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Rhizosphere and Endophytic Bacteria Associated to Ocimum basilicum L. with Decaclorobiphenyl Removal Potential

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Abstract

Basil (Ocimum basilicum L.) is a hyperaccumulative herbaceous plant that has the ability to grow in contaminated soils and is believed to harbor a wide variety of bacterial species resistant to recalcitrant toxic chemical compounds. The objective of this work was to evaluate the potential for removal of decaclorobiphenyl PCB-209 by bacteria associated with the O. basilicum plant. A total of 34 endophytes and 52 strains from the rhizosphere of this plant were isolated using selective culture media. The adaptive capacity of the bacteria in phenol and Arochlor 1242 was initially determined and then a set of bacteria was selected and their removal potential of decachlorobiphenyl PCB-209 was evaluated. The phylogenetic analysis of 16S rRNA gene grouped to the O. basilicum isolates within bacterial genera Acinetobacter, Bacillus, Lysinibacillus, Novosphingobium, Pseudomonas, Rhizobium, Sphingobium, Stenotrophomonas, and Terribacillus as well as bacterial strains Pseudomonas taiwanensis BS-1, Rhizobium nepotum BS-2, Terribacillus sacharophilus BS-3, Stenotrophomonas rhizophila BS-4, Bacillus arybhattai BS-5, and Lysinibacillus macroides BS-6 showed the ability to adapt and use phenol and Arochlor 1242 as source of C. The strains BS-4 isolated from the root of the plant showed a higher potential from the removal of the PCB-209 (390.75 mg L−1) at an initial concentration of 500 mg L−1 and also had the ability to synthesize biosurfactant (EI = 60%) compared to the other strains evaluated. The diversity of bacteria associated to O. basilicum had biological qualities that may contribute to their adaptation and proliferation in an environment contaminated by PCB and be used efficiently as bioremediation to relieve agricultural soils contaminated by persistent organic compounds.

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References

  • Aguirre-De Cárcer, D., Martín, M., Mackova, M., Macek, T., Karlson, U., & Rivilla, R. (2007). The introduction of genetically modified microorganisms designed for rhizoremediation induces changes on native bacteria in the rhizosphere but not in the surrounding soil. ISME Journal, 1, 215–223.

    Google Scholar 

  • Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410.

    CAS  Google Scholar 

  • Anyasi, R. O., & Atagana, H. I. (2011). Biological remediation of polychlorinated biphenyls (PCB) in the environment by microorganisms and plants. African Journal of Biotechnology, 10, 18916–18938.

    CAS  Google Scholar 

  • Azaizeh, H., Castro, P. M. L., & Petra, K. (2011). Biodegradation of organic xenobiotic pollutants in the rhizosphere. Plant Ecophysiology, 8. https://doi.org/10.1007/978-90-481-9852-8_9.

  • Barea, J., Pozo, M., Azcón, R., & Azcón-Aguilar, C. (2005). Microbial co-operation in the rhizosphere. Journal of Experimental Botany, 56, 1761–1778.

    CAS  Google Scholar 

  • Becerra-Gutiérrez, L. K., & Horna-Acevedo, M. V. (2016). Aislamiento de microorganismos productores de biosurfactantes y lipasas a partir de efluentes residuales de camales y suelos contaminados con hidrocarburos. Scientia Agropecuaria, 7(1), 23–31.

    Google Scholar 

  • Bedard, D. L., Haberl, M. L., May, R. J., & Brennan, M. J. (1987). Evidence for novel mechanisms of polychlorinated biphenyl metabolism in Alcaligenes eutrophus H850. Applied and Environmental Ecology, 53(5), 1103–1112.

    CAS  Google Scholar 

  • Berendsen, R. L., Pieterse, C. M. J., & Bakker, P. A. H. M. (2012). The rhizosphere microbiome and plant health. Trends in Plant Science, 17(8), 478–486.

    CAS  Google Scholar 

  • Boonchan, S., Britz, M. L., & Stanley, G. A. (2000). Degradation and mineralization of high-molecular-weight polycyclic aromatic hydrocarbons by defined fungal-bacterial cocultures. Applied and Environmental Microbiology, 66(3), 1007–1019.

