Lead resistant bacteria: Lead resistance mechanisms, their applications in lead bioremediation and biomonitoring

Ecotoxicology and Environmental Safety

Volumn 98, Issue , 2013, Pages 1-7

  Naik, Milind Mohan ^a   Dubey, Santosh Kumar ^a  

^a GOA UNIVERSITY   (India)

Author keywords

Bacteria; Biomonitoring; Bioremediation; Lead resistance

Indexed keywords

ADENOSINE TRIPHOSPHATASE; AMIKACIN; AMPICILLIN; CADMIUM; CEFALORIDINE; CHLORAMPHENICOL; COPPER; COTRIMOXAZOLE; ERYTHROMYCIN; KANAMYCIN; LEAD; LEAD NITRATE; LINCOMYCIN; MECILLINAM; METALLOTHIONEIN; OLEANDOMYCIN; PROTEIN TYROSINE PHOSPHATASE 1B; SILVER; TOBRAMYCIN; ZINC;

BIOACCUMULATION; BIOMONITORING; BIOREMEDIATION; ECOTOXICOLOGY; LEAD; MICROBIAL ACTIVITY; POLLUTION TOLERANCE; WASTEWATER; WATER TREATMENT;

ANTIBIOTIC RESISTANCE; BACTERIUM; BIOACCUMULATION; BIOAVAILABILITY; BIOCHEMISTRY; BIOLOGICAL MONITORING; BIOREMEDIATION; BIOSENSOR; BIOSORPTION; BIOTRANSFORMATION; CELL STRUCTURE; CELLULAR DISTRIBUTION; DRUG RESISTANCE; ENTEROCOCCUS HIRAE; ENZYME DEGRADATION; ESCHERICHIA COLI; HELICOBACTER PYLORI; LIMIT OF DETECTION; MULTIDRUG RESISTANCE; NONHUMAN; PRECIPITATION; REVIEW; WASTE COMPONENT REMOVAL; WATER POLLUTION;

BACTERIA; BIOMONITORING; BIOREMEDIATION; LEAD RESISTANCE;

BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; BIODEGRADATION, ENVIRONMENTAL; BIOSENSING TECHNIQUES; BIOTRANSFORMATION; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ENVIRONMENTAL MONITORING; ENVIRONMENTAL POLLUTANTS; HAZARDOUS SUBSTANCES; LEAD; WASTE WATER;

EID: 84887186640     PISSN: 01476513     EISSN: 10902414     Source Type: Journal    
DOI: 10.1016/j.ecoenv.2013.09.039     Document Type: Review

References (90)

1. Aickin R.M., Dean A.C.R. Lead accumulation by microorganisms. Microbios Letters 1977, 5:129-133.
2. Aickin R.M., Dean A.C.R., Cheetham A.K., Skarnulis A.J. Electron microscope studies on the uptake of lead by a Citrobacter species. Microbios Letters 1979, 9:7-15.
3. Aiking H., Govers H., van't Riet J. Detoxification of mercury, cadmium, and lead in Klebsiella aerogenes NCTC 418 growing in continuous culture. Applied and Environmental Microbiology 1985, 50:1262-1267.
4. Al-Aoukaty A., Appanna V.D., Huang J. Exocellular and intracellular accumulation of lead in Pseudomonas fluorescens ATCC 13525 is mediated by the phosphate content of the growth medium. FEMS Microbiology Letters 1991, 83:283-290.
5. Asmub M., Mullenders L.H.F., Hartwig A. Interference by toxic metal compounds with isolated zinc finger DNA repair proteins. Toxicology Letters 2000, 112:227-231.
6. Bayoumy M.A.E., Bewtra J.K., Ali H.I., Biswas N. Biosorption of lead by biomass of sulfate reducing bacteria. Canadian Journal of Civil Engineering 1997, 24:840-843.
7. Bhaskar P.V., Bhosle N.B. Bacterial extracellular polymeric substances (EPS) a carrier of heavy metals in the marine food-chain. Environment International 2006, 32:192-198.
8. Blindauer C.A., Harrison M.D., Robinson A.K., Parkinson J.A., Bowness P.W., Sadler P.J., Robinson N.J. Multiple bacteria encode metallothioneins and SmtA-like fingers. Molecular Microbiology 2002, 45:1421-1432.
9. Borremans B., Hobman J.L., Provoost A., Brown N.L., van der Lelie D. Cloning and functional analysis of the pbr lead resistance determinant of Ralstonia metallidurans CH34. Journal of Bacteriology 2001, 183:5651-5658.
10. Bramhachari P.V., Kavi Kishor P.B., Ramadevi R., Kumar R., Rao B.R., Dubey S.K. Isolation and characterization of mucous exopolysaccharide produced by Vibrio furnissii VB0S3. Journal of Microbiology and Biotechnology 2007, 17:44-51.
11. Braissant O., Decho A.W., Dupraz C., Glunk C., Przekop K.M., Visscher P.T. Exopolymeric substances of sulfate-reducing bacteria: interactions with calcium at alkaline pH and implication for formation of carbonate minerals. Geobiology 2007, 5:401-411.
12. Cameron R.E. Guide to site and soil description for hazardous waste characterization. Metals 1992, 250. (Environmental Protection Agency EPA/600/4-91/029).
13. Chang J.S., Law R., Chang C.C. Biosorbtion of lead, copper and cadmium by biomass of Pseudomonas aeruginosa PU21. Water Research 1997, 31:1651-1658.
14. Chakravarty R., Manna S., Ghosh A.K., Banerjee P.C. Morphological changes in an Acidocella strain in response to heavy metal stress. Res. Journal of Microbiology 2007, 2:742-748.
15. Chakravarty R., Banerjee P.C. Morphological changes in acidophilic bacterium induced by heavy metals. Extremophiles 2008, 12:279-284.
16. Chen P., Greenberg B., Taghavi S., Romano C., van der Lelie D., He C. An exceptionally selective lead (II)-regulatory protein from Ralstonia metallidurans: development of a fluorescent lead (II) probe. Angewandte Chemie International Edition 2005, 44:2715-2719.
17. Chen P.R., Wasinger E.C., Zhao J., van der Lelie D., Chen L.X., He C. Spectroscopic insights into lead (II) coordination by the selective lead (II)-binding protein PbrR691. Journal of the American Chemical Society 2007, 129:12350-12351.
18. Clarke S.E., Stuart J., Sanders-Loehr J. Induction of siderophore activity in Anabaena sp. and its moderation of copper toxicity. Applied and Environmental Microbiology 1987, 53:917-922.
19. Coombs J.M., Barkay T. Molecular evidence for the evolution of metal homeostasis genes by lateral gene transfer in bacteria from the deep terrestrial subsurface. Applied and Environmental Microbiology 2004, 70:1698-1707.
20. Coombs J.M., Barkay T. New findings on evolution of metal homeostasis genes: evidence from comparative genome analysis of bacteria and archaea. Applied and Environmental Microbiology 2005, 71:7083-7091.
21. Cox C.D., Adams P. Siderophore activity of pyoverdine for Pseudomonas aeruginosa. Infection and Immunity 1985, 48:130-138.
22. Dauvin J-C. Effects of heavy metal contamination on the macrobenthic fauna in estuaries: the case of the Seine estuary. Marine Pollution Bulletin 2008, 57:160-167.
23. De J., Ramaiah N., Bhosle N.B., Garg A., Vardanyan L., Nagle V.L., Fukami K. Potential of mercury resistant marine bacteria for detoxification of chemicals of environmental concern. Microbes and Environments 2007, 22:336-345.
24. De J., Ramaiah N., Vardanyan L. Detoxification of toxic heavy metals by marine bacteria highly resistant to mercury. Marine Biotechnology 2008, 10:471-477.
25. Decho A.W. Microbial exopolymer secretion in ocean environment, their roles in food webs and marine processes. Oceanography and Marine Biology: An Annual Review 1990, vol. 28:73-153.
26. Desai C., Jain K., Madamwar D. Hexavalent chromate reductase activity in cytosolic fractions of Pseudomonas sp. G1DM21 isolated from Cr (VI) contaminated industrial landfill. Process Biochemistry 2008, 4:713-721.
27. Flora S.J.S., Mittal M., Mehta A. Heavy metal induced oxidative stress and its possible reversal by chelation therapy. Indian Journal of Medical Research 2008, 128:501-523.
28. Fowler B.A. Roles of lead-binding proteins in mediating lead bioavailability. Environmental Health Perspectives 1998, 106:1585-1588.
29. Gadd G.M. Heavy metal accumulation by bacteria and other microorganisms. Experientia 1990, 46:834-840.
30. Gadd G.M., White C. Microbial treatment of metal pollution-a working biotechnology. Trends in Biotechnology 1993, 11:353-359.
31. Garg S.K., Tripathi M., Srinath T. Strategies for chromium bioremediation of tannery effluent. Reviews of Environmental Contamination 2012, 217:75-140.
32. Gavrilescu V. Removal of heavy metals from the environment by biosorption. Engineering in Life Sciences 2004, 4:219-232.
33. Gilis A., Corbisier P., Baeyens W., Taghavi S., Mergeay M., van der Lelie D. Effect of the siderophore alcaligin E on the bioavailability of Cd to Alcaligenes eutrophus CH34. Journal of Industrial Microbiology and Biotechnology 1998, 20:61-68.
34. Hamer D.H. Metallothioneins. Annual Review of Biochemistry 1986, 55:913-951.
35. Hartwig A., Asmuss M., Ehleben I., Herzer U., Kostelac D., Pelzer A., Schwerdtle T., Burkle A. Interference by toxic metal ions with DNA repair processes and cell cycle control: molecular mechanisms. Environmental Health Perspectives 2002, 110:797-799.
36. Hepinstall S.E., Turner B.F., Maurice P.A. Effect of siderophores on Pb and Cd adsorption to kaolinite. Clays and Clay Minerals 2005, 53:557-563.
37. Hermansson M., Jones G.W., Kjelleberg S. Frequency of antibiotic and heavy metal resistance, pigmentation and plasmids in bacteria of the marine air-water interface. Applied and Environmental Microbiology 1987, 53:2338-2342.
38. Higham D.P., Sadler P.J., Scawen M.D. Effect of cadmium on the morphology, membrane integrity and permeability of Pseudomonas putida. Journal of General Microbiology 1986, 132:1475-1482.
39. Hossain S.M., Anantharaman N. Studies on bacterial growth and lead biosoption using Bacillus subtilis. Indian Journal of Chemical Technology 2006, 13:591-596.
40. Hynninen A., Touze T., Pitkanen L., Mengin-Lecreulx D., Virta M. An efflux transporter PbrA and a phosphatase PbrB cooperate in a lead-resistance mechanism in bacteria. Molecular Microbiology 2009, 74:384-394.
41. Hynninen A., Tonismann K., Virta M. Improving the sensitivity of bacterial bioreporters for heavy metals. Bioengineered Bugs 2010, 1:132-138.
42. van Hullebusch E.D., Zandvoort M.H., Lens P.N.L. Metal immobilization by biofilms: mechanisms and analytical tools. Reviews in Environmental Science and Biotechnology 2003, 2:9-33.
43. Ivask A., Rolova T., Kahru A. A suite of recombinant luminescent bacterial strains for the quantification of bioavailable heavy metals and toxicity testing. BMC Biotechnology 2009, 9:41.
44. Iyer A., Mody K., Jha B. Accumulation of hexavalent chromium by an exopolysaccharide producing marine Enterobacter cloaceae. Marine Pollution Bulletin 2004, 49:974-977.
45. Jarvie A.W. Organoleads in the environment: a review. Science of the Total Environment 1988, 73:121-126.
46. Kassab D.M., Roane T.M. Differential responses of a mine tailings Pseudomonas isolate to cadmium and lead exposures. Biodegradation 2006, 17:379-387.
47. Lam T.V.P., Agovino X.N., Roche L. Linkage study of cancer risk among lead exposed workers in New Jersey. Science of the Total Environment 2007, 372:455-462.
48. Levinson H.S., Mahler I. Phosphatase activity and lead resistance in Citrobacter freundii and Staphylococcus aureus. FEMS Microbiology Letters 1998, 161:135-138.
49. Levinson H.S., Mahler I., Blackwelder P., Hood T. Lead resistance and sensitivity in Staphylococcus aureus. FEMS Microbiology Letters 1996, 145:421-425.
50. Liu T., Nakashima S., Hirose K., Uemura Y., Shibasaka M., Katsuhara M., Kasamo K. A metallothionein and CPx-ATPase handle heavy-metal tolerance in the filamentous cyanobacteria Oscillatoria brevis. FEBS Letters 2003, 542:159-163.
51. Lombardi P.E., Peri S.I., Verrengia N.R. ALA-D and ALA-D reactivated as biomarkers of lead contamination in the fish Prochilodus lineatus. Ecotoxicology and Environmental Safety 2010, 73:1704-1711.
52. Macaskie L.E., Dean A.C. Trimethyl lead degradation by free and immobilized cells of an Arthrobacter sp. and by wood decay fungus Phaeolus schweinitzii. Applied Microbiology and Biotechnology 1990, 33:81-87.
53. Mire C.E., Tourjee J.A., O'Brien W.F., Ramanujachary K.V., Hecht G.B. Lead precipitation by Vibrio harveyi: evidence for novel quorum-sensing interactions. Applied Microbiology and Biotechnology 2004, 70:855-864.
54. Morillo J.A., Aguilera M., Ramoz-Cormenzana A., Monteoliva S.M. Production of metal-binding exopolysaccharide by Paenibacillus jamilae using two-phase olive-mill waste as fermentation substrate. Current Microbiology 2006, 53:189-193.
55. Morillo J.A., Garcia-Ribera R., Quesada T., Aguilera M., Ramos-Cormenzana A., Monteoliva-Sanchez M. Biosorption of heavy metals by the exopolysaccharide produced by Paenibacillus jamilae. World Journal of Microbiology and Biotechnology 2008, 24:2699-2704.
56. Naik M.M., Dubey S.K. Lead-enhanced siderophore production and alteration in cell morphology in a Pb-resistant Pseudomonas aeruginosa strain 4EA. Current Microbiology 2011, 62:409-414.
57. Naik M.M., Pandey A., Dubey S.K. Pseudomonas aeruginosa strain WI-1 from Mandovi estuary possesses metallothionein to alleviate lead toxicity and promotes plant growth. Ecotoxicology and Environmental Safety 2012, 79:129-133.
58. Naik M.M., Pandey A., Dubey S.K. Biological characterization of lead-enhanced exopolysaccharide produced by a lead resistant Enterobacter cloacae strain P2B. Biodegradation 2012, 23:775-783.
59. Naik M.M., Shamim K., Dubey S.K. Biological characterization of lead resistant bacteria to explore role of bacterial metallothionein in lead resistance. Current Science 2012, 103:1-3.
60. +2 as lead phosphate. Letters in Applied Microbiology 2013, 56:99-104.
61. Nair S., Chandramohan D., Loka Bharathi P.A. Differential sensitivity of pigmented and non-pigmented marine bacteria to metals and antibiotics. Water Research 1992, 26:431-434.
62. Namiranian S., Richardson D.J., Russell D.A., Sodeau J.R. Excited state properties of siderophore pyochelin and its complex with zinc ions. Photochemistry and Photobiology 1977, 65:777-782.
63. Neumann G., Veeranagauda Y., Karegoudar T.B., Sahin O., Mausezahl I., Kabelitz N., Kappelmeyer U., Heipieper H,J. Cells of Pseudomonas putida and Enterobacter sp. adapt to toxic organic compounds by increasing their size. Extremophiles 2005, 9:163-168.
64. Nies D.H., Silver S. Ion efflux systems involved in bacterial metal resistance. Journal of Industrial Microbiology 1995, 14:186-199.
65. Nies D.H. Microbial heavy-metal resistance. Applied Microbiology and Biotechnology 1999, 51:730-750.
66. Nies D.H. Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiology Reviews 2003, 27:313-339.
67. Pal A., Paul A.K. Microbial extracellular polymeric substances: central elements in heavy metal bioremediation. Indian Journal of Microbiology 2008, 48:49-64.
68. Park J.H., Bolan N., Meghraj M., Naidu N. Concomitant rock phosphate dissolution and lead immobilization by phosphate solubilising bacteria (Enterobacter sp.). Journal of Environmental Management 2011, 92:1115-1120.
69. Park J.H., Bolan N., Meghraj M., Naidu N., Chung J.W. Bacterial-assisted immobilization of lead in soils: implications for remediation. Pedologists 2011, 162-174.
