNA genes. Applied and Environmental Microbiology 76, 6751–6759

[59] Wyszkowska, J., Borowik, A., Kucharski, M., Kucharski, J., 2013. Effect of cadmium, copper and zinc on plants, soil microorganisms and soil enzymes. Journal of Elementology 18, 769–796

[60] Xie, L., Hao, P., Cheng, Y., Ahmed, I.M., Cao, F., 2018. Effect of combined application of lead, cadmium, chromium and copper on grain, leaf and stem heavy metal contents at different growth stages in rice. Ecotoxicology and Environmental Safety 162, 71–76

[61] Xie, W., Zhou, J., Wang, H., Chen, X., Lu, Z., Yu, J., Chen, X., 2009. Short-term effects of copper, cadmium and cypermethrin on dehydrogenase activity and microbial functional diversity in soils after long-term mineral or organic fertilization. Agriculture, Ecosystems & Environment 129, 450–456

[62] Xu, C., Peng, C., Sun, L., Zhang, S., Huang, H., Chen, Y., Shi, J., 2015. Distinctive effects of TiO₂ and CuO nanoparticles on soil microbes and their community structures in flooded paddy soil. Soil Biology & Biochemistry 86, 24–33

[63] Yan, C., Wang, F., Geng, H., Liu, H., Pu, S., Tian, Z., Chen, H., Zhou, B., Yuan, R., Yao, J., 2020. Integrating high-throughput sequencing and metagenome analysis to reveal the characteristic and resistance mechanism of microbial community in metal contaminated sediments. Science of the Total Environment 707, 136116

[64] Yang, W., Li, P., Rensing, C., Ni, W., Xing, S., 2019. Biomass, activity and structure of rhizosphere soil microbial community under different metallophytes in a mining site. Plant and Soil 434, 245–262

[65] Yu, P., Sun, Y., Huang, Z., Zhu, F., Sun, Y., Jiang, L., 2020. The effects of ectomycorrhizal fungi on heavy metals’ transport in Pinus massoniana and bacteria community in rhizosphere soil in mine tailing area. Journal of Hazardous Materials 381, 121203.

[66] Yuebing, S., Shunan, Z., Lin, W., Xuefeng, L., Yingming, X., 2020. Changes of enzymatic activities, substrate utilization pattern, and microbial community diversity in heavy metal-contaminated soils. Water, Air, and Soil Pollution 231, 422

[67] Zhang, Q., Zhang, L., Liu, T., Liu, B., Huang, D., Zhu, Q., Xu, C., 2018. The influence of liming on cadmium accumulation in rice grains via iron-reducing bacteria. Science of the Total Environment 645, 109–118

[68] Zhang, W., Chen, L., Zhang, R., Lin, K., 2016. High throughput sequencing analysis of the joint effects of BDE209-Pb on soil bacterial community structure. Journal of Hazardous Materials 301, 1–7

[69] Zhao, X., Huang, J., Lu, J., Sun, Y., 2019. Study on the influence of soil microbial community on the long-term heavy metal pollution of different land use types and depth layers in mine. Ecotoxicology and Environmental Safety 170, 218–226

[70] Zhao, Z.B., He, J.Z., Quan, Z., Wu, C.F., Sheng, R., Zhang, L.M., Geisen, S., 2020. Fertilization changes soil microbiome functioning, especially phagotrophic protists. Soil Biology & Biochemistry 148, 107863

[71] Zhou, J., Deng, Y., Luo, F., He, Z., Yanga, Y., 2011. Phylogenetic molecular ecological network of soil microbial communities in response to elevated CO₂. mBio 2, 1–8

[72] Zhou, Q., Guo, J.J., He, C.T., Shen, C., Huang, Y.Y., Chen, J.X., Guo, J.H., Yuan, J.G., Yang, Z.Y., 2016. Comparative transcriptome analysis between low- and high-cadmium-accumulating genotypes of pakchoi (Brassica chinensis L.) in response to cadmium stress. Environmental Science & Technology 50, 6485–6494

[73] Zia, M., Rizwan, M., Hussain, A., Saqib, M., Ali, S., Irfan, M., Sha, M., 2018. Alleviation of cadmium (Cd) toxicity and minimizing its uptake in wheat (Triticum aestivum) by using organic carbon sources in Cd- spiked soil. Environmental Pollution 241, 557–565

Authorship contribution

Qirui An: Performed the most of the experiments, writing-original draft. Yuyang Li: Performed the part of the experiments. Na Zheng: Funding acquisition, writing–review and editing, and supervision. Jincai Ma and Chunmei Zhao: Formal analysis, and supervision. Sujing Wang and Siyu Sun: Software. Pengyang Li: Formal analysis. Xiaoqian Li and Shengnan Hou: Conceptualization.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgment

The authors would like to acknowledge the support of the National Natural Science Foundation of China (41722110), the Leading Talents and Team Project of Scientific and Technological Innovation for young and Middle-aged Group in Jilin Province (20200301015RQ). the Major Special Program of Scientific and Technological of Jilin Province (20200503003SF), and the Research Fund Program of Guangdong Provincial Key Laboratory of Environmental Pollution Control and Remediation Technology (2020B1212060022).

RIGHTS & PERMISSIONS

2021 Higher Education Press