    CAS  Google Scholar 

  • Bruna, M., Carla, U., & Simona, R. (2016). Microbiome dynamics of a polychlorobiphenyl (PCB) historically contaminated marine sediment under conditions promoting reductive dechlorination. Frontiers in Microbiology, 7, 1502. https://doi.org/10.3389/fmicb.2016.01502.

    Article  Google Scholar 

  • Cameotra, S., & Makkar, R. (2010). Biosurfactante enhanced bioremediation of hydrophobic pollutants. Applied Chemistry, 1, 97–116.

    Google Scholar 

  • Chandankere, R., Yao, J., Choi, M., Masakorala, K., & Chan, Y. (2013). An efficient biosurfactant-producing and crude-oil emulsifying bacterium Bacillus methylotrophicus USTBa isolated from petroleum reservoir. Biochemical Engineering Journal, 74, 46–53.

    CAS  Google Scholar 

  • Costabeber, I., Sifuentes dos Santos, J., Odorissi, X. A. A., Weber, J., Leaes, F., Bogusz, S., & Emanuelli, T. (2006). Levels of polychlorinated biphenyls (PCBs) in meat and meat products from the state of Rio Grande do Sul, Brazil. Food and Chemical Toxicology, 44, 1–7.

    CAS  Google Scholar 

  • De la Rosa-Cruz, N. L., Sánchez-Salinas, E., & Ortiz-Hernández, M. L. (2014). Biosurfactantes y su papel en la biorremediación de suelos contaminados con plaguicidas. Revista Latinoamericana de Biotecnología Ambiental y Algal, 5, 47–67.

    Google Scholar 

  • Dercová, K., Murínová, S., Dudášová, H., Lászlová, K., & Horváthová, H. (2018). The adaptation mechanisms of bacteria applied in bioremediation of hydrophobic toxic environmental pollutants: how indigenous and introduced bacteria can respond to persistent organic pollutants-induced stress? IntechOpen. https://doi.org/10.5772/intechopen.79646.

  • Etesami, H., & Maheshwarib, D. K. (2018). Use of plant growth promoting rhizobacteria (PGPRs) with multiple plant growth promoting traits in stress agriculture: action mechanisms and future prospects. Ecotoxicology and Environmental Safety, 156, 225–246.

    CAS  Google Scholar 

  • Fedi, S., Tremaroli, V., Scala, D., Perez-Jimenez, J. R., Fava, F., Young, L., & Zannoni, D. (2005). T-RFLP analysis of bacterial communities in cyclodextrin-amended bioreactors developed for biodegradation of polychlorinated biphenyls. Research in Microbiology, 156, 201–210.

    CAS  Google Scholar 

  • Garrido-Sanz, D., Manzano, J., Martín, M., Redondo-Nieto, M., & Rivilla, R. (2018). Metagenomic analysis of a biphenyl degrading soil bacterial consortium reveals the metabolic roles of specific populations. Frontiers in Microbiology, 9, 232.

    Google Scholar 

  • Guanyu, Z., & Wong, J. W. C. (2010). Application of microemulsion to remediate organochlorine pesticides contaminated soils. Water and Energy, 15, 22–35.

    Google Scholar 

  • Han, X., O’Connor, J. C., Donner, E. M., Nabb, D. L., Mingoia, R. T., Snajdr, S. I., Clarke, J. J., & Kaplan, A. M. (2009). Noncoplanar 2,2′, 3,3′, 4,4′, 5,5′, 6,6′-decachlorobiphenyl (PCB 209) did not induce cytochrome P450 enzyme activities in primary cultured rat hepatocytes, was not genotoxic, and did not exhibit endocrine-modulating activities. Toxicology, 255, 177–186.

