This study was conducted to elucidate the inherent potential of Bacillus sp. MR-1/2, which was isolated from root zone of maize crop grown on a textile wastewater-irrigated soil. The isolated strain was identified through its ribosomal RNA sequence. Under in vitro conditions, the strain demonstrated its tolerance for high concentrations of various heavy metal ions as determined by minimum inhibitory concentration. Moreover, the strain MR-1/2 exhibited many important phytobeneficial traits such as inorganic P solubilization and 1-aminocyclopropane-1-carboxylate (ACC) deaminase ability even under high metal and salt stress. Results showed that the strain proficiently decolorizes various azo dye compounds, e.g., reactive black-5, reactive red-120, and direct blue-1 and congo red, in broth culture. The bioremediation potential of the strain MR-1/2 was further confirmed by analyzing the retrieved azoreductase gene sequence through bioinformatics tools, whereby a subsequent prediction revealed that the azoreductase enzyme activity was involved in decolorization process. When mung bean seeds were grown in pots under various concentrations of decolorized and non-decolorized azo dye, the Bacillus sp. MR-1/2 not only alleviated the azo dye toxicity, but also increased the plant growth parameters. In conclusion, the strain MR-1/2 efficiently decolorized the azo dyes and helped in mung bean plant growth by alleviating azo dye toxicity.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
Abbas N, Hussain S, Azeem F, Shahzad T, Bhatti SH, Imran M, Ahmad Z, Maqbool Z, Abid M (2016) Characterization of a slat resistant bacterial strain Proteus sp. NA6 capable of decolorizing reactive dyes in presence of multi-metal stress. World J Microbiol Biotechnol 32:181
Ahmed F, Arshad M, Ditta A, Hussain A, Naveed M, Hasnain M, Nazir Q (2016) Combining textile effluent wastewater with organic fertilizer for improved growth and productivity of wheat and soil health. J Environ Agric Sci 8:14–20
Akram MS, Shahid M, Tariq M, Azeem M, Javed MT, Saleem S, Riaz S (2016) Deciphering Staphylococcus sciuri SAT-17 mediated anti-oxidative defense mechanisms and growth modulations in salt stressed maize (Zea mays L.). Front Microbiol 7:867
Arif MS, Shahzad SM, Riaz M, Yasmeen T, Shahzad T, Akhtar MJ, Bragazza L, Buttler A (2017) Nitrogen-enriched compost application combined with plant growth-promoting rhizobacteria (PGPR) improves seed quality and nutrient use efficiency of sunflower. J Plant Nutr Soil Sci 180:464–473
Bashan Y, Puente ME, de Bashan LE, Hernandez JP (2008) Environmental uses of plant growth-promoting bacteria. Plant Microb Interact 661:69–93
Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350
Chacko JT, Subramaniam K (2011) Enzymatic degradation of azo dyes—a review. Int J Environ Sci 1:1250–1260
Chen Y, Feng L, Li H, Wang Y, Chen G, Zhang Q (2018) Biodegradation and detoxification of Direct Black G textile dye by a newly isolated thermophilic microflora. Bioresour Technol 250:650–657
Cui D, Kong FY, Liang B, Cheng HY, Liu D, Sun Q, Wang AJ (2011) Decolorization of azo dyes in dual-chamber biocatalyzed electrolysis systems seeding with enriched inoculum. J Environ Anal Toxicol 3:001
Ebency CL, Rajan S, Murugesan AG, Rajesh A, Elayarajah B (2013) Biodegradation of textile azo dyes and its bioremediation potential using seed germination efficiency. Int J Curr Microbiol Appl Sci 2:496–505
Götz S, Arnold R, Sebastián-León P, Martín-Rodríguez S, Tischler P, Jehl MA, Dopazo J, Rattei T, Conesa A (2011) B2G-FAR, a species-centered GO annotation repository. Bioinformatics 27(7): 919–924
