Abstract
A novel heavy metal resistant actinobacterial strain was isolated from an old lead and zinc mine in north-eastern Algeria. This strain was shown to resist high concentrations of heavy metals, including up to 500 ppm arsenic, 700 ppm cadmium, 1750 ppm chromium, 1250 ppm cobalt, 1000 ppm copper, 2750 ppm iron, 2750 ppm lead, 800 ppm mercury, 1750 ppm nickel, and 2750 ppm zinc. In addition, it was able to degrade dyes of the most used families, i.e., triphenylmethane (Malachite Green), azo (Ponceau S), and anthraquinone (Remazol Brilliant Blue R) dyes at 97.79%, 62.93%, and 39.41%, respectively. This bacterium was identified by sequencing the 16S rRNA encoding gene and affiliated to the genus Streptomyces by the RDP Naive Bayesian rDNA Classifier Version 2.11. The genome of Streptomyces sp. KY75 was sequenced using Illumina MiSeq and Oxford Nanopore. It was annotated by the MicroScope platform, and gene codings for resistance to heavy metals and dye biodecolorization were identified. It has a single linear chromosome with 7,837,660 bp and a GC content of 71.58%, 7509 of coding sequences (CDS), 66 tRNA genes, 18 rRNA genes, and 11 pseudogenes. The effect of hexavalent chromium on the dye biodegradation in liquid medium was also tested. Surprisingly, the dye biodegradation was not affected by the addition of hexavalent chromium. These observations make the actinobacterial strain Streptomyces sp. KY75 a good candidate for the bioremediation of textile dyeing industry effluents.
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Data Availability
The complete sequences of the Streptomyces sp. KY75 genome have been deposited in DDBJ/EMBL/GenBank under BioProject PRJEB40385 and assembly accession number GCA_904440645.1.
References
Ayed, L., Chaieb, K., Cheref, A., & Bakhrouf, A. (2010). Biodegradation and decolorization of triphenylmethane dyes by Staphylococcus epidermidis. Desalination, 260, 137–146. https://doi.org/10.1016/j.desal.2010.04.052
Basutkar, M., & Shivannavar, C. (2019). Decolorization study of reactive red-11 by using dye degrading bacterial strain Lysinibacillus boronitolerans CMGS-2. International Journal Of Current Microbiology And Applied Sciences, 8, 1135–1143. https://doi.org/10.20546/ijcmas.2019.806.140
Beitz, E. (2000). TeXshade: Shading and labeling of multiple sequence alignments using LaTeX2e. Bioinformatics, 16, 135–139. https://doi.org/10.1093/bioinformatics/16.2.135
Blümel, S., Knackmuss, H. J., & Stolz, A. (2002). Molecular cloning and characterization of the gene coding for the aerobic azoreductase from Xenophilus azovorans KF46F. Applied Environmental Microbiology, 68, 3948–3955. https://doi.org/10.1128/AEM.68.8.3948-3955.2002
Bürger, S., & Stolz, A. (2010). Characterisation of the flavin-free oxygen-tolerant azoreductase from Xenophilus azovorans KF46F in comparison to flavin-containing azoreductases. Applied Microbiology Biotechnology, 87, 2067–2076. https://doi.org/10.1007/s00253-010-2669-1
Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., & Madden, T. L. (2009). BLAST+: Architecture and applications. BMC Bioinformatics, 10, 421. https://doi.org/10.1186/1471-2105-10-421
Chauhan, A. K., & Choudhury, B. (2021). Synthetic dyes degradation using lignolytic enzymes produced from Halopiger aswanensis strain ABC_IITR by Solid State Fermentation. Chemosphere, 273, 129671. https://doi.org/10.1016/j.chemosphere.2021.129671
Chen, C., Shrestha, R., Jia, K., Gao, P. F., Geisbrecht, B. V., Bossmann, S. H., Shi, J., & Li, P. (2015). Characterization of dye-decolorizing peroxidase (DyP) from Thermomonospora curvata reveals unique catalytic properties of A-type DyPs. Journal of Biological Chemistry, 290, 23447–23463. https://doi.org/10.1074/jbc.M115.658807
