Abstract
A novel Cr(VI)-resistant haloalkaliphilic bacterial strain NRC-R, identified as Salipaludibacillus agaradhaerens, was isolated from hypersaline soda lakes and characterized for its Cr(VI) bioreduction efficiency. Strain NRC-R grew well and effectively reduced Cr(VI) under a wide range of sodium chloride, pH, shaking velocity and temperature, showing maximum Cr(VI) reduction at 8% NaCl, pH 10, 150 rpm and 35 °C, respectively. Strain NRC-R was able to grow and reduce Cr(VI) effectively in the presence of different heavy metals and oxyanions (Pb2+, Zn2+, Co2+, Mn2+, Ni2+, Mo2+, HPO4−, NO3−, SO42− and HCO3−). Furthermore, Fe3+ and Cu2+ significantly enhanced the Cr(VI) removal by about 1.5 fold. Strain NRC-R could reduce Cr(VI) using a variety of electron donors, exhibiting a maximum reduction in the presence of NADH and fructose. The bioremoval of Cr(VI) using strain NRC-R was due to direct enzymatic reduction and the chromate reductase activity was mainly detected in the bacterial cell membrane. Under the optimized conditions, strain NRC-R showed a remarkable Cr(VI) bioreduction with highest reduction rate of 240 uM/h. Cr(VI) concentrations of up to 3 mM (888.5 mg/L) and 4 mM (1177 mg/L) were completely reduced within 16 h and 32 h, respectively. TEM and SEM–EDX analyses confirmed the biosorption of chromium species into the cells. To the best of our knowledge, this is the first report about Cr(VI) reduction by S. agaradhaerens. In conclusion, S. agaradhaerens NRC-R was a highly efficient Cr(VI) reducing haloalkaliphilic bacterium that has a significant potential in the bioremediation of Cr(VI)-contaminated environments.
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References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Baldiris R, Acosta-Tapia N, Montes A, Hernández J, Vivas-Reyes R (2020) Reduction of Hexavalent Chromium and Detection of Chromate Reductase (ChrR) in Stenotrophomonas maltophilia. Molecules 23:406. https://doi.org/10.3390/molecules23020406
Banerjee S, Misra A, Chaudhury S, Dam B (2019) A Bacillus strain TCL isolated from Jharia coalmine with remarkable stress responses, chromium reduction capability and bioremediation potential. J Hazard Mater 367:215–223. https://doi.org/10.1016/j.jhazmat.2018.12.038
Bartlett RJ, James BR (1996) Chromium. In: DL Sparks (ed) Methods of soil analysis. Part 3 chemical methods. SSA, Madison
Bharagava RN, Mishra S (2018) Hexavalent chromium reduction potential of Cellulosimicrobium sp. isolated from common effluent treatment plant of tannery industries. Ecotoxicol Environ Saf 147:102–109. https://doi.org/10.1016/j.ecoenv.2017.08.040
Chai L, Ding C, Li J, Yang Z, Shi Y (2019) Multi-omics response of Pannonibacter phragmitetus BB to hexavalent chromium. Environ Pollut 249:63–73. https://doi.org/10.1016/j.envpol.2019.03.005
Chen J, Tian Y (2021) Hexavalent chromium reducing bacteria: mechanism of reduction and characteristics. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-021-13325-7
Chen R, Wang P, Li M, Tian F, Xiao J, Fu X, Ding C, Shi Y (2018) Removal of Cr(VI) by magnetic Fe/C crosslinked nanoparticle for water purification: rapid contaminant removal property and mechanism of action. Water Sci Technol 78:2171–2182. https://doi.org/10.2166/wst.2018.497