Gordon SA, Weber RP (1951) Colorimetric estimation of indoleacetic acid. Plant Physiol 26:192–195
Heydarian Z, Gruber M, Glick BR, Hegedus DD (2018) Gene expression patterns in roots of Camelina sativa with enhanced salinity tolerance arising from inoculation of soil with plant growth promoting bacteria producing 1-aminocyclopropane-1-carboxylate deaminase or expression the corresponding acds gene. Front Microbiol 9:1297
Hilda R, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339
Hussain S, Maqbool Z, Ali S, Yasmeen T, Imran M, Mahmood F, Abbas F (2013) Biodecolorization of reactive black-5 by a metal and salt tolerant bacterial strain Pseudomonas sp. RA20 isolated from Paharang drain effluents in Pakistan. Ecotoxicol Environ Saf 98:331–338
Hussain S, Quinn L, Li J, Casey E, Murphy CD (2017) Simultaneous removal of malachite green and hexavalent chromium by Cunninghamella elegans biofilm in a semi-continuous system. Int Biodeterior Biodegrad 125:142–149
Imran M, Arshad M, Negm F, Khalid A, Shaharoona B, Hussain S, Nadeem SM, Crowley DE (2016a) Yeast extract promotes decolorization of azo dyes by stimulating azoreductase activity in Shewanella sp. strain IFN4. Ecotoxicol Environ Saf 124:42–49
Imran M, Negm F, Hussain S, Ashraf M, Ahmad Z, Arshad M, Crowley DE (2016b) Characterization and purification of membrane-bound azoreductase from azo dye degrading Shewanella sp. Strain IFN4. Clean Soil Air Water 44:1523–1530
Lade H, Kadam A, Paul D, Govindwar S (2015) Biodegradation and detoxification of textile azo dyes by bacterial consortium under sequential microaerophilic/aerobic processes. EXCLI J 14:158–174
Mahmood S, Khalid A, Mahmood T, Arshad M, Ahmad R (2013) Potential of newly isolated bacterial strains for simultaneous removal of hexavalent chromium and reactive black-5 azo dye from tannery effluent. J Chem Technol Biotechnol 88:1506–1513
Mahmood F, Shahid M, Hussain S, Shahzad T, Tahir M, Ijaz M, Hussain A, Mahmood K, Imran M, Babar SAK (2017) Potential plant growth-promoting strain Bacillus sp. SR-2-1/1 decolorized azo dyes through NADH-ubiquinone: oxidoreductase activity. Bioresour Technol 235:176–184
Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, New York, p 545
Maqbool Z, Hussain S, Ahmad T, Nadeem H, Imran M, Khalid A, Abid M, Martin-Laurent F (2016) Use of RSM modeling for optimizing decolorization of simulated textile wastewater by Pseudomonas aeruginosa strain ZM130 capable of simultaneous removal of reactive dyes and hexavalent chromium. Environ Sci Pollut Res 23:11224–11239
Murphy J, Riley JP (1962) Modified solution method for determination of phosphate in natural water. Anal Chim Acta 27:31–36
Najme R, Hussain S, Maqbool Z, Imran M, Mahmood F, Manzoor H, Yasmeen T, Shahzad T (2015) Biodecolorization of reactive yellow-2 by Serratia sp. RN34 isolated from textile wastewater. Water Environ Res 87:2065–2075
Nelson DW, Sommers L (1982) Total carbon, organic carbon, and organic matter 1. Methods of soil analysis. Part 2. Chemical and microbiological properties. American Society of Agronomy, Madison, pp 539–579
Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol Plant 118:10–15
Pradhan N, Sukla LB (2005) Solubilization of inorganic phosphates by fungi isolated from agriculture soil. Afr J Biotechnol 5:850–854
Rashid MI, Mujawar LH, Shahzad T, Almeelbi T, Ismail IMI, Oves M (2016) Bacteria and fungi can contribute to nutrients bioavailability and aggregate formation in degraded soils. Microbiol Res 183:26–24
