Assessment of residual chlorine in soil microbial community using metagenomics

Yitian Yu, Qi Zhang, Zhenyan Zhang, Nuohan Xu, Yan Li, Mingkang Jin, Guoqiang Feng, Haifeng Qian, Tao Lu

PDF(1683 KB)
PDF(1683 KB)
Soil Ecology Letters ›› 2023, Vol. 5 ›› Issue (1) : 66-78. DOI: 10.1007/s42832-022-0130-x
RESEARCH ARTICLE
RESEARCH ARTICLE

Assessment of residual chlorine in soil microbial community using metagenomics

Author information +
History +

Highlights

• Continuous chlorine treatment have no obvious effect on soil microbial community structure and composition.

• Residual chlorine slightly affected soil microbial functions.

• Daily use of chlorine-containing disinfectants slightly threatened the soil ecosystem.

Abstract

Chlorine-containing disinfectants have been widely used around the world for the prevention and control of the COVID-19 pandemic. However, at present, little is known about the impact of residual chlorine on the soil micro-ecological environment. Herein, we treated an experimental soil-plant-microbiome microcosm system by continuous irrigation with a low concentration of chlorine-containing water, and then analyzed the influence on the soil microbial community using metagenomics. After 14-d continuous chlorine treatment, there were no significant lasting effect on soil microbial community diversity and composition either in the rhizosphere or in bulk soil. Although metabolic functions of the rhizosphere microbial community were affected slightly by continuous chlorine treatment, it recovered to the original status. The abundance of several resistance genes changed by 7 d and recovered by 14 d. According to our results, the chlorine residue resulting from daily disinfection may present a slight long-term effect on plant growth (shoot length and fresh weight) and soil micro-ecology. In general, our study assisted with environmental risk assessments relating to the application of chlorine-containing disinfectants and minimization of risks to the environment during disease control, such as COVID-19.

Graphical abstract

Keywords

Soil microbes / Chlorine-containing disinfectants / Plant microbiome / Metagenome / Sodium hypochlorite

Cite this article

Download citation ▾
Yitian Yu, Qi Zhang, Zhenyan Zhang, Nuohan Xu, Yan Li, Mingkang Jin, Guoqiang Feng, Haifeng Qian, Tao Lu. Assessment of residual chlorine in soil microbial community using metagenomics. Soil Ecology Letters, 2023, 5(1): 66‒78 https://doi.org/10.1007/s42832-022-0130-x