    CAS  Google Scholar 

  • Hatamian-Zarmi, A., Shojaosadati, S. A., Vasheghani-Farahani, E., Hosseinkhani, S., & Emamzadeh, A. (2009). Extensive biodegradation of highly chlorinated biphenyl and Aroclor 1242 by Pseudomonas aeruginosa TMU56 isolated from contaminated soils. International Biodeterioration & Biodegradation, 63, 788–794.

    CAS  Google Scholar 

  • Horváthová, H., Lászlová, K., & Dercová, K. (2018). Bioremediation of PCB-contaminated shallow river sediments: the efficacy of biodegradation using individual bacterial strains and their consortia. Chemosphere, 11, 012. https://doi.org/10.1016/j.chemosphere.2017.11.012.

    Article  CAS  Google Scholar 

  • Huang, L., Su, G., Liu, Y., Li, L., Liu, S., Lu, H., & Zheng, M. (2014). Effect of NiFe2O4 on PCDF by products formation during termal degradation of decachlorobiphenyl. RSC Advances Home, 4, 25453–25460.

    CAS  Google Scholar 

  • Jianjun, S., Xurun, Y., Jing, Z., Ai-sheng, X., & Fei, X. (2016). Regional analysis of potential polychlorinated biphenyl degrading bacterial strains from China. Brazilian Journal of Microbiology, 47, 536–541.

    Google Scholar 

  • Kim, I., Lee, H., & Trevors, J. (2001). Effects of 2, 2′, 5, 5′-tetrachlorobiphenyl and biphenyl a cell membranes of Ralstonia eutropha H850. FEMS Microbiology Letters, 200, 17–24.

    CAS  Google Scholar 

  • Koubek, J., Mackova, M., Macek, T., & Uhlik, O. (2013). Diversity of chlorobiphenyl-metabolizing bacteria and their biphenyl dioxygenases in contaminated sediment. Chemosphere, 93, 1548–1555.

    CAS  Google Scholar 

  • Kriti, K., & Fulekar, M. (2013). Rhizoremediation of pesticides: mechanism of microbial interaction in mycorrhizosphere. International Journal of Advancements in Research & Technology, 2(7), 2278–7763.

    Google Scholar 

  • Kuiper, I., Lagendijk, E., Bloemberg, G., & Lugtenberg, B. (2004). Rhizoremediation: a beneficial plant microbe interaction. Molecular Plant-Microbe Interactions, 17, 6–15.

    CAS  Google Scholar 

  • Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., Mc Gettigan, P. A., Mc William, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., & Higgins, D. G. (2007). Clustal Wand Clustal X version 2.0. Bioinformatics, 23, 2947–2948.

    CAS  Google Scholar 

  • López-López, A., Rogel, M. A., Ormeno-Orrillo, E., Martínez-Romero, J., & Martínez-Romero, E. (2010). Phaseolus vulgaris seed-borne endophytic community with novel bacterial species such as Rhizobium endophyticum sp. nov. Systematic and Applied Microbiology, 33, 322–327.

    Google Scholar 

  • Mrozik, A., Cycoń, M., & Piotrowska-Seget, Z. (2010). Changes of FAME profiles as a marker of phenol degradation in different soils inoculated with Pseudomonas sp. CF600. International Biodeterioration & Biodegradation, 64, 86–96.

    CAS  Google Scholar 

  • Nagata, Y., Endo, R., Ito, M., Ohtsubo, Y., & Tsuda, M. (2007). Aerobic degradation of lindane (γ-hexachlorocyclohexane) in bacteria and its biochemical and molecular basis. Applied Microbiology and Biotechnology, 76, 741–752.

    CAS  Google Scholar 

  • Nurzyńska-Wierdak, R., Rożek, E., Dzida, K., & Borowski, B. (2012). Growth response to nitrogen and potassium fertilization of common basil (Ocimum basilicum L.) plants. Hortorum Cultus, 11, 275–288.

    Google Scholar 

  • Peng, Y. H., Chen, Y. J., Chang, Y. J., & Shih, Y. (2015). Biodegradation of bisphenol A with diverse microorganisms from river sediment. Journal of Hazardous Materials, 286, 285–290.