Rathod J, Dhebar S, Archana G (2017) Efficient approach to enhance whole cell azo dye decolorization by heterologous overexpression of Enterococcus sp. L2 azoreductase (azoA) and Mycobacterium vaccae formate dehydrogenase (fdh) in different bacterial systems. Int Biodeterior Biodegrad 124:91–100
Saratale RG, Gandhi SS, Purankar MV, Kurade MB, Govindwar SP, Oh SE, Saratale GD (2013) Decolorization and detoxification of sulfonated azo dye CI Remazol Red and textile effluent by isolated Lysinibacillus sp. RGS J Biosci Bioeng 115:658–667
Shahid M, Hameed S, Tariq M, Zafar M, Ali A, Ahmad N (2015) Characterization of mineral phosphate-solubilizing bacteria for enhanced sunflower growth and yield-attributing traits. Ann Microbiol 65:1525–1536
Shahid M, Hussain B, Riaz D, Khurshid M, Ismail M, Tariq M (2017) Identification and partial characterization of potential probiotic lactic acid bacteria in freshwater Labeo rohita and Cirrhinus mrigala. Aquac Res 48:1688–1698
Shinwari KI, Shah AU, Afridi MI, Zeeshan M, Hussain H, Hussain J, Ahmad O (2015) Application of plant growth promoting rhizobacteria in bioremediation of heavy metal polluted soil. Asian J Multidiscip Stud 3:179–185
Somasegaran P, Hoben HJ (1994) Handbook for rhizobia: methods in legume rhizobium technology. Springer, Berlin
Song L, Shao Y, Ning S, Tan L (2017) Performance of a newly isolated salt-tolerant yeast strain Pichia occidentalis G1 for degrading and detoxifying azo dyes. Bioresour Technol 233:21–29
Stavenhagen M, Buurman J, Tortajada C (2018) Saving water in cities: assessing policies for residential water demand management in four cities in Europe. Cities 79:187–195
Steel RG, Torrie JH, Dickey D (1997) Principles and procedures of statistics, a biometrical approach. The McGraw-Hill Co. Inc., New York
Sun Z, Liu K, Zhang J, Zhang Y, Xu K, Yu D, Wang J, Hu L, Chen L, Li C (2017) IAA producing Bacillus altitudinis alleviates iron stress in Triticum aestivum L. seedling by both bioleaching of iron and up-regulation of genes encoding ferritins. Plant Soil 419:1–11
Tak HI, Ahmad F, Babalola OO (2013) Advances in the application of plant growth-promoting rhizobacteria in phytoremediation of heavy metals. Rev Environ Contam Toxicol 223:33–52
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729
Trivedi P, Sa T (2008) Pseudomonas corrugata (NRRL B-30409) mutants increased phosphate solubilization, organic acid production, and plant growth at lower temperatures. Curr Microbiol 56:140–144
Wang H, Su JQ, Zheng XW, Tian Y, Xiong XJ, Zheng TL (2009) Bacterial decolorization and degradation of the reactive dye Reactive Red 180 by Citrobacter sp. CK3. Int Biodeterior Biodegrad 63:395–399
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703
The authors are indebted to the financial contribution of Department of Bioinformatics and Biotechnology and Department of Environmental Sciences and Engineering, Government College University, Faisalabad, Pakistan, from the departmental annual grant.
Conflict of interest
The authors declare that there is no conflict of interest related to this study.
Electronic supplementary material
Below is the link to the electronic supplementary material.
About this article
Cite this article
Shahid, M., Mahmood, F., Hussain, S. et al. Enzymatic detoxification of azo dyes by a multifarious Bacillus sp. strain MR-1/2-bearing plant growth-promoting characteristics. 3 Biotech 8, 425 (2018). https://doi.org/10.1007/s13205-018-1442-5
- Azo dyes
- Plant growth