References

[1]
Baxi, N.N., 2013. Influence of ε-caprolactam on growth and physiology of environmental bacteria. Annals of Microbiology 63, 1471–1476
CrossRef Google scholar
[2]
Bogatcheva, E., Dubuisson, T., Protopopova, M., Einck, L., Nacy, C.A., Reddy, V.M., 2011. Chemical modification of capuramycins to enhance antibacterial activity. Journal of Antimicrobial Chemotherapy 66, 578–587
CrossRef Google scholar
[3]
Bolger, A.M., Lohse, M., Usadel, B., 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics (Oxford, England) 30, 2114–2120
CrossRef Google scholar
[4]
Bulgarelli, D., Rott, M., Schlaeppi, K., van Themaat, E.V.L., Ahmadinejad, N., Assenza, F., Rauf, P.,  Huettel, B.,  Reinhardt, R.,  E., Schmelzer, J., Peplies, F.O., Gloeckner, R., Amann, T., Eickhorst, P., Schulze-Lefert, 2012. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488, 91–95
CrossRef Google scholar
[5]
Chen, Q.L., An, X.L., Li, H., Su, J.Q., Ma, Y.B., Zhu, Y.G., 2016. Long-term field application of sewage sludge increases the abundance of antibiotic resistance genes in soil. Environment International 92–93, 1–10
CrossRef Google scholar
[6]
China Huanqiu Web, 2020.02.20. Implementation of urban sewer disinfection, Wuhan has put in a total of 1963.58 tons of disinfectants, https://china.huanqiu.com/article/9CaKrnKptOt.
[7]
Choi, H.Y., Lee, Y.H., Lim, C.H., Kim, Y.S., Lee, I.S., Jo, J.M., Lee, H.Y., Cha, H.G., Woo, H.J., Seo, D.S., 2020. Assessment of respiratory and systemic toxicity of Benzalkonium chloride following a 14-day inhalation study in rats. Particle and Fibre Toxicology 17, 5
CrossRef Google scholar
[8]
Chu, W., Fang, C., Deng, Y., Xu, Z., 2021. Intensified disinfection amid COVID-19 pandemic poses potential risks to water quality and safety. Environmental Science & Technology 55, 4084–4086
CrossRef Google scholar
[9]
Cui, Y.X., Wang, X., Wang, X.X., Zhang, X.C., Fang, L.C., 2021. Evaluation methods of heavy metal pollution in soils based on enzyme activities: A review. Soil Ecology Letters 3, 169–177
CrossRef Google scholar
[10]
Dixon, P., 2003. VEGAN, a package of R functions for community ecology. Journal of Vegetation Science 14, 927–930
CrossRef Google scholar
[11]
Duarte, R., Furtado, I., Sousa, L., Carvalho, C., 2020. The 2019 novel coronavirus (2019-nCoV): Novel virus, old challenges. Acta Medica Portuguesa 33, 33
CrossRef Google scholar
[12]
Feng, J.Y., Franks, A.E., Lu, Z.J., Xu, J.M., He, Y., 2021. Assembly and variation of root-associated microbiota of rice during their vegetative growth phase with and without lindane pollutant. Soil Ecology Letters 3, 207–219
CrossRef Google scholar
[13]
Fu, L.M., Niu, B.F., Zhu, Z.W., Wu, S.T., Li, W.Z., 2012. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics (Oxford, England) 28, 3150–3152
CrossRef Google scholar
[14]
Hao, F.Z., Li, J.S., Wang, Z., Li, Y.F., 2018. Influence of chlorine injection on soil enzyme activities and maize growth under drip irrigation with secondary sewage effluent. Irrigation Science 36, 363–379
CrossRef Google scholar
[15]
Hu, B., Liang, D.L., Liu, J.J., Xie, J.Y., 2013. Ecotoxicological effects of copper and selenium combined pollution on soil enzyme activities in planted and unplanted soils. Environmental Toxicology and Chemistry 32, 1109–1116
CrossRef Google scholar
[16]
Huang, Y.L., Zeng, Y.H., Feng, H., Wu, Y.H., Xu, X.W., 2015. Croceicoccus naphthovorans sp. nov., a polycyclic aromatic hydrocarbons-degrading and acylhomoserine-lactone-producing bacterium isolated from marine biofilm, and emended description of the genus Croceicoccus. International Journal of Systematic and Evolutionary Microbiology 65, 1531–1536
CrossRef Google scholar
[17]
Huson, D.H., Auch, A.F., Qi, J., Schuster, S.C., 2007. MEGAN analysis of metagenomic data. Genome Research 17, 377–386
CrossRef Google scholar
[18]
Krishnan, R., Menon, R.R., Likhitha, Busse, H.J., Tanaka, N., Krishnamurthi, S., Rameshkumar, N., 2017. Novosphingobium pokkalii sp. nov., a novel rhizosphere-associated bacterium with plant beneficial properties isolated from saline-tolerant pokkali rice. Research in Microbiology 168, 113–121