Chéraiti, N., Plewniak, F., Tighidet, S., Sayeh, A., Gil, L., Malherbe, L., Memmi, Y., Zilliox, L., Vandecasteele, C., Boyer, P., Lopez-Roques, C., Jaulhac, B., Bensouilah, M., & Bertin, P. N. (2020). Complete genome sequence of Microbacterium sp. strain Nx66, isolated from waters contaminated with petrochemicals in El Saf-Saf Valley. Algeria. Microbiology Resource Announcements, 9, e01130-e1220. https://doi.org/10.1128/MRA.01130-20
Chittal, V., Gracias, M., Anu, A., Saha, P., & Rao, K. V. B. (2019). Biodecolorization and biodegradation of azo dye reactive orange-16 by marine Nocardiopsis sp. Iranian Journal of Biotechnology, 17, 18–26. https://doi.org/10.29252/ijb.1551
Desai, C., Jain, K., Patel, B., & Madamwar, D. (2009). Efficacy of bacterial consortium-AIE2 for contemporaneous Cr(VI) and azo dye bioremediation in batch and continuous bioreactor systems, monitoring steady-state bacterial dynamics using qPCR assays. Biodegradation, 20, 813–826. https://doi.org/10.1007/s10532-009-9269-8
Dewi, R. S., Ilyas, M., & Sari, A. A. (2019). Ligninolitic enzyme immobilization from Pleurotus ostreatus for dye and batik wastewater decolorization. Jurnal Pendidikan IPA Indonesia, 8, 220–229. https://doi.org/10.15294/jpii.v8i2.19372
Dubé, E., Shareck, F., Hurtubise, Y., Beauregard, M., & Daneault, C. (2008). Decolourization of recalcitrant dyes with a laccase from Streptomyces coelicolor under alkaline conditions. Journal Industrial Microbiology Biotechnology, 35, 1123–1129. https://doi.org/10.1007/s10295-008-0391-0
Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797. https://doi.org/10.1093/nar/gkh340
Fang, Z., Li, T., Wang, Q., Zhang, X., Peng, H., Fang, W., Hong, Y., Ge, H., & Xiao, Y. (2011). A bacterial laccase from marine microbial metagenome exhibiting chloride tolerance and dye decolorization ability. Applied Microbiology and Biotechnology, 89, 1103–1110. https://doi.org/10.1007/s00253-010-2934-3
Fillat, U., Prieto, A., Camarero, S., Martínez, Á. T., & Martínez, M. J. (2012). Biodeinking of flexographic inks by fungal laccases using synthetic and natural mediators. Biochemical Engineering Journal, 67, 97–103. https://doi.org/10.1016/j.bej.2012.05.010
Forootanfar, H., Moezzi, A., Aghaie-Khozani, M., Mahmoudjanlou, Y., Ameri, A., Niknejad, F., & Faramarzi, M. A. (2012). Synthetic dye decolorization by three sources of fungal laccase. Iranian Journal of Environmental Health Science and Engineering, 9, 1–10. https://doi.org/10.1186/1735-2746-9-27
Gao, F., Ding, H., Shao, L., Xu, X., & Zhao, Y. (2015). Molecular characterization of a novel thermal stable reductase capable of decoloration of both azo and triphenylmethane dyes. Applied Microbiology and Biotechnology, 99, 255–267. https://doi.org/10.1007/s00253-014-5896-z
Gianolini, J. E., Britos, C. N., Mulreedy, C. B., & Trelles, J. A. (2020). Hyperstabilization of a thermophile bacterial laccase and its application for industrial dyes degradation. 3 Biotech, 10, 1–7. https://doi.org/10.1007/s13205-020-02277-3
Gönen, F., & Aksu, Z. (2009). Single and binary dye and heavy metal bioaccumulation properties of Candida tropicalis: Use of response surface methodology (RSM) for the estimation of removal yields. Journal of Hazardous Materials, 172, 1512–1519. https://doi.org/10.1016/j.jhazmat.2009.08.021
Gupta, A., Nederlof, I., Sottini, S., Tepper, A. W. J. W., Groenen, E. J. J., Thomassen, E. A. J., & Canters, G. W. (2012). Involvement of Tyr108 in the Enzyme mechanism of the small laccase from Streptomyces coelicolor. Journal of the American Chemical Society, 134, 18213–18216. https://doi.org/10.1021/ja3088604
