Soil-derived microbiota associated with plant roots are conducive to plant growth and stress resistance. However, the spatio-temporal dynamics of microbiota in response to organochlorine pollution during the unstable vegetative growth phase of rice is not well understood. In this study, we focused on the rice (Oryza sativa L.) microbiota across the bulk soil, rhizosphere and endosphere compartments during the vegetative growth phase in two different soils with and without lindane pollutant. The results showed that the factors of growth time, soil types and rhizo-compartments had significant influence on the microbial communities of rice, while lindane mostly stimulated the construction of endosphere microbiota at the vegetative phase. Active rice root-soil-microbe interactions induced an inhibition effect on lindane removal at the later vegetative growth phase in rice-growth-dependent anaerobic condition, likely due to the root oxygen loss and microbial mediated co-occurring competitive electron-consuming redox processes in soils. Each rhizo-compartment owned distinct microbial communities, and therefore, presented specific ecologically functional categories, while the moderate functional differences were also affected by plants species and residual pollution stress. This work revealed the underground micro-ecological process of microbiota and especially their potential linkage to the natural attenuation of residual organochlorine such as lindane.
Asshauer, K.P., Wemheuer, B., Daniel, R., Meinicke, P., 2015. Tax4Fun: predicting functional profiles from metagenomic 16S rRNA data. Bioinformatics (Oxford, England) 31, 2882–2884.
Benjamini, Y., Hochberg, Y., 1995. Controlling the false discovery ratea practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series A, (Statistics in Society) 57, 289–300.
Bulgarelli, D., Rott, M., Schlaeppi, K., Ver Loren Van Themaat, E., Ahmadinejad, N., Assenza, F., Rauf, P., Huettel, B., Reinhardt, R., Schmelzer, E., Peplies, J., Gloeckner, F.O., Amann, R., Eickhorst, T., Schulze-Lefert, P., 2012. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488, 91–95.
Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Pena, A.G., Goodrich, J.K., Gordon, J.I., Huttley, G.A., Kelley, S.T., Knights, D., Koenig, J.E., Ley, R.E., Lozupone, C.A., McDonald, D., Muegge, B.D., Pirrung, M., Reeder, J., Sevinsky, J.R., Tumbaugh, P.J., Walters, W.A., Widmann, J., Yatsunenko, T., Zaneveld, J., Knight, R., 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7, 335–336.
Castrillo, G., Teixeira, P.J.P.L., Paredes, S.H., Law, T.F., de Lorenzo, L., Feltcher, M.E., Finkel, O.M., Breakfield, N.W., Mieczkowski, P., Jones, C.D., Paz-Ares, J., Dangl, J.L., 2017. Root microbiota drive direct integration of phosphate stress and immunity. Nature 543, 513–518.
Chaparro, J.M., Badri, D.V., Vivanco, J.M., 2014. Rhizosphere microbiome assemblage is affected by plant development. ISME Journal 8, 790–803.
Chen, L., Ran, Y., Xing, B., Mai, B., He, J., We, X., Fu, J., Sheng, G., 2015. Content and source of polycyclic aromatic hydrocarbons and organochlorine pesticides in vegetable soils of Guangzhou, China. Chemosphere 60, 879–890.
Chen, X., Wu, Y., Huang, X., Lü, H., Zhao, H., Mo, C., Li, H., Cai, Q., Wong, M., 2018. Variations in microbial community and di-(2-ethylhexyl) phthalate (DEHP) dissipation in different rhizospheric compartments between low- and high-DEHP accumulating cultivars of rice (Oryza sativa L.). Ecotoxicology and Environmental Safety 163, 567–576.
Chouychai, W., Kruatrachue, M., Lee, H., 2015. Effect of plant growth regulators on phytoremediation of hexachlorocyclohexane-contaminated soil. International Journal of Phytoremediation 17, 1053–1059.
Dai, Z.M., Su, W.Q., Chen, H.H., Albert, B., Zhao, H.C., Yu, M.J., Yu, L., Philip, C.B., Christopher, W.S., Scott, X.C., Xu, J.M., 2018. Long-term nitrogen fertilization decreases bacterial diversity and favors the growth of Actinobacteria and Proteobacteria in agroecosystems across the globe. Global Change Biology 24, 3452–3461.