    CAS  Google Scholar 

  • Pereira, P., Nesci, A., & Etcheverry, M. G. (2009). Analysis of the bacterial seed treatments for the control of Fusarium verticillioides in maize. Biocontrol, 54, 109–111.

    Google Scholar 

  • Pilon-Smits, E. (2005). Phytoremediation. Annual Review of Plant Biology, 56, 15–39.

    CAS  Google Scholar 

  • Polak, M. L., Zlatic, E., Demšar, L., Zlender, B., & Polak, T. (2016). Degradation of PCBs in dry fermented sausages during drying/ripening. Food Chemistry, 213, 246–250.

    Google Scholar 

  • Qiu, L., Wang, H., & Wang, X. (2016). Isolation and characterization of a cold-resistant PCB 209-degrading bacterial strain from river sediment and its application in bioremediation of contaminated soil. Journal of Environmental Science and Health A, 0, 1–9.

    Google Scholar 

  • Ramírez-Sandoval, M., Melchor-Partida, G. N., Muñiz-Hernández, S., Girón-Pérez, M. I., Rojas-García, A. E., Medina-Díaz, I. M., Robledo-Marenco, M. L., & Velázquez-Fernández, J. B. (2011). Phytoremediatory effect and growth of two species of Ocimum in endosulfan polluted soil. Journal of Hazardous Materials., 192, 388–392.

    Google Scholar 

  • Robson, A., Benedict, C., Márcio, R., Leandro, B., George, W., & Flávio, A. (2010). Bacterial stimulation of copper phytoaccumulation by bioaugmentation with rhizosphere bacteria. Chemosphere, 81, 1149–1154.

    Google Scholar 

  • Schafer, J. R., Hallett, S. G., & Johnson, W. G. (2014). Rhizosphere microbial community dynamics in glyphosate-treated susceptible and resistant biotypes of giant ragweed (Ambrosia trifida). Weed Science, 62, 370–381.

    CAS  Google Scholar 

  • Shahaliyan, F., Safahieh, A., & Abyar, H. (2015). Evaluation of emulsification index in marine bacteria Pseudomonas sp. and Bacillus sp. Arabian Journal for Science and Engineering, 40(7), 1849–1854.

    CAS  Google Scholar 

  • She, J., Holden, A., Sharp, M., Tañer, M., Williams, C., & Hooper, K. (2007). Polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) in breast milk from the pacific northwest. Chemosphere, 67, S307–S317.

    CAS  Google Scholar 

  • Tamura, K., & Nei, M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10, 512–526.

    CAS  Google Scholar 

  • Tharakan, J., Tomlinson, D., Addagada, A., & Shafagati, A. (2006). Biotransformation of PCBs in contaminated sludge: potential for novel biological technologies. Engineering in Life Sciences, 6, 43–50.

    CAS  Google Scholar 

  • Umeoguaju, U., Ononamadu, C., Okonkwo, M., & Ezeigwe, O. (2016). The survival of four tropical plants on soil artificially polluted with toxic levels of zinc. International Journal of Science Environment and Technology, 5(1), 17–24.

    Google Scholar 

  • Valenzuela-Encinas, C., Neria-González, I., Alcántara-Hernández, R. J., Enríquez-Aragón, J. A., Estrada-Alvarado, I., Hernández-Rodríguez, C., Dendooven, L., & Marsch, R. (2009). Phylogenetic analysis of the archaeal community in an alkaline-saline soil of the former Lake Texcoco (Mexico). Extremophiles, 12, 247–254.

    Google Scholar 

  • Vergani, L., Mapelli, F., Zanardini, E., Terzaghi, E., Di Guardo, A., Morosini, C., Raspa, G., & Borin, S. (2017). Phyto-rhizoremediation of polychlorinated biphenyl contaminated soils: an outlook on plant-microbe beneficial interactions. Science of the Total Environment, 575, 1395–1406.