Harvey, D. J. (1982). Picolinyl esters as derivatives for the structural determination of long chain branched and unsaturated fatty acids. Biological Mass Spectrometry, 9, 33–38. https://doi.org/10.1002/bms.1200090107
Jain, C., Rodriguez-R, L. M., Phillippy, A. M., Konstantinidis, K. T., & Aluru, S. (2018). High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nature Communications, 9, 5114. https://doi.org/10.1038/s41467-018-07641-9
Jang, M. S., Lee, Y. M., Kim, C. H., Lee, J. H., Kang, D. W., Kim, S. J., & Lee, Y. C. (2005). Triphenylmethane reductase from Citrobacter sp. strain KCTC 18061P: Purification, characterization, gene cloning, and overexpression of a functional protein in Escherichia coli. Applied and Environmental Microbiology, 71, 7955–7960. https://doi.org/10.1128/AEM.71.12.7955-7960.2005
Ji, J., Kulshreshtha, S., Kakade, A., Majeed, S., Li, X., & Liu, P. (2020). Bioaugmentation of membrane bioreactor with Aeromonas hydrophila LZ-MG14 for enhanced malachite green and hexavalent chromium removal in textile wastewater. International Biodeterioration and Biodegradation, 150, 104939. https://doi.org/10.1016/j.ibiod.2020.104939
Khebizi, N., Boudjella, H., Bijani, C., Bouras, N., Klenk, H. P., Pont, F., Mathieu, F., & Sabaou, N. (2018). Oligomycins A and E, major bioactive secondary metabolites produced by Streptomyces sp. strain HG29 isolated from a Saharan soil. Journal of Medical Mycology, 28, 150–160. https://doi.org/10.1016/j.mycmed.2017.10.007
Kim, M. H., Kim, Y., Park, H. J., Lee, J. S., Kwak, S. N., Jung, W. H., Lee, S. G., Kim, D., Lee, Y. C., & Oh, T. K. (2008). Structural insight into bioremediation of triphenylmethane dyes by Citrobacter sp. triphenylmethane reductase. The Journal of Biological Chemistry, 283, 31981–31990. https://doi.org/10.1074/jbc.m804092200
Kumaran, S., Ngo, A. C. R., Schultes, F. P. J., & Tischler, D. (2020). Draft genome sequence of Kocuria indica DP-K7, a methyl red degrading actinobacterium. 3 Biotech, 10, 1–10. https://doi.org/10.1007/s13205-020-2136-3
Kuykendall, L. D., Roy, M. A., O’Neill, J. J., & Devine, T. E. (1988). Fatty acids, antibiotic resistance, and deoxyribonucleic acid homology groups of Bradyrhizobium japonicum. International Journal of Systematic and Evolutionary Microbiology, 38, 358–361. https://doi.org/10.1099/00207713-38-4-358
Larsson, A. (2014). AliView: A fast and lightweight alignment viewer and editor for large datasets. Bioinformatics, 30, 3276–3278. https://doi.org/10.1093/bioinformatics/btu531
Li, J., Liu, C., Li, B., Yuan, H., Yang, J., & Zheng, B. (2012). Identification and molecular characterization of a novel DyP-type peroxidase from Pseudomonas aeruginosa PKE117. Applied Biochemistry and Biotechnology, 166, 774–785. https://doi.org/10.1007/s12010-011-9466-x
Lončar, N., Colpa, D. I., & Fraaije, M. W. (2016). Exploring the biocatalytic potential of a DyP-type peroxidase by profiling the substrate acceptance of Thermobifida fusca DyP peroxidase. Tetrahedron, 72, 7276–7281. https://doi.org/10.1016/j.tet.2015.12.078
Majzlik, P., Strasky, A., Adam, V., et al. (2011). Influence of zinc(II) and copper(II) ions on Streptomyces bacteria revealed by electrochemistry. International Journal of Electrochemical Science, 6(6), 2171–2191.
Médigue, C., Calteau, A., Cruveiller, S., et al. (2019). MicroScope-An integrated resource for community expertise of gene functions and comparative analysis of microbial genomic and metabolic data. Briefings in Bioinformatics, 20, 1071–1084. https://doi.org/10.1093/bib/bbx113
Miller, L. T. (1982). Single derivatization method for routine analysis of bacterial whole-cell fatty acid methyl esters, including hydroxy acids. Journal of Clinical Microbiology, 16(3), 584–586.