Deng, Y., Jiang, Y.H., Yang, Y., He, Z., Luo, F., Zhou, J., 2012. Molecular ecological network analyses. BMC Bioinformatics 13, 113.
Edwards, J., Johnson, C., Santos-Medellín, C., Lurie, E., Podishetty, N.K., Bhatnagar, S., Eisen, J.A., Sundaresan, V., 2015. Structure, variation, and assembly of the root-associated microbiomes of rice. Proceedings of the National Academy of Sciences of the United States of America 112, E911–E920.
Edwards, J.A., Santos-Medellín, C.M., Liechty, Z.S., Nguyen, B., Lurie, E., Eason, S., Phillips, G., Sundaresan, V., 2018. Compositional shifts in root-associated bacterial and archaeal microbiota track the plant life cycle in field-grown rice. PLoS Biology 16, e2003862.
Feng, J.Y., Shentu, J., Zhu, Y.J., Tang, C.X., He, Y., Xu, J.M., 2020a. Crop-dependent root-microbe-soil interactions induce contrasting natural attenuation of organochlorine lindane in soils. Environmental Pollution 257, 113580.
Feng, J.Y., Xu, Y., Ma, B., Tang, C.X., Brookes, P.C., He, Y., Xu, J.M., 2019. Assembly of root-associated microbiomes of typical rice cultivars in response to lindane pollution. Environment International 131, 104975.
Feng, J.Y., Zhu, Y.J., Shentu, J., Lu, Z.J., He, Y., Xu, J.M., 2020. 2020b. Pollution adaptive responses of root-associated microbiomes induced the promoted but different attenuation of soil residual lindane. Science of the Total Environment 732, 139170.
Fierer, N., Bradford, M.A., Jackson, R.B., 2007. Toward an ecological classification of soil bacteria. Ecology 6, 1354–1364.
Hayat, T., Ding, N., Ma, B., He, Y., Shi, J., Xu, J., 2011. Dissipation of pentachlorophenol in the aerobic-anaerobic interfaces established by the rhizosphere of rice (L.) root. Journal of Environmental Quality 40, 1722–1729.
Hua, X., Shan, Z., 1996. The production and application of pesticides and factor analysis of their pollution in China. Advances in Environmental Sciences 4, 33–45.
Kögel-Knabner, I., Amelung, W., Cao, Z., Fiedler, S., Frenzel, P., Jahn, R., Kalbitz, K., Kölbl, A., Schloter, M., 2010. Biogeochemistry of paddy soils. Geoderma 157, 1–14.
Li, Y., Wang, X., 2013. Root-induced changes in radial oxygen loss, rhizosphere oxygen profile, and nitrification of two rice cultivars in Chinese red soil regions. Plant and Soil 365, 115–126.
Lundberg, D.S., Lebeis, S.L., Paredes, S.H., Yourstone, S., Gehring, J., Malfatti, S., Tremblay, J., Engelbrektson, A., Kunin, V., Rio, T.G.D., Edgar, R.C., Eickhorst, T., Ley, R.E., Hugenholtz, P., Tringe, S. G., Dangl, J.L., 2012. Defining the core Arabidopsis thaliana root microbiome. Nature 488, 86–90.
Luo, J., Tao, Q., Wu, K., Li, J., Qian, J., Liang, Y., Yang, X., Li, T., 2017. Structural and functional variability in root-associated bacterial microbiomes of Cd/Zn hyperaccumulator Sedum alfredii. Applied Microbiology and Biotechnology 101, 7961–7976.
Niu, L., Xu, C., Yao, Y., Liu, K., Yang, F., Tang, M., Liu, W., 2013. Status, influences and risk assessment of hexachlorocyclohexanes in agricultural soils across China. Environmental Science & Technology 47, 12140–12147.
Peperanney, C., Campbell, A.N., Koechli, C.N., Berthrong, S., Buckley, D.H., 2016. Unearthing the ecology of soil microorganisms using a high resolution DNA-SIP approach to explore cellulose and xylose metabolism in soil. Frontiers in Microbiology 7, 703.
Phillips, T.M., Seech, A.G., Lee, H., Trevors, J.T., 2005. Biodegradation of hexachlorocyclohexane (HCH) by microorganisms. Biodegradation 16, 363–392.
Poolpak, T., Pokethitiyook, P., Kruatrachue, M., Arjarasirikoon, U., Thanwaniwat, N., 2008. Residue analysis of organochlorine pesticides in the Mae Klong river of Central Thailand. Journal of Hazardous Materials 156, 230–239.
Rani, R., Usmani, Z., Gupta, P., Avantika, C., Aakankshya, D., Vipin, K., 2018. Effects of organochlorine pesticides on plant growth-promoting traits of phosphate-solubilizing rhizobacterium, Paeni-bacillus sp. IITISM08. Environmental Science and Pollution Research International 25, 5668–5680.
Robinson, M.D., McCarthy, D.J., Smyth, G.K., 2009. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics (Oxford, England) 26, 139–140.
Salam, J.A., Hatha, M.A.A., Das, N., 2017. Microbial-enhanced lindane removal by sugarcane (Saccharum officinarum) in doped soil-applications in phytoremediation and bioaugmentation. Journal of Environmental Management 193, 394–399.
Santos-Medellín, C., Edwards, J., Liechty, Z., Nguyen, B., Sundaresan, V., 2017. Drought stress results in a compartment-specific restructuring of the rice root-associated microbiomes. mBio 8, e00764–e17.
Singha, L.P., Sinha, N., Pandey, P., 2018. Rhizoremediation prospects of polyaromatic hydrocarbon degrading rhizobacteria, that facilitate glutathione and glutathione-S-transferase mediated stress response, and enhance growth of rice plants in pyrene contaminated soil. Ecotoxicology and Environmental Safety 164, 579–588.
Su, Y., Zhu, Y., 2007. Transport mechanisms for the uptake of organic compounds by rice (Oryza sativa) roots. Environmental Pollution 148, 94–100.
Taiz, L., Murphy, A., 1995. Comparison of metallothionein cene expression and nonprotein thiols in ten Arabidopsis ecotypes. Plant Physiology 109, 945–954.
Tang, X., Zhang, R., Zhang, Q., Wang, W., 2016. Dehydrochlorination mechanism of γ-hexachlorocyclohexane degraded by dehydrochlorinase LinA from Sphingomonas paucimobilis UT26. RSC Advances 6, 4183–4192.
Walters, W.A., Jin, Z., Youngblut, N., Wallace, J.G., Sutter, J., Zhang, W., González-Peña, A., Peiffer, J., Koren, O., Shi, Q., Knight, R., Glavina Del Rio, T., Tringe, S.G., Buckler, E.S., Dangl, J.L., Ley, R. E., 2018. Large-scale replicated field study of maize rhizosphere identifies heritable microbes. Proceedings of the National Academy of Sciences of the United States of America 115, 7368–7373.
Wang, M., Chen, A., Wong, M., Qiu, R., Cheng, H., Ye, Z., 2011. Cadmium accumulation in and tolerance of rice (Oryza sativa L.) varieties with different rates of radial oxygen loss. Environmental Pollution 159, 1730–1736.
Wu, C., Ye, Z., Li, H., Wu, S., Deng, D., Zhu, Y., Wong, M., 2012. Do radial oxygen loss and external aeration affect iron plaque formation and arsenic accumulation and speciation in rice? Journal of Experimental Botany 63, 2961–2970.
Xu, Y., Ge, Y., Song, J.X., Rensing, C., 2020b. Assembly of root-associated microbial community of typical rice cultivars in different soil types. Journal of Hazardous Materials 56, 249–260.
Xu, Y., He, Y., Zhang, Q., Xu, J., Crowley, D., 2015. Coupling between pentachlorophenol dechlorination and soil redox as revealed by stable carbon isotope, microbial community structure, and biogeochemical data. Environmental Science & Technology 49, 5425–5433.
Xu, Y., Liu, J.Q., Cai, W.S., Feng, J.Y., Lu, Z., Wang, H.Z., Franks, A. E., Tang, C.X., He, Y., Xu, J.M., 2020a. Dynamic processes in conjunction with microbial response to disclose the biochar effect on pentachlorophenol degradation under both aerobic and anaerobic conditions. Journal of Hazardous Materials 384, 121503.
Xu, Y., Xue, L., Ye, Q., Franks, A.E., Zhu, M., Feng, X., Xu, J., He, Y., 2018. Inhibitory effects of sulfate and nitrate reduction on reductive dechlorination of PCP in a flooded paddy soil. Frontiers in Microbiology 9, 9.
Xue, L., Feng, X., Xu, Y., Li, X., Zhu, M., Xu, J., He, Y., 2017. The dechlorination of pentachlorophenol under a sulfate and iron reduction co-occurring anaerobic environment. Chemosphere 182, 166–173.
Zecchin, S., Corsini, A., Martin, M., Romani, M., Beone, G.M., Zanchi, R., Zanzo, E., Tenni, D., Fontanella, M.C., Cavalca, L., 2017. Rhizospheric iron and arsenic bacteria affected by water regime: Implications for metalloid uptake by rice. Soil Biology & Biochemistry 106, 129–137.
Zhang, A., Liu, W., Yuan, H., Zhou, S., Su, Y., Li, Y., 2011. Spatial distribution of hexachlorocyclohexanes in agricultural soils in Zhejiang Province, China, and correlations with elevation and temperature. Environmental Science & Technology 45, 6303–6308.
Zhang, J., Liu, Y., Zhang, N., Hu, B., Jin, T., Xu, H., Qin, Y., Yan, P., Zhang, X., Guo, X., Hui, J., Cao, S., Wang, X., Wang, C., Wang, H., Qu, B., Fan, G., Yuan, L., Garrido-Oter, R., Chu, C., Bai, Y., 2019. NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice. Nature Biotechnology 37, 676–684.
Zhang, J., Zhang, N., Liu, Y.X., Zhang, X., Hu, B., Qin, Y., Xu, H., Wang, H., Guo, X., Qian, J., Wang, W., Zhang, P., Jin, T., Chu, C., Bai, Y., 2018. Root microbiota shift in rice correlates with resident time in the field and developmental stage. Science China. Life Sciences 61, 613–621.
Zhou, X., Zhang, J., Pan, D., Ge, X., Jin, X., Chen, S., Wu, F., 2018. p-Coumaric can alter the composition of cucumber rhizosphere microbial communities and induce negative plant-microbial interactions. Biology and Fertility of Soils 54, 363–372.
Zhu, M., Zhang, L., Franks, A.E., Feng, X., Brookes, P.C., Xu, J., He, Y., 2019. Improved synergistic dechlorination of PCP in flooded soil microcosms with supplementary electron donors, as revealed by strengthened connections of functional microbial interactome. Soil Biology & Biochemistry 136, 107515.
This research was financially supported by the National Natural Science Foundation of China (41721001, 41771269), China Agriculture Research System (CARS-04), and the National Key Research and Development Program of China (2016YF-D0800207).
• Rice microbiota responded to lindane pollutant was studied spatiotemporally.
• Growth time, soil types and rhizo-compartments had significant influence.
• Lindane stimulated the endosphere micro-biota of rice which was highly dynamic.
• Root-soil-microbe interactions induced an inhibited redox-coupled lindane removal.
• This work was beneficial to better regulation of plant growth against adversity.
Eletronic Supplementary Material
Assembly and variation of root-associated microbiota of rice during their vegetative growth phase with and without lindane pollutant
Rights and permissions
About this article
Cite this article
Feng, J., Franks, A.E., Lu, Z. et al. Assembly and variation of root-associated microbiota of rice during their vegetative growth phase with and without lindane pollutant. Soil Ecol. Lett. 3, 207–219 (2021). https://doi.org/10.1007/s42832-020-0063-1
- Lindane pollutant
- Rice (Oryza sativa L.)
- Root-associated microbiota
- Root-microbe-soil interaction
- Vegetative growth phase
- Metagenome functions