    CAS  Google Scholar 

  • Verma, S. K., Trivedi, P., Gupta, A. K, & Verma, R. K. (2017). Aromatic plant–microbe associations: a sustainable approach for remediation of polluted soils. In: J.S. Singh, G. Seneviratne (eds.), Agroenvironmental sustainability, DOI https://doi.org/10.1007/978-3-319-49727-3_5, pp: 85–103. Springer International Publishing AG.

  • Vidali, M. (2001). Bioremediation an overview. Pure and Applied Chemistry, 73, 1163–1172.

    CAS  Google Scholar 

  • Villalobos-Maldonado, J. J., Meza-Gordillo, R., Mancilla-Margalli, N. A., Ayora Talavera, T. R., Rodríguez-Mendiola, M. A., Arias-Castro, C., & Ruiz-Valdiviezo, V. M. (2015). Removal of decachlorobiphenyl in vermicomposting process amended with rabbit manure and peat moss. Water Air & Soil Pollution, 226, 159. https://doi.org/10.1007/s11270-015-2400-z.

    Article  CAS  Google Scholar 

  • Weisburg, W. G., Barns, S. M., Pelletier, D. A., & Lane, D. J. (1991). 16S ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology, 73, 697–703.

    Google Scholar 

  • Yuanyuan, S., Yu, J., Chunrong, L., Pingping, J., Wenke, W., Yuan, Z., & Daniel, N. (2018). Effects of phytoremediation treatment on bacterial community structure and diversity in different petroleum-contaminated soils. International Journal of Environmental Research and Public Health, 15, 2168.

    Google Scholar 

  • Zenteno-Rojas, A., Martínez-Romero, E., Rincón-Molina, C. I., Ruíz-Valdiviezo, V. M., Meza-Gordillo, R., Villalobos-Maldonado, J. J., & Rincón-Rosales, R. (2019). Removal of high concentrations decachlorobiphenyl of earthworm Eisenia fetida and its symbiotic bacteria in a vermicomposting system. Water Air & Soil Pollution, 230, 116. https://doi.org/10.1007/s11270-019-4170-5.

    Article  CAS  Google Scholar 

  • Zhao, L., Hou, H., Shimoda, K., Terada, A., & Hosomi, M. (2012). Formation pathways of polychlorinated dibenzofurans (PCDFs) in sediments contaminated with PCBs during the thermal desorption process. Chemosphere, 88, 1368–1374.

    CAS  Google Scholar 

  • Zhou, Q., Cai, Z., Zhang, Z., & Liu, W. (2011). Ecological remediation of hydrocarbon contaminated soils with weed plant. Journal of Resources and Ecology, 2(2), 97–105.

    Google Scholar 

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Acknowledgments

We thank Posgrado of Ingenieria Bioquimica-ITTG and CONAcyT for a fellowship to Blanca Nelly Sanchez-Perez. We thank Nestor H. Cruz Perez for the technical assistance. We also thank Phillip Medina Barrios for reading this manuscript.

Funding

The work received financial support from the Tecnológico Nacional de México 6841.18-P.

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Authors and Affiliations

  1. Tecnológico Nacional de México, IT de Tuxtla Gutiérrez, Carretera Panamericana Km. 1080, 29050, Tuxtla Gutiérrez, Chiapas, Mexico

    Blanca Nelly Sánchez-Pérez, Adalberto Zenteno-Rojas, Clara Ivette Rincón-Molina, Víctor Manuel Ruíz-Valdiviezo, Federico Antonio Gutiérrez-Miceli, Juan José Villalobos-Maldonado & Reiner Rincón-Rosales

  2. Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Av. Universidad s/n, Col. Chamilpa, 62210, Cuernavaca, Morelos, Mexico

    Miguel Angel Vences-Guzmán

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  1. Blanca Nelly Sánchez-Pérez
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Sánchez-Pérez, B.N., Zenteno-Rojas, A., Rincón-Molina, C.I. et al. Rhizosphere and Endophytic Bacteria Associated to Ocimum basilicum L. with Decaclorobiphenyl Removal Potential. Water Air Soil Pollut 231, 134 (2020). https://doi.org/10.1007/s11270-020-04481-6

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