Research Article

A Gateway to Metal Resistance: Bacterial Response to Heavy Metal Toxicity in the Biological Environment

Loai Aljerf* and Nuha AlMasri

Published: 09/03/2018 | Volume 2 - Issue 1 | Pages: 017-044

Abstract

Heavy metals and metalloids are dangerous because they have the tendency to bioaccumulate in biological organisms over a period of time. However, it is conceived that a number of phytochemical agents as well microorganism can act as heavy metal removing agent both from human beings and the environment surrounding. For instance, microbes are used for the removal of heavy metals from the water bodies including bacteria, fungi, algae and yeast. This review shows that bacteria can play an important role in understanding the uptake and potential removal behaviour of heavy metal ions. The bacteria are chosen based on their resistance to heavy metals (incl. their toxicities) and capacity of adsorbing them. Due to specific resistance transfer factors, cell impermeability is drastically inhibited by several ion (i.e. mercury, cadmium, cobalt, copper, arsenic) forms. Between these elements, free-ion cadmium and copper concentrations in the biological medium provide more accurate determination of metal concentrations that affect the bacteria, than with most of the other existing media. Metal toxicity is usually assessed by using appropriate metal ion chelators and adjusting pH factor. Bacteria and metals in the ecosystem can form synergistic or antagonistic relationships, supplying each other with nutrients or energy sources, or producing toxins to reduce growth and competition for limiting nutritional elements. Thus, this relation may present a more sustainable approach for the restoration of contaminated sources.

Read Full Article HTML DOI: 10.29328/journal.aac.1001012 Cite this Article

References

  1. Jung H. Nutrients and heavy metals contamination in an urban estuary of northern New Jersey. Geosciences. 2017; 7: 108. Ref.: https://tinyurl.com/ycnj3936
  2. Aljerf L, Choukaife AE. Review: Assessment of the doable utilisation of dendrochronology as an element tracer technology in soils artificially contaminated with heavy metals. Biodiversity International Journal. 2018; 2: 1-8. Ref.: https://tinyurl.com/yc3hkbnl
  3. Mustafa G, Komatsu S. Toxicity of heavy metals and metal-containing nanoparticles on plants. Biochim Biophys Acta. 2016; 1864: 932-944. Ref.: https://tinyurl.com/y8zo7dbq
  4. Aljerf L, Al Masri N. Mercury toxicity: ecological features of organic phase of mercury in biota-Part I. Archives of Organic and Inorganic Chemical Sciences. 2018; 3: 1-8. Ref.: https://tinyurl.com/yazn237c
  5. Jadoon S, Malik A. DNA damage by heavy metals in animals and human beings: an overview. Biochem Pharmacol. 2017; 6: 1-8. Ref.: https://tinyurl.com/yartpqd9
  6. Warburg O. Heavy metal prosthetic groups and enzyme action. Soil Sci. 1950; 70: 166. Ref.: https://tinyurl.com/ybqu4znr
  7. Lalotra P. Bioaccumulation of heavy metals in the sporocarps of some wild mushrooms. Curr Res Environ Appl Mycol J Fungal Biol. 2016; 6: 159-165. Ref.: https://tinyurl.com/y7733ojc
  8. Aljerf L. Advanced highly polluted rainwater treatment process. Journal of Urban and Environmental Engineering. 2018.
  9. Stasinos S, Nasopoulou C, Tsikrika C, Zabetakis I. The bioaccumulation and physiological effects of heavy metals in carrots, onions, and potatoes and dietary implications for Cr and Ni: A review. J Food Sci. 2014; 79: 765-780. Ref.:  https://tinyurl.com/ya4cegqp
  10. Shah SA. Trace minerals and heavy metals: implications in prostate cancer. Bangl J Med  Biochem. 2017; 8: 27. Ref.: https://tinyurl.com/ybtxln4j
  11. Bjørklund G, Mutter J, Aaseth J. Metal chelators and neurotoxicity: lead, mercury, and arsenic. Arch Toxicol. 2017; 91: 3787-3797. Ref.: https://tinyurl.com/y9dlr5u2
  12. Feingold A. The elimination of volatile substances from the lungs. Int Anesthesiol Clin. 1977; 15: 153-168. Ref.: https://tinyurl.com/ydhge79v
  13. Sato Y. The pathological findings of placenta with neonatal placenta. Placenta. 2017; 59: 169. Ref.: https://tinyurl.com/yc7oneo3
  14. De J, Ramaiah N, Vardanyan L. Detoxification of toxic heavy metals by marine bacteria highly resistant to mercury. Mar Biotechnol. 2008; 10: 471-477. Ref.: https://tinyurl.com/y77bkov7
  15. Robinson T. Removal of toxic metals during biological treatment of landfill leachates. Waste Manage. 2017; 63: 299-309. Ref.: https://tinyurl.com/ybcsnoy8
  16. Aljerf L. High-efficiency extraction of bromocresol purple dye and heavy metals as chromium from industrial effluent by adsorption onto a modified surface of zeolite: kinetics and equilibrium study. Journal of Environmental Management. 2018. Ref.:  https://tinyurl.com/y7zos28k
  17. Soltani N, Shaheli M. Cow milk contamination with heavy metals (mercury and lead) and the possibility of heavy metals disintegration by the human intestinal bacteria. J Med Microbiol Diag. 2017; 6: 267. Ref.:  https://tinyurl.com/yazt4xew
  18. Mathew R, College SM, Krishnaswamy VG. Remediation of mixed heavy metals using acido-tolerant bacterial co-cultures. Int J Agric Environ Sci. 2017; 4: 43-52. Ref.: https://tinyurl.com/ybjyax2w
  19. Waturangi DE, Rahayu BS, Lalu KY, Mulyono N. Characterization of bioactive compound from actinomycetes for antibiofilm activity against Gram-negative and Gram-positive bacteria. Malays J Microbiol. 2016; 12: 291-299. Ref.:  https://tinyurl.com/y954g78q
  20. Puyen ZM, Villagrasa E, Maldonado J, Diestra E, Esteve I, et al. Biosorption of lead and copper by heavy-metal tolerant Micrococcus luteus DE2008. Bioresour Technol. 2012; 126: 233-237. Ref.: https://tinyurl.com/ycsqrvno
  21. Barrow W, Himmel M, Squire PG, Tornabene TG. Evidence for alteration of the membrane-bound ribosomes in Micrococcus luteus cells exposed to lead. Chem Biol Interact. 1978; 23: 387-397. Ref.: https://tinyurl.com/y9vj62hn
  22. Bishop R. Bacterial lipids. Biochim Biophys Acta. 2016; 1862: 1285-1286. Ref.: https://tinyurl.com/ydhs6r97
  23. Gautam S, Sood NK, Gupta K. Aberrant cytoplasmic accumulation of retinoblastoma protein in basal cells may lead to increased survival in malignant canine mammary tumours. Vet Med. 2018; 59: 76-80. Ref.: https://tinyurl.com/ybgurms5
  24. Owen P, Salton MRJ. Isolation and characterization of a mannan from mesosomal membrane vesicles of Micrococcus lysodeikticus. Biochim Biophys Acta 1975; 406: 214-234. Ref.:  https://tinyurl.com/yb3aucpg
  25. Saxena G, Flora SJS. Lead-induced oxidative stress and hematological alterations and their response to combined administration of calcium disodium EDTA with a thiol chelator in rats. J Biochem Mol Toxicol. 2004; 18: 221-233. Ref.:  https://tinyurl.com/ydx8su6m
  26. Nielsen AM, Sojka GA. Photoheterotrophic utilization of acetate by the wild type and an acetate-adapted mutant of Rhodopseudomonas capsulata. Arch Microbiol. 1979; 120: 39-42. Ref.: https://tinyurl.com/yd2d5j4j
  27. Jaiganesh T, Rani JDV, Girigoswami A. Spectroscopically characterized cadmium sulfide quantum dots lengthening the lag phase of Escherichia coli growth. Spectrochim Acta A. 2012; 92: 29-32. Ref.: https://tinyurl.com/y7xsknvu
  28. Parran DK. Effects of methylmercury and mercuric Chloride on differentiation and cell viability in PC12 cells. Toxicol Sci. 2001; 59: 278-290. Ref.:  https://tinyurl.com/y82hp9a4
  29. Kato F, Tanaka M, Nakamura K. Rapid fluorometric assay for cell viability and cell growth using nucleic acid staining and cell lysis agents. Toxicol In Vitro. 1999; 13: 923-929. Ref.: https://tinyurl.com/ycdm4erf
  30. Mokkapati SK, de Henestrosa ARF, Bhagwat AS. Escherichia coli DNA glycosylase Mug: a growth-regulated enzyme required for mutation avoidance in stationary-phase cells. Mol Microbiol. 2008; 41: 1101-1111. Ref.: https://tinyurl.com/yaadvf7l
  31. Cheng TC. In vivo effects of heavy metals on cellular defense mechanisms of Crassostrea virginica: Total and differential cell counts. J Invertebr Pathol. 1988; 51: 207-214. Ref.: https://tinyurl.com/y8cm89mq
  32. Singleton FL, Guthrie RK. Aquatic bacterial populations and heavy metals-I. Composition of aquatic bacteria in the presence of copper and mercury salts. Water Res. 1977; 11: 639-642. Ref.:  https://tinyurl.com/y7k45ttd
  33. Bradberry SM. Metals (cobalt, copper, lead, mercury). Medicine. 2016; 44: 182-184. Ref.: https://tinyurl.com/ybfj8flz
  34. Albright LJ, Wilson EM. Sub-lethal effects of several metallic salts-organic compounds combinations upon the heterotrophic microflora of a natural water. Water Res. 1974; 8: 101-105. Ref.: https://tinyurl.com/y94cbuds
  35. Anderson DM, Lively JS, Vaccaro RF. Copper complexation during spring phytoplankton blooms in coastal waters. Mar Res. 1984; 42: 677-695. Ref.: https://tinyurl.com/y7lmq5wq
  36. Couillard D, Chartier M, Mercier G. Bacterial leaching of heavy metals from aerobic sludge. Bioresour Technol. 1991; 36: 293-302. Ref.:  https://tinyurl.com/y8a9tcfo
  37. Kobayashi N, Okamura H. Effects of heavy metals on sea urchin embryo development-Part 2 Interactive toxic effects of heavy metals in synthetic mine effluents. Chemosphere. 2005; 61: 1198-1203. Ref.: https://tinyurl.com/y92xphnv
  38. Ipeaiyeda AR, Onianwa PC. Sediment quality assessment and dispersion pattern of toxic metals from brewery effluent discharged into the Olosun river, Nigeria. Environ Earth Sci. 2016; 75: 325. Ref.:  https://tinyurl.com/yb9ty5kw
  39. Aquino SF, Stuckey DC. Bioavailability and toxicity of metal nutrients during anaerobic digestion. Environ Eng. 2007; 133: 28-35. Ref.:  https://tinyurl.com/ydbtwz6u
  40. Shi Y, Qi X, Gao Q. Removal of heavy metals by bacteria in bio-ceramsite and their toxicity to bacteria. Asian J Chem. 2015; 27: 2463-2467. Ref.:   https://tinyurl.com/y7opseds
  41. Mendiguchía C, Moreno C, García-Vargas M. Separation of heavy metals in seawater by liquid membranes: preconcentration of copper. Sep Sci Technol. 2002; 37: 2337-2351. Ref.: https://tinyurl.com/y95hpbgo
  42. Ornaghi F, Ferrini S, Prati M, Giavini E. The protective effects of N-acetyl-L-cysteine against methyl mercury embryo toxicity in Mice. Toxicol Sci. 1993; 20: 437-445. Ref.: https://tinyurl.com/y9f8fryx
  43. Sato C, Leung SW, Schnoor JL. Toxic response of Nitrosomonas europaea to copper in inorganic medium and wastewater. Water Res. 1988; 22: 1117-1127. Ref.: https://tinyurl.com/y8mrco68
  44. McIver CJ, Tapsall JW. Cysteine requirements of naturally occurring cysteine auxotrophs of Escherichia coli. Pathology. 1987; 19: 361-363. Ref.:  https://tinyurl.com/y8ryl9oh
  45. Sprague JB. Promising anti-pollutant: chelating agent NTA protects fish from copper and zinc. Nature. 1968; 220: 1345-1346. Ref.:  https://tinyurl.com/yc998qxb
  46. Shaikh ZA, Blazka ME, Endo T. Metal transport in cells: cadmium uptake by rat hepatocytes and renal cortical epithelial cells. Environ Health Perspect. 1995; 103: 73-75. Ref.:  https://tinyurl.com/y8o5fwqt
  47. Puