Screening of silver-tolerant bacteria from a major Philippine landfill as potential bioremediation agents

• Autorzy: Adriano J. S. , Oyong G. G. , Cabrera E. C. , Janairo J. I. B.

Identyfikatory

DOI

10.1515/eces-2018-0032

Warianty tytułu

PL

Badania przesiewowe bakterii odpornych na działanie srebra z dużego składowiska odpadów na Filipinach, możliwych do wykorzystania w bioremediacji

• Języki publikacji: EN

Abstrakty

EN

The field of microbial biotechnology has revolutionized the utilization of microorganisms to overcome the problems of environmental pollutions. The present study aimed to identify silver-tolerant isolates and screen their ability to synthesize silver nanoparticles for possible use as bioremediation agents. Seventeen bacterial isolates from soil collected from the Smokey Mountain landfill in Manila, Philippines, were found to tolerate 0.01 M AgNO3 in the culture medium. Molecular and phylogenetic analyses using the 16S rRNA gene sequence identified the isolates as Bacillus cereus, Bacillus subtilis, Bacillus flexus, Bacillus thuringiensis, Alcaligenes faecalis, Achromobacter sp. and Ochrobactrum sp. The formation of silver nanoparticles was evident in the change in color of the reaction mixtures, and was detected through UV-VIS spectroscopy with absorbance peaks at 250-300 nm and 400-450 nm. Scanning electron microscopy revealed the aggregation of diverse shapes of silver nanoparticles with sizes ranging from 70 to 200 nm. The best silver nanoparticle-synthesizing isolates were Alcaligenes faecalis and Bacillus cereus. The results denote the promising microbial technology application of the 17 silver-tolerant isolates in combating the adverse effects of metals and other pollutants in the environment.

Słowa kluczowe

EN

microbial biotechnology; bioremediation; silver nanoparticles; silver-tolerant bacteria; biosynthesis; landfill

PL

biotechnologia mikrobiologiczna; bioremediacja; nanocząstki srebra; bakterie tolerujące srebro; biosynteza; składowisko odpadów

• Wydawca: Towarzystwo Chemii i Inżynierii Ekologicznej
• Czasopismo: Ecological Chemistry and Engineering. S
• Rocznik: 2018
• Tom: Vol. 25, nr 3
• Strony: 469--485
• Opis fizyczny: Bibliogr. 75 poz., map., rys., wykr., tab.

Twórcy

autor

Adriano J. S.

• Biology Department, College of Science, De La Salle University, 2401 Taft Avenue, Manila 0922, Philippines
• Biological Sciences Department, School of Science and Technology, Centro Escolar University, 9 Mendiola, Manila, Philippines, phone [phone]

autor

Oyong G. G.

• Biology Department, College of Science, De La Salle University, 2401 Taft Avenue, Manila 0922, Philippines
• Molecular Science Unit Laboratory, Center for Natural Sciences and Environmental Research, De La Salle University, 2401 Taft Avenue, Manila 0922, Philippines

autor

Cabrera E. C.

• Biology Department, College of Science, De La Salle University, 2401 Taft Avenue, Manila 0922, Philippines
• Molecular Science Unit Laboratory, Center for Natural Sciences and Environmental Research, De La Salle University, 2401 Taft Avenue, Manila 0922, Philippines

autor

Janairo J. I. B.

• Biology Department, College of Science, De La Salle University, 2401 Taft Avenue, Manila 0922, Philippines
• Materials Science and Nanotechnology Research Unit, Center for Natural Sciences and Environmental Research, De La Salle University, 2401 Taft Avenue, Manila 0922, Philippines