Mishra, A., & Malik, A. (2013). Recent advances in microbial metal bioaccumulation. Critical Reviews in Environmental Science and Technology, 43, 1162–1222. https://doi.org/10.1080/10934529.2011.627044
Mishra, S., & Maiti, A. (2018). The efficacy of bacterial species to decolourise reactive azo, anthroquinone and triphenylmethane dyes from wastewater: A review. Environmental Science and Pollution Research International, 25, 8286–8314. https://doi.org/10.1007/s11356-018-1273-2
Moss, C. W., & Lambert-Fair, M. A. (1989). Location of double bonds in monounsaturated fatty acids of Campylobacter cryaerophila with dimethyl disulfide derivatives and combined gas chromatography-mass spectrometry. Journal of Clinical Microbiology, 27, 1467–1470. https://doi.org/10.1128/jcm.27.7.1467-1470.1989
Muller, D., Médigue, C., Koechler, S., et al. (2007). A tale of two oxidation states: Bacterial colonization of arsenic-rich environments. PLOS Genetics, 3, 0518–0530. https://doi.org/10.1371/journal.pgen.0030053
Myronovskyi, M., Tokovenko, B., Manderscheid, N., et al. (2013). Complete genome sequence of Streptomyces fulvissimus. Journal of Biotechnology, 168(1), 117–118. https://doi.org/10.1016/j.jbiotec.2013.08.013
Rahmanpour, R., Rea, D., Jamshidi, S., Fülöp, V., & Bugg, T. D. H. (2016). Structure of Thermobifida fusca DyP-type peroxidase and activity towards Kraft lignin and lignin model compounds. Archives of Biochemistry and Biophysics, 594, 54–60. https://doi.org/10.1016/j.abb.2016.02.019
Remenár, M., Karelová, E., Harichová, J., et al. (2014). Actinobacteria occurrence and their metabolic characteristics in the nickel-contaminated soil sample. Biology, 69, 1453–1463. https://doi.org/10.2478/s11756-014-0451-z
Roberts, J. N., Singh, R., Grigg, J. C., Murphy, M. E. P., Bugg, T. D. H., & Eltis, L. D. (2011). Characterization of Dye-Decolorizing Peroxidases from Rhodococcus jostii RHA1. Biochemistry, 50, 5108–5119. https://doi.org/10.1021/bi200427h
Santos, A., Mendes, S., Brissos, V., & Martins, L. O. (2014). New dye-decolorizing peroxidases from Bacillus subtilis and Pseudomonas putida MET94: Towards biotechnological applications. Applied Microbiology and Biotechnology, 98, 2053–2065. https://doi.org/10.1007/s00253-013-5041-4
Schlüter, A., Krahn, I., Kollin, F., Bönemann, G., Stiens, M., Szczepanowski, R., et al. (2007). IncP-1β plasmid pGNB1 isolated from a bacterial community from a wastewater treatment plant mediates decolorization of triphenylmethane dyes. Applied and Environmental Microbiology, 73, 6345–6350. https://doi.org/10.1128/AEM.01177-07
Shirling, E. B., & Gottlieb, D. (1966). Methods for characterization of Streptomyces species. International Journal of Systematic Bacteriology, 16(3), 313–340. https://doi.org/10.1099/00207713-16-3-313
Simões, M. F., Maiorano, A. E., Dos Santos, J. G., Peixoto, L., De Souza, R. F. B., Neto, A. O., et al. (2019). Microbial fuel cell-induced production of fungal laccase to degrade the anthraquinone dye Remazol Brilliant Blue R. Environmental Chemistry Letters, 17, 1413–1420. https://doi.org/10.1007/s10311-019-00876-y
Soraia, E. B., Mohamed, B., et al. (2015). Resistance to and accumulation of heavy metals by actinobacteria isolated from abandoned mining areas. The Scientific World Journal, 2015, 1–14. https://doi.org/10.1155/2015/761834
Spitzer, V. (1996). Structure analysis of fatty acids by gas chromatography - low resolution electron impact mass spectrometry of their 4,4-dimethyloxazoline derivatives - A review. Progress in Lipid Research, 35, 387–408. https://doi.org/10.1016/S0163-7827(96)00011-2
Sudha, M., Saranya, A., Selvakumar, G., & Sivakumar, N. (2014). Microbial degradation of azo dyes: A review. International Journal of Current Microbiology and Applied Sciences, 3, 670–690.