70. Rensing C., Ghosh M., Rosen B.P. Families of soft-metal-ion-transporting ATPases. Journal of Bacteriology 1999, 181:5891-5897.
71. Roane T.M. Lead resistance in two bacterial isolates from heavy metal-contaminated soils. Microbial Ecology 1999, 37:218-224.
72. Rossbach S., Wilson T.L., Kukuk M.L., Carty H.A. Elevated zinc induces siderophore biosynthesis genes and a zntA-like gene in Pseudomonas fluorescens. FEMS Microbiology Letters 2000, 191:61-70.
73. Sharma S., Sundaram C.S., Luthra P.M., Singh Y., Sirdeshmukh R., Gade W.N. Role of proteins in resistance mechanism of Pseudomonas fluorescens against heavy metal induced stress with proteomics approach. Journal of Biotechnology 2006, 126:374-382.
74. Shahid M., Pinelli E., Dumat C. Review of Pb availability and toxicity to plants in relation with metal speciation; role of synthetic and natural organic ligands. Journal of Hazardous Materials 2012, 219:1-12.
75. Sinha S., Mukherjee S.K. Cadmium-induced siderophore production by a highly Cd-resistant bacterial strain relieved Cd toxicity in plants through root colonization. Current Microbiology 2008, 56:55-60.
76. Srivastava N.K., Majumder C.B. Novel biofiltration methods for the treatment of heavy metals from industrial wastewater. Journal of Hazardous Materials 2008, 151:1-8.
77. Sun G.X., Zhou W.Q., Zhong J.J. Organotin decomposition by Pyochelin, secreted by Pseudomonas aeruginosa even in an iron-sufficient environment. Applied and Environmental Microbiology 2008, 72:6411-6413.
78. Taghavi S., Lesaulnier C., Monchy S., Wattiez R., Mergeay M., van der Lelie D. Lead (II) resistance in Cupriavidus metallidurans CH34: interplay between plasmid and chromosomally-located functions. Antonie van Leeuwenhoek 2009, 96:171-182.
79. Tauriainen S., Karp M., Chang W., Virta M. Luminescent bacterial sensor for cadmium and lead. Biosensors and Bioelectronics 1998, 13:931-938.
80. Teeling H., Cypionka H. Microbial degradation of tetraethyl lead in soil monitored by microcalorimetry. Applied and Environmental Microbiology 1997, 48:275-279.
81. Tong S., von Schirnding Y.E., Prapamontol T. Environmental lead exposure: a public health problem of global dimensions. Bulletin of the World Health Organization 2000, 78:1068-1077.
82. Trajanovska S., Britz M.L., Bhave M. Detection of heavy metal ion resistance genes in gram-positive and gram-negative bacteria isolated from a lead-contaminated site. Biodegradation 1997, 8:113-124.
83. +2-sensing by the cyanobacterial metallothionein repressor SmtB: different motifs mediate metal-induced protein-DNA dissociation. Nucleic Acids Research 1996, 24:3714-3721.
84. Voleski B. Advances in biosorbtion of metals: selection of biomass type. FEMS Microbiology Reviews 1994, 14:291-302.
85. Wang W., Shao Z., Liu Y., Wang G. Removal of multi-heavy metals using biogenic manganese oxides generated by a deep-sea sedimentary bacterium Brachybacterium sp. strain Mn32. Microbiology 2009, 155:1989-1996.
86. Watt G.C.M., Britton A., Gilmour H.G., Moore M.R., Murray G.D., Robertson S.J. Public health implications of new guidelines for lead in drinking water: a case study in an area with historically high water lead levels. Food and Chemical Toxicology 2000, 38:73-79.
87. Xu Z., Lei Y., Patel J. Bioremediation of soluble heavy metals with recombinant Caulobacter crescentus. Bioengineered Bugs 2012, 1(3):207-212.
88. Yamoka Y., Inoue H., Takimura O., Oota S. Effect of iron on the degradation of triphenyltin by pyoverdines isolated from Pseudomonas chlororaphis. Organometallic Chemistry 2002, 16:277-279.
89. Zanardini E., Andreoni V., Borin S., Cappitelli F., Daffonchio D., Talotta P., Sorlini C., Ranalli G., Bruni S., Cariati F. Lead resistant microorganisms from red stains of marble of the Certosa of Pavia, Italy and use of nucleic acid based techniques for detection. International Biodeterioration and Biodegradation 1998, 40:171-182.
90. Zucconi L., Ripa C., Alianiello F., Benedetti A., Onofri S. Lead resistance, sorption and accumulation in a Paecilomyces lilacinus strain. Biology and Fertility of Soils 2003, 37:17-22.