Bibliografia

• [1] Silver S, Phung LT, Silver G. Silver as biocides in burn and wound dressings and bacterial resistance to silver compounds. J Ind Microbiol Biotechnol. 2006;33(7)627-634. DOI: 10.1007/s10295-006-0139-7.
• [2] Massarsky A, Trudeau VL, Moon TW. Predicting the environmental impact of nanosilver. Environ Toxicol Pharmacol. 2014;38(3):861-873. DOI: 10.1016/j.etap.2014.10.006.
• [3] Quadros ME, Marr LC. Environmental and human health risks of aerosolized silver nanoparticles. J Air Waste Manage Assoc. 2010;60(7):770-781. https://www.ncbi.nlm.nih.gov/pubmed/20681424.
• [4] Benn T, Cavanagh B, Hristovski K, Posner JD, Westerhoff P. The release of nanosilver from consumer products used in the home. J Environ Qual. 2010;39(6):1875-1882. https://www.ncbi.nlm.nih.gov/pubmed/21284285.
• [5] Benn TM, Westerhoff P. Nanoparticle silver released into water from commercially available sock fabrics. Environ Sci Technol. 2008;42(11):4133-4139. DOI: 10.1021/es7032718.
• [6] Navarro E, Piccapietra F, Wagner B, Marconi F, Kaegi R, Odzak N, et al. Toxicity of silver nanoparticles to Chlamydomonas reinhardlii. Environ Sci Technol. 2008;42(23):8959-8964. DOI: 10.1021/es801785m.
• [7] Roh JY, Sim SJ, Yi J, Park K, Chung KH, Ryu DY, et al. Ecotoxicity of silver nanoparticles on the soil nematode Caenorhabdilis elegans using functional ecotoxicogenomics. Environ Sci Technol. 2009;43(10):3933-3940. https://www.ncbi.nlm.nih.gov/pubmed/19544910.
• [8] Percival SL, Woods E, Nutekpor M, Bowler P, Radford A, Cochrane C. Prevalence of silver resistance in bacteria isolated from diabetic foot ulcers and efficacy of silver-containing wound dressings. Ostomy Wound Manage. 2008;54(3):30-40. https://www.ncbi.nlm.nih.gov/pubmed/18382046.
• [9] El-Ansary A, Al-Daihan S. On the toxicity of therapeutically used nanoparticles: an overview. J Toxicol. 2009. Article ID 754810. DOI:10.1155/2009/754810.
• [10] Greulich C, Kittler S, Epple M, Muhr G, Köller M. Studies on the biocompatibility and the interaction of silver nanoparticles with human mesenchymal stem cells (hMSCs). Langenbecks Arch Surg. 2009;394(3):495-502. DOI: 10.1007/s00423-009-0472-1.
• [11] Harzevili FD, Chen H. Microbial Biotechnology: Progress and Trends. CRC Press; 2017. ISBN: 9781138748699.
• [12] Kumar BL, Gopal DVRS. Effective role of indigenous microorganisms for sustainable environment. 3 Biotech. 2015;5(6):867. DOI: 10.1007/s13205-015-0293-6.
• [13] Zhang S, Wang Q, Wan R, Xie S, Zhejiang J. Changes in bacterial community of anthracene bioremediation in municipal solid waste composting soil. Univ Sci B. 2011;12(9):760-768. DOI: 10.1631/jzus.B1000440.
• [14] Chen WY, Wu JH, Lin YY, Huang HJ, Chang JE. Bioremediation potential of soil contaminated with highly substituted polychlorinated dibenzo-p-dioxins and dibenzofurans: microcosm study and microbial community analysis. J Hazard Mater. 2013;261:351-361. DOI: 10.1016/j.jhazmat.2013.07.039.
• [15] Xenia ME, Refugio RV. Microorganisms metabolism during bioremediation of oil contaminated soils. J Bioremed Biodegr. 2016;7:340. DOI: 10.4172/2155-6199.1000340.
• [16] Durán M, Faljoni-Alario A, Durán N. Mechanistic aspects of biosynthesis of silver nanoparticles by several Fusarium oxysporum strains. Folia Microbiol (Praha). 2010;55(6):535-547. DOI: 10.1007/s12223-010-0088-4.
• [17] Yang C, Song C, Mulchandani A, Qiao C. Genetic engineering of Stenotrophomonas strain YC-1 to possess a broader substrate range for organophosphates. J Agric Food Chem. 2010;58(11):6762-6766. DOI: 10.1021/jf101105s.
• [18] Jiang J, Liu H, Li Q, Gao N, Yao Y, Xu H. Combined remediation of Cd-phenanthrene co-contaminated soil by Pleurotus cornucopiae and Bacillus thuringiensis FQ1 and the antioxidant responses in Pleurotus cornucopiae. Ecotoxicol Environ Saf. 2015;120:386-393. DOI: 10.1016/j.ecoenv.2015.06.028.