Suzuki, H. (2019). Remarkable diversification of bacterial azoreductases: Primary sequences, structures, substrates, physiological roles, and biotechnological applications. Applied Microbiology and Biotechnology, 103, 3965–3978. https://doi.org/10.1007/s00253-019-09775-2
Vignesh, A., Manigundan, K., Santhoshkumar, J., et al. (2020). Microbial degradation, spectral analysis and toxicological assessment of malachite green by Streptomyces chrestomyceticus S20. Bioprocess and Biosystems Engineering, 43, 1457–1468. https://doi.org/10.1007/s00449-020-02339-z
Yu, Q. T., Liu, B. N., Zhang, J. Y., & Huang, Z. H. (1989). Location of methyl branchings in fatty acids: Fatty acids in uropygial secretion of shanghai duck by GC-MS of 4,4-dimethyloxazoline derivatives. Lipids, 24, 160. https://doi.org/10.1007/BF02535256
Zubieta, C., Joseph, R., Sri Krishna, S., McMullan, D., Kapoor, M., Axelrod, H. L., et al. (2007). Identification and structural characterization of heme binding in a novel dye-decolorizing peroxidase, TyrA. Proteins, 69, 234–243. https://doi.org/10.1002/prot.21673
Adenan, N.H., Lim, Y.Y., & Ting, A.S.Y. (2021) Identification and optimization of triphenylmethane dyes removal by Streptomyces sp. from forest soil. Sustaining Environmental Resources, 31,8. https://doi.org/10.1186/s42834-021-00081-z
Baati, H., Siala, M., Azri, C., Ammar, E., Dunlap, C., & Trigui, M. (2020). Resistance of a Halobacterium salinarum isolate from a solar saltern to cadmium, lead, nickel, zinc, and copper. Antonie van Leeuwenhoek, https://doi.org/10.1007/s10482-020-01475-6
Bej, S., Mondal, A., & Banerjee, P. (2020) Effluent water Treatment: A potential way out towards conservation of fresh water in India. In Ghosh, S. K., Saha, P. D., Frances Di M Recent Trends in Waste Water Treatment and Water Resource Management. Springer Singapore. pp33–46. https://doi.org/10.1007/978-981-15-0706-9
R Core Team, (2020) R: A language and environment for statistical computing, Vienna, Austria: R Foundation for Statistical Computing.
Semai, A., Plewniak, F., Charrie ́-Duhaut, A. et al. (2021) Characterisation of hydrocarbon degradation, biosurfactant production, and biofilm formation in Serratia sp. Tan611: A new strain isolated from industrially contaminated environment in Algeria. Antonie Van Leeuwenhoek, https://doi.org/10.1007/s10482-021-01527-5
Telke, A. A., Kadam, A. A., Vinash, A., & Govindwar, S. P. (2015). Bacterial enzymes and their role in decolorization of azo dyes. In S. N. Singh (Ed.), Microbial degradation of synthetic dyes in wastewaters. Cham: Springer. pp. 149–168. https://doi.org/10.1007/978-3-319-10942-8
Funding
This work was supported by the DMO/DMA project funded by the national program EC2CO-MicrobiEn of CNRS (France) and Directorate-General of scientific research and technological development (Algeria). It was carried out in collaboration with the GeT core facility, Toulouse, France (http://get.genotoul.fr), and was supported by the national infrastructure France Génomique, funded under the program “'Investissement d’avenir'” managed by the Agence Nationale pour la Recherche (contract ANR-10- INBS-09). We thank the Genoscope (Evry, France) for the online access to MicroScope, the Microbial Genome Annotation and Analysis Platform (https://mage.genoscope.cns. fr/microscope/home/index.php).
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ST performed research and wrote the paper; FP performed research and wrote the paper, AS and LG performed research; CV contributed new methods; CL-R wrote the paper; MK analyzed data; PNB conceived study, analyzed data, and wrote the paper.
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Tighidet, S., Plewniak, F., Sayeh, A. et al. Dyes Biodegradation in the Presence of Hexavalent Chromium by Streptomyces sp. KY75: a Novel Heavy Metal Resistant Strain Isolated in Algeria. Water Air Soil Pollut 233, 285 (2022). https://doi.org/10.1007/s11270-022-05756-w
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DOI: https://doi.org/10.1007/s11270-022-05756-w