Cheung KH, Gu JD (2007) Mechanism of hexavalent chromium detoxification by microorganisms and bioremediation application potential: a review. Int Biodeterior Biodegrad 59(1):8–15. https://doi.org/10.1016/j.ibiod.2006.05.002
Das S, Mishra J, Das SK, Pandey S, Rao DS, Chakraborty A, Sudarshan M, Das N, Thatoi H (2014) Investigation on mechanism of Cr(VI) reduction and removal by Bacillus amyloliquefaciens, a novel chromate tolerant bacterium isolated from chromite mine soil. Chemosphere 96:112–121. https://doi.org/10.1016/j.chemosphere.2013.08.080
Das S, Behera BC, Mohapatra RK, Pradhan B, Sudarshan M, Chakraborty A, Thatoi H (2021) Reduction of hexavalent chromium by Exiguobacterium mexicanum isolated from chromite mines soil. Chemosphere 282:131135. https://doi.org/10.1016/j.chemosphere.2021.131135
Dong G, Wang Y, Gong L, Wang M, Wang H, He N, Zheng Y, Li Q (2013) Formation of soluble Cr(III) end-products and nanoparticles during Cr(VI) reduction by Bacillus cereus strain XMCr-6. Biochem Eng J 70:166–172. https://doi.org/10.1016/j.bej.2012.11.002
He D, Zheng M, Ma T, Li C, Ni J (2015) Interaction of Cr(VI) reduction and denitrification by strain Pseudomonas aeruginosa PCN-2 under aerobic conditions. Biores Technol 185:346–352. https://doi.org/10.1016/j.biortech.2015.02.109
Ibrahim AS, El-Tayeb MA, Elbadawi YB, Al-Salamah AA (2011) Isolation andcharacterization of novel potent Cr(VI) reducing alkaliphilic Amphibacillus spKSUCr3 from hypersaline soda lakes. Electr J Biotechnol. https://doi.org/10.2225/vol14-issue4-fulltext-4
Ibrahim AS, El-Tayeb MA, Elbadawi YB, Al-Salamah AA, Antranikian G (2012) Hexavalent chromate reduction by alkaliphilic Amphibacillus sp KSUCr3 is mediated by cupper dependent membrane-associated Cr(VI) reductase. Extremophiles 16(4):659–668. https://doi.org/10.1007/s00792-012-0464-x
Jankiewicz B, Ptaszyñski B (2005) Determination of chromium in soil of lódÿ gardens. Pol J Environ Stud 14(6):869–875
Karthik C, Oves M, Thangabalu R, Sharma R, Santhosh SB, Arulselvi PI (2016) Cellulosimicrobium funkei-like enhances the growth of Phaseolus vulgaris by modulating oxidative damage under Chromium(VI) toxicity. J Adv Res 7:839–850. https://doi.org/10.1016/j.jare.2016.08.007
Karthik C, Barathi S, Pugazhendhi A, Ramkumar VS, Thi ND, Arulselvi PI (2017) Evaluation of Cr(VI) reduction mechanism and removal by Cellulosimicrobium funkei strain AR8, a novel haloalkaliphilic bacterium. J Hazard Mater 333(5):42–53. https://doi.org/10.1016/j.jhazmat.2017.03.037
Khan AR, Ullah I, Khan AL, Park GS, Waqas M, Hong SJ, Jung BK, Kwak Y, Lee HJ, Shin JH (2015) Improvement in phytoremediation potential of Solanum nigrum under cadmium contamination through endophytic-assisted Serratia sp. RSC-14 inoculation. Environ Sci Pollut Res 22:14032–14042. https://doi.org/10.1007/s11356-015-4647-8
Khattar JS, Parveen S, Singh Y, Singh DP, Gulati A (2014) Intracellular uptake and reduction of hexavalent chromium by the cyanobacterium Synechocystis sp. PUPCCC 62. J Appl Phycol 27:1–11. https://doi.org/10.1007/s10811-014-0374-7
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematic. Whiley, New York, pp 115–175
Li N, Pan Y, Zhang N, Wang X, Zhou W (2016) The bio-reduction of chromate with periplasmic reductase using a novel isolated strain Pseudoalteromonas sp CF10-13. RSC Adv 6:106600–106607. https://doi.org/10.1039/C6RA16320C
Li M, He Z, Hu Y, Hu L, Zhong H (2019) Both cell envelope and cytoplasm were the locations for chromium(VI) reduction by Bacillus sp. M6. Biores Technol 273:130–135. https://doi.org/10.1016/j.biortech.2018.11.006
Lin X, Luo M, Jiang C, Wei X, Kong P, Liang X, Zhao J, Yang L, Liu H (2012) In vitro reduction of hexavalent chromium by cytoplasmic fractions of Pannonibacter phragmitetus LSSE-09 under aerobic and anaerobic conditions. Appl Biochem Biotechnol. 166:933–941. https://doi.org/10.1007/s12010-011-9481-y
Long D, Xianjin Tang X, Cai K, Chen G, Chen L, Duan D, Zhu J, Chen Y (2013) Cr(VI) reduction by a potent novel alkaliphilic halotolerant strain Pseudochrobactrum saccharolyticum LY10. J Hazard Mater 256–257:24–32. https://doi.org/10.1016/j.jhazmat.2013.04.020
Lu YZ, Chen GJ, Bai YN, Fu L, Qin LP, Zeng RJ (2018) Chromium isotope fractionation during Cr(VI) reduction in a methane-based hollow-fiber membrane biofilm reactor. Water Res 130:263–270. https://doi.org/10.1016/j.watres.2017.11.045
Lyu H, Tang J, Yao H, Gai L, Zeng EY, Liber K, Gong Y (2017) Removal of hexavalent chromium from aqueous solutions by a novel biochar supported nanoscale iron sulfide composite. Chem Eng J 322:516–524. https://doi.org/10.1016/j.cej.2017.04.058
Mala JG, Sujatha D, Rose C (2015) Inducible chromate reductaseexhibiting extracellular activity in Bacillus methylotrophicus for chromium bioremediation. Microbiol Res 170:235–241. https://doi.org/10.1016/j.micres.2014.06.001
Mangaiyarkarasi SM, Vincent S, Janarthanan S, Rao TS, Tata BR (2011) Bioreduction of Cr(VI) by alkaliphilic Bacillus subtilis and interaction of the membrane groups. Saudi J Biol Sci 18:157–167. https://doi.org/10.1016/j.sjbs.2010.12.003
Mishra RR, Dhal B, Dutta SK, Dangar TK, Das NN, Thatoi HN (2012) Optimization and characterization of chromium(VI) reduction in saline condition by moderately halophilic Vigribacillus sp. isolated from mangrove soil of Bhitarkanika, India. J Hazard Mater 227–228:219–226. https://doi.org/10.1016/j.jhazmat.2012.05.063
Mistry LK, Desai C, Lal S, Patel K, Patel B (2010) Hexavalent chromium reduction by staphylococcus Sp. isolated from Cr (VI) contaminated land fill. Int J Biotechnol Biochem 6(1):117–129
Mondal MH, Malik S, Garain A, Mandal S, Saha B (2017) Extraction of natural surfactant saponin from soapnut (Sapindus mukorossi) and its utilization in the remediation of hexavalent chromium from contaminated water. Tenside, Surfactants, Deterg 54:519–529. https://doi.org/10.3139/113.110523
Narayan R, Meena RP, Patel AK, Prajapati AK, Srivastava S, Mondal MK (2016) Characterization and application of biomass gasifier waste material for adsorptive removal of Cr (VI) from aqueous solution. Environ Progress Sustain Energy 35:95–102. https://doi.org/10.1002/ep.12205
Nielsen P, Fritze D, Priest FG (1995) Phenetic diversity of alkaliphilic Bacillus strains: proposal for nine new species. Microbiology 141:1745–1761. https://doi.org/10.1099/13500872-141-7-1745
Pal A, Paul AK (2004) Aerobic chromate reduction by chromium-resistant bacteria isolated from serpentine soil. Microbiol Res 159:347–354. https://doi.org/10.1016/j.micres.2004.08.001
Pal A, Dutta S, Paul AK (2005) Reduction of hexavalent chromium by cell free extract of Bacillus sphaericus AND 303 isolated from serpentine soil. Curr Microbiol 51:327–330. https://doi.org/10.1007/s00284-005-0048-4
Pradhan D, Sukla LB, Sawyer M, Rahman PM (2017) Recent bioreduction of hexavalent chromium in wastewater treatment: a review. J Ind Eng Chem 55:1–20. https://doi.org/10.1016/j.jiec.2017.06.040
Sultanpuram VR, Mothe T (2016) Salipaludibacillus aurantiacus gen. nov., sp. nov. a novel alkali tolerant bacterium, reclassification of Bacillus agaradhaerens as Salipaludibacillus agaradhaerens comb. nov. and Bacillus neizhouensis as Salipaludibacillus neizhouensis comb. nov. Int J Syst Evol Microbiol 66:2747–2753. https://doi.org/10.1099/ijsem.0.001117
Tan H, Wang C, Zeng G, Luo Y, Li H, Heng XuH (2020) Bioreduction and biosorption of Cr(VI) by a novel Bacillus sp. CRB-B1 strain. J Hazardous Mat 386:121628. https://doi.org/10.1016/j.jhazmat.2019.121628
Thacker U, Parikh R, Shouche Y (2006) Hexavalent chromium reduction by Providencia sp. Proc Biochem 41:1332–1337. https://doi.org/10.1016/j.procbio.2006.01.006
Troiano JM, Jordan DS, Hull CJ, Geiger FM (2016) Interaction of Cr(III) and Cr(VI) with hematite studied by second harmonic generation. J Phys Chem C 117:5164–5171. https://doi.org/10.1021/jp3122819
Viti C, Marchi E, Decorosi F, Giovannetti L (2014) Molecular mechanisms of Cr(VI) resistance in bacteria and fungi. FEMS Microbiol Rev 38:633–659. https://doi.org/10.1111/1574-6976.12051
Wu M, Li Y, Li J, Wang XH, Zhao Y (2019) Bioreduction of hexavalent chromium using a novel strain CRB-7 immobilized on multiple materials. J Hazard Mater 368:412–420. https://doi.org/10.1016/j.jhazmat.2019.01.059
Xu W, Jian H, Liu G, Zeng GM, Li X, Zhang W (2015) Bioreduction of chromate by an isolated Bacillus anthracis Cr-4 with soluble Cr(III) product. Water Air Soil Pollut 226:82. https://doi.org/10.1007/s11270-015-2356-z
Yao Y, Hu L, Li S, Zeng Q, HuiZhong H, Zhiguo He Z (2020) Exploration on the bioreduction mechanisms of Cr(VI) and Hg(II) by a newly isolated bacterial strain Pseudomonas umsongensis CY-1. Ecotoxicol Environ Saf 201:110850. https://doi.org/10.1016/j.ecoenv.2020.110850
Zeng Q, Hu Y, Yang Y, Hu L, Zhong Het Z (2019) Cell envelop is the key site for Cr(VI) reduction by Oceanobacillus oncorhynchi W4, a newly isolated Cr(VI) reducing bacterium. J Hazard Mater 368:149–155. https://doi.org/10.1016/j.jhazmat.2019.01.031
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This project was supported by National Research Centre (Grant Number E120210), El-Buhouth St., Dokki, Cairo 12622, Egypt.
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Abo-Alkasem, M.I., Maany, D.A., El-Abd, M.A. et al. Bioreduction of hexavalent chromium by a novel haloalkaliphilic Salipaludibacillus agaradhaerens strain NRC-R isolated from hypersaline soda lakes. 3 Biotech 12, 7 (2022). https://doi.org/10.1007/s13205-021-03082-2
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DOI: https://doi.org/10.1007/s13205-021-03082-2