• [19] Zinicovscaia I, Rudi L, Valuta A, Cepoi L,Vergel K, Frontasyeva MV, et al. Biochemical changes in Nostoc linckia associated with selenium nanoparticles biosynthesis. Ecol Chem Eng S. 2016; 23(4): 559-569. DOI: 10.1515/eces-2016-0039.
• [20] Gargi B, Ranjit D, Sufia K. Chromium bioremediation by Alcaligenes faecalis strain P-2 isolated from tannery effluents. J Environ Res Develop. 2015;9:3A. https://www.researchgate.net/publication/288991602.
• [21] Ghoreishi G, Alemzadeh A, Mojarrad M, Djavaheri M. Kerosene biodegradation ability and characterization of bacteria isolated from oil-polluted soil and water. J Environ Chem Eng. 2016;4(4):4323-4329. DOI: 10.1016/j.jece.2016.09.035.
• [22] Kundu D, Hazra C, Chaudhari A. Bioremediation potential of Rhodococcus pyridinivorans NT2 in nitrotoluene-contaminated soils: the effectiveness of natural attenuation, biostimulation and bioaugmentation approaches. Soil Sediment Contamin, Int J. 2016;25(6):637-651. DOI: 10.1080/15320383.2016.1190313.
• [23] Liu W, Luo Y, Teng Y, Li Z, Ma L. Bioremediation of oily sludge-contaminated soil by stimulating indigenous microbes. Environ Geochem Health. 2010;32(1):23-29. DOI: 10.1007/s10653-009-9262-5.
• [24] Rajkumar M, Ae N, Freitas H. Endophytic bacteria and their potential to enhance heavy metal phytoextraction. Chemosphere. 2009;77(2):153-160. DOI: 10.1016/j.chemosphere.2009.06.047.
• [25] Sameera V. Novel techniques in the production of industrially imperative products. J Microbial Biochem Technol R1:003. 2011. DOI: 10.4172/1948-5948.R1-003.
• [26] Padil VVT, Wacławek S, Černík M. Green synthesis: nanoparticles and nanofibres based on tree gums for environmental applications. Ecol Chem Eng S. 2016; 23(4):533-557. DOI: 10.1515/eces-2016-0038.
• [27] Smokey Mountain Remediation and Development Project: Philippines. Poverty Environment Partnership. 25 October 2012. Accessed 24 Oct 2016. http://www.povertyenvironment.net/adb/subprojects/phi-smokey.
• [28] Torres, Tetch. “SC upholds Smokey Mountain contract between NHA, R-II”. Inquirer.net. Posted 15 August 2007. Accessed 24 Oct 2016. https://tetchtorres.wordpress.com/2007/08/15/sc-upholds-smokey-mountain-contract-between-nha-r-ii/.
• [29] Medina M. The World’s Scavengers: Salvaging for Sustainable Consumption and Production. Lanham, MD [u.a.]: AltaMira Press; 2007. ISBN 0759109419.
• [30] Bergey DH, Holt JG, Krieg NR, Sneath PHA, Staley JT, Williams ST. Bergey’s Manual of Determinative Bacteriology, 9th ed. Baltimore: Williams and Wilkins. 1994. https://archive.org/stream/bergeysmanualofd00amer/bergeysmanualofd00amer_djvu.txt.
• [31] Pisapia C, Gerard E, Gerard M, Meñez B. Mineralizing filamentous bacteria from the Porny Bay hydrothermal field give new insights into the functioning of sepentization-based subseafloor ecosystems. Front Microbiol. 2017;8:7. DOI: 10.3389/fmicb.2017.00057.
• [32] Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows. 95/98/NT. Nucl Acids Symp Ser. 1999;41:95-98. http://brownlab.mbio.ncsu.edu/JWB/papers/1999Hall1.pdf.
• [33] Hall TA. BioEdit: An important software for molecular biology. GERF Bull Biosci. 2011;2(1):60-61. https://www.gerfbb.com/images/upload/article/pdf/1387127438.
• [34] https://www.ncbi.nlm.nih.gov/.
• [35] Katoh K, Toh H. Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform. 2008;9(4):286-298. DOI: 10.1093/bib/bbn013.
• [36] Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol. 2007;56(4):564-577. DOI: 10.1080/10635150701472164.
• [37] Rzhetsky A, Nei M. A simple method for estimating and testing minimum evolution trees. Molecular Biol Evolution. 1992;9:945-967. DOI: 10.1093/oxfordjournals.molbev.a040771.
• [38] Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biol Evolution. 2016;33(7):1870-1874. DOI: 10.1093/molbev/msw054.
• [39] Felsenstein J. Confidence limits on phylogenies: An approach using the bootstrap. Evolution. 1985;39(4):783-791. DOI: 10.1111/j.1558-5646.1985.tb00420.x.
• [40] Shahverdi AR, Fakhimi A, Shahverdi HR, Minaian S. Synthesis and effect of silver nanoparticles on the antibacterial activity of different antibiotics against Staphylococcus aureus and Escherichia coli. Nanomedicine. 2007;3(2):168-171. DOI: 10.1016/j.nano.2007.02.001.
• [41] Li WR, Xie XB, Shi QS, Zeng HY, Ou-Yang YS, Chen YB. Antibacterial activity and mechanism of silver nanoparticles on Escherichia coli. Appl Microbiol Biotechnol. 2010;85(4):1115-1122. DOI: 10.1007/s00253-009-2159-5.
• [42] Sharma HS, Hussain S, Schlager J, Ali SF, Sharma A. Influence of nanoparticles on blood-brain barrier permeability and brain edema formation in rats. Acta Neurochir Suppl. 2010;106:359-364. DOI: 10.1007/978-3-211-98811-4_65.
• [43] Liau, SY, Read DC, Pugh WJ, Furr JR, Russell AD. Interaction of silver nitrate with readily identifiable groups: relationship to the antibacterial action of silver ions. Lett Appl Microbiol. 1997;25(4):279-283. DOI: 10.1046/j.1472-765X.1997.00219.x.
• [44] Klueh U, Wagner V, Kelly S, Johnson A, Bryers JD. Efficacy of silver-coated fabric to prevent bacterial colonization and subsequent device-based biofilm formation. J Biomedical Mater Res Part B: Appl Biomaterials. 2000;53(6):621-631. DOI: 10.1002/1097-4636(2000)53:63.0.CO;2-Q.
• [45] Fox CL, Modak SM. Mechanism of silver sulfadiazine action on burn wound infections. Antimicrob Agents Chemother. 1974;5(6)582-588. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC429018/.
• [46] Yang W, Shen C, Ji Q, An H, Wang J, Liu Q, Zhang Z. Food storage material silver nanoparticles interfere with DNA replication fidelity and bind with DNA. Nanotechnology. 2009;20(8):085102. DOI: 10.1088/0957-4484/20/8/085102.
• [47] McHugh GL, Moellering RC, Hopkins CC et al. Salmonella typhimurium resistant to silver nitrate, chloramphenicol, and ampicillin. Lancet. 1975;1(7901):235-240. DOI: 10.1016/S0140-6736(75)91138-1.
• [48] Gupta A, Matsui K, Lo JF et al. Molecular basis for resistance to silver cations in Salmonella. Nat Med. 1999;5(2):183-188. DOI: 10.1038/5545.
• [49] Silver S. Bacterial silver resistance: molecular biology and uses and misuses of silver compounds. FEMS Microbiol Rev. 2003; 27:(2-3):341-353. DOI: 10.1016/S0168-6445(03)00047-0.
• [50] Gupta A, Phung LT, Taylor DE, Silver S. Diversity of silver resistance genes in IncH incompatibility group plasmids. Microbiology. 2001;147:3393-3402. DOI: 10.1099/00221287-147-12-3393.
• [51] Sandegren L, Linkevicius M, Lytsy B, Melhus Å, Andersson DI. Transfer of an Escherichia coli ST131 multiresistance cassette has created a Klebsiella pneumoniae-specific plasmid associated with a major nosocomial outbreak. J Antimicrob Chemother. 2012;67(1):74-83. DOI: 10.1093/jac/dkr405.
• [52] Sütterlin S. Aspects of Bacterial Resistance to Silver. Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Medicine 1084. Uppsala: Acta Universitatis Upsaliensis. 2015. 64 pp. ISBN 978915549205. https://www.diva-portal.org/smash/get/diva2:796254/FULLTEXT01.pdf.
• [53] Galdiero S, Falanga A, Cantisani M, Tarallo R, Della Pepa ME, D’Oriano V, et al. Microbe-host interactions: structure and role of Gram-negative bacterial porins. Curr Protein Pept Sci. 2012;13(8):843-854. DOI: 10.2174/138920312804871120.
• [54] Koebnik R, Locher KP, Van Gelder P. Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol. 2000;37(2):239-253. DOI: 10.1046/j.1365-2958.2000.01983.
• [55] Nikaido H. Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev. 2003;67(4):593-656. DOI: 10.1128/MMBR.67.4.593-656.2003.
• [56] Hancock RE, Bell A. Antibiotic uptake into gram-negative bacteria. Eur J Clin Microbiol Infect Dis. 1988;7(6):713-720. DOI: 10.1007/978-3-642-46666-3_6.
• [57] Achouak W, Heulin T, Pages JM. Multiple facets of bacterial porins. FEMS Microbiol Lett. 2001;199(1):1-7.
• [58] Poole K. Outer membranes and efflux: the path to multidrug resistance in Gram-negative bacteria. Curr Pharm Biotechnol. 2002;3(2):77-98. DOI : 10.2174/1389201023378454.
• [59] Zgurskaya HI, Nikaido H. Multidrug resistance mechanisms: drug efflux across two membranes. Molecular Microbiol. 2000;37(2):219-225. DOI: 10.1046/j.1365-2958.2000.01926.
• [60] Ma D, Alberti M, Lynch C, Nikaido H, Hearst JE. The local repressor AcrR plays a modulating role in the regulation of acrAB genes of Escherichia coli by global stress signals. Molecular Microbiol. 1996;19(1):101-112. DOI: 10.1046/j.1365-2958.1996.357881.
• [61] Nikaido H, Takatsuka Y. Mechanisms of RND multidrug efflux pumps. Biochim Biophys Acta. 2009;1794(5): 769-81. DOI:10.1016/j.bbapap.2008.10.004.
• [62] Ren Q, Chen K, Paulsen IT. TransportDB: a comprehensive database resource for cytoplasmic membrane transport systems and outer membrane channels. Nucleic Acids Res. 2007;35(D274-D279). DOI: 10.1093/nar/gkl925.
• [63] Huelsenbeck JP, Ronquist F. Bayesian Analysis of Molecular Evolution using MrBayes. In: Statistical Methods in Molecular Evolution. Springer Science & Business Media;2005. DOI: 10.1007/0-387-27733-1_7.
• [64] Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17(8):754-755. DOI: 10.1093/bioinformatics/17.8.754.
• [65] Saklani V, Suman, Jain VK. Microbial synthesis of silver nanoparticles: a review. J Biotechnol Biomaterial. 2012;S13:007. DOI: 10.4172/2155-952X.S13-007.
• [66] Balaji DS, Basavaraja S, Deshpande R, Mahesh D, Prabhakar BK, Venkataraman A. Extracellular biosynthesis of functionalized silver nanoparticle by strains of Cladosporium cladosporioides fungus. Colloids Surf B Biointerfaces. 2009;68(1):88-92. DOI: 10.1016/j.colsurfb.2008.09.022.
• [67] Wani IA, Khatoon S, Ganguly A, Ahmed J, Ganguli AK, Ahmad T. Silver nanoparticles: large scale solvothermal synthesis and optical properties. Mater Res Bull. 2010;45(8):1033-1038. DOI: 10.1016/j.materresbull.2010.03.028.
• [68] Esfandiary R, Hunjan JS, Lushington G, Joshi S, Middaugh R. Temperature dependent 2nd derivative absorbance spectroscopy of aromatic amino acids as a probe of protein dynamics. Protein Sci. 2009;18(12):2603-2614. DOI: 10.1002/pro.264.
• [69] Hristovski KD, Nguyen H, Westerhoff PK. Removal of arsenate and 17-ethinyl estradiol (EE2) by iron (hydr) oxide modified activated carbon fibers. J Environ Sci Health A Tox Hazard Subst Environ Eng. 2009:44(4):354-361. DOI: 10.1080/10934520802659695.
• [70] Huang J, Cao Y, Liu Z, Deng Z, Tang F, Wang W. Efficient removal of heavy metal ions from water system by titanate nanoflowers. Chem Eng J. 2012;180:75-80. DOI: 10.1016/j.cej.2011.11.005.
• [71] Khan SB, Marwani, HM, Asiri AM, Bakhsh EM. Exploration of calcium doped zinc oxide nanoparticles as selective adsorbent for extraction of lead ion. Desalin Water Treat. 2016;57(41)1-10. DOI: 10.1080/19443994.2015.1109560.
• [72] Liu M, Chen C, Hu J, Wu X, Wang X. Synthesis of magnetite/graphene oxide composite and application for cobalt(II) removal. J Phys Chem C. 2011;115(51):25234-25240. DOI: 10.1021/jp208575m.
• [73] Zhu J, Wei S, Chen M, Gu H, Rapole SB, Pallavkar S, et al. Magnetic nanocomposites for environmental remediation. Adv Powder Technol. 2013;24(2):459-467. DOI: 10.1016/j.apt.2012.10.012.
• [74] Yadav KJ, Singh K, Gupta N, Kumar V. A review of nanobioremediation technologies for environmental cleanup: a novel biological approach. J Mater Environ Sci. 2017;8(2):740-757. https://www.jmaterenvironsci.com/Document/vol8/vol8_N2/78-JMES-2831-Yadav.pdf.
• [75] Watlington K. U.S. Environmental Protection Agency, August 2005; www.epa.gov; www.clu-in.org. Accessed June 2017.

Uwagi

PL

Opracowanie rekordu w ramach umowy 509/P-DUN/2018 ze środków MNiSW przeznaczonych na działalność upowszechniającą naukę (2018).