CrossRef Google scholar
[19]
Lee, Y., Jo, E., Lee, Y.J., Hettiaarachchi, S.A., Park, G.H., Lee, S.J., Heo, S.J., Kang, D.H., Oh, C., 2018. A novel glycosyl hydrolase family 16 β-agarase from the agar-utilizing marine bacterium Gilvimarinus agarilyticus JEA5: the first agarase molecular and biochemical characterization in the genus Gilvimarinus. Journal of Microbiology and Biotechnology 28, 776–783
CrossRef Google scholar
[20]
Li, D.H., Liu, C.M., Luo, R.B., Sadakane, K., Lam, T.W., 2015. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics (Oxford, England) 31, 1674–1676
CrossRef Google scholar
[21]
Li, P., Fan, X.Y., Qi, X.B., Fan, T., Zhao, Z.J., Zhao, X.F., 2013. Influence of soil residual nitrogen and coliforms in potato under alternate irrigation with chlorine reclaimed water. Chinese Agricultural Science Bulletin 29, 82–87.
[22]
Lonigro, A., Montemurro, N., Laera, G., 2017. Effects of residual disinfectant on soil and lettuce crop irrigated with chlorinated water. Science of the Total Environment 584, 595–602
CrossRef Google scholar
[23]
Lu, T., Ke, M.J., Lavoie, M., Jin, Y.J., Fan, X.J., Zhang, Z.Y., Fu, Z.W., Sun, L.W., Gillings, M., Penuelas, J., Qian, H., Zhu, Y.G., 2018. Rhizosphere microorganisms can influence the timing of plant flowering. Microbiome 6, 231
CrossRef Google scholar
[24]
Mendes, R., Garbeva, P., Raaijmakers, J.M., 2013. The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiology Reviews 37, 634–663
CrossRef Google scholar
[25]
Mincarelli, L., Vischetti, C., Craft, J., Tiano, L., 2016. DNA damage in different Eisenia andrei coelomocytes sub-populations after in vitro exposure to hydrogen peroxide. SpringerPlus 5, 1–7
CrossRef Google scholar
[26]
Miwa, N., Mitsuhashi, M., Kajiura, T., 2019. Screening of microorganisms producing a novel protein-asparaginase and characterization of the enzyme derived from Luteimicrobium album. Journal of Bioscience and Bioengineering 127, 281–287
CrossRef Google scholar
[27]
Murphy, R., Benndorf, R., de Beer, Z.W., Vollmers, J., Kaster, A.K., Beemelmanns, C., Poulsen, M., 2016. Comparative genomics reveals prophylactic and catabolic capabilities of actinobacteria within the fungus-farming termite symbiosis. MSphere 6, e01233–e20.
[28]
Olander, L.P., Vitousek, P.M., 2000. Regulation of soil phosphatase and chitinase activityby N and P availability. Biogeochemistry 49, 175–191
CrossRef Google scholar
[29]
Oleńska, E., Maek, W., Wójcik, M., Swiecicka, I., Vangronsveld, J., 2020. Beneficial features of plant growth-promoting rhizobacteria for improving plant growth and health in challenging conditions: A methodical review. Science of the Total Environment 743, 140682
CrossRef Google scholar
[30]
Podlena, A., 2009. Effect of fertilization on content and uptake of chlorine by oilseed rape under pot experiment conditions. Journal of Elementology 14, 773–778.
[31]
Qian, H.F., Hu, B.L., Wang, Z.Y., Xu, X., Hong, T., 2007. Effects of validamycin on some enzymatic activities in soil. Environmental Monitoring and Assessment 125, 1–8
CrossRef Google scholar
[32]
Qian, H.F., Zhang, Q., Lu, T., Peijnenburg, W.J.G.M., Josep, P., Zhu, Y.G., 2021. Lessons learned from COVID-19 on potentially pathogenic soil microorganisms. Soil Ecology Letters 3, 1–5
CrossRef Google scholar
[33]
Qu, Q., Zhang, Z.Y., Peijnenburg, W.J.G.M., Liu, W.Y., Lu, T., Hu, B.L., Chen, J., Chen, J., Lin, Z., Qian, H., 2020. Rhizosphere microbiome assembly and its impact on plant growth. Journal of Agricultural and Food Chemistry 68, 5024–5038
CrossRef Google scholar
[34]
Rangjaroen, C., Sungthong, R., Rerkasem, B., Teaumroong, N., Noisangiam, R., Lumyong, S., 2017. Untapped endophytic colonization and plant growth-promoting potential of the genus Novosphingobium to optimize rice cultivation. Microbes and Environments 32, 84–87
CrossRef Google scholar
[35]
Rueschhoff, E.E., 2009. Vitamin B6 metabolism in Arabidopsis thaliana. Dissertations & Theses-Gradworks, 3405145.
[36]
Shousei, K., Katsuhiko, F., 2018. Biochemical characteristics of cellulose and a green alga degradation by Gilvimarinus japonicas 12–2T, and its application potential for seaweed saccharification. Bioscience, Biotechnology, and Biochemistry 82, 1–7.
[37]
Subpiramaniyam, S., 2021. Outdoor disinfectant sprays for the prevention of COVID-19: Are they safe for the environment? Science of the Total Environment 759, 144289
CrossRef Google scholar
[38]
Sun, J.P., W, Z.H., Li, X.J., Ding, Y.F., Sun, H., Ping, W.L., 2017. Effect of high chlorine irrigation water on the chlorine absorption and distribution of potted flue-cured tobacco. Journal of Henan Agricultural Sciences 46, 44–48.
[39]
Truchado, P., Gil, M.I., Moreno-Candel, M., Allende, A., 2019. Impact of weather conditions, leaf age and irrigation water disinfection on the major epiphytic bacterial genera of baby spinach grown in an open field. Food Microbiology 78, 46–52
CrossRef Google scholar
[40]
Truchado, P., Gil, M.I., Suslow, T., Allende, A., Simon, V., 2018. Impact of chlorine dioxide disinfection of irrigation water on the epiphytic bacterial community of baby spinach and underlying soil. PLoS One 13, e0199291
CrossRef Google scholar
[41]
Wang, J., Zhang, B., Duan, H., Liang, C., Zhang, L., 2020. Key points of the program for disinfection technology in special places during the coronavirus disease-2019 (COVID-19) outbreak. China CDC Weekly 2, 140–142
CrossRef Google scholar
[42]
Wang, Y., Wang, X.J., Li, Y., Liu, Y.Y., Sun, Y., Xia, S.Q., Zhao, J.F., 2021. Effects of coexistence of tetracycline, copper and microplastics on the fate of antibiotic resistance genes in manured soil. Science of the Total Environment 790, 148087
CrossRef Google scholar
[43]
WHO, 2020a. WHO coronavirus disease (COVID-19) dashboard. https://covid19.who.int/.
[44]
WHO, 2020b. Water, sanitation, hygiene, and waste management for SARS-CoV-2, the virus that causes COVID-19. https://www.who.int/publications/i/item/water-sanitation-hygiene-and-waste-management-for-covid-19.
[45]
Yurkov, V., Stackebrandt, E., Holmes, A., Fuerst, J.A., Hugenholtz, P., Golecki, J., Gadon, N., Gorlenko, V.M., Kompantseva, E.I., Drews, G., 1994. Phylogenetic positions of novel aerobic, bacteriochlorophyll a-containing bacteria and description of Roseococcus thiosulfatophilus gen. nov., sp. nov., Erythromicrobium ramosum gen. nov., sp. nov., and Erythrobacter litoralis sp. nov. International Journal of Systematic and Evolutionary Microbiology 44, 427–434.
[46]
Zhang, J., Zhang, C.W., Lei, Z., Jiang, J.Q., Kim, S.G., 2016. Novosphingobium oryzae sp. nov., a potential plant-promoting endophytic bacterium isolated from rice roots. International Journal of Systematic and Evolutionary Microbiology 66, 302–307
CrossRef Google scholar
[47]
Zhang, Z., Zhang, Q., Lu, T., Zhang, J., Sun, L., Hu, B., Hu, J., Peñuelas, J., Zhu, L., Qian, H., 2021. Residual chlorine disrupts the microbial communities and spreads antibiotic resistance in freshwater. Journal of Hazardous Materials 423, 127152
CrossRef Google scholar
[48]
Zhu, B., Chen, Q., Chen, S., Zhu, Y.G., 2016. Does organically produced lettuce harbor higher abundance of antibiotic resistance genes than conventionally produced? Environment International 98, 152–159
CrossRef Google scholar
[49]
Ziegler, S., Waidner, B., Itoh, T., Schumann, P., Spring, S., Gescher, J., 2013. Metallibacterium scheffleri gen. nov., sp. nov., an alkalinizing gammaproteobacterium isolated from an acidic biofilm. International Journal of Systematic and Evolutionary Microbiology 63, 1499–1504
CrossRef Google scholar

Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (41907210, 71903079, 21976161, 21777144).

Electronic supplementary material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s42832-022-0130-x and is accessible for authorized users.

RIGHTS & PERMISSIONS

2022 Higher Education Press
AI Summary AI Mindmap
PDF(1683 KB)

Accesses

Citations

Detail

Sections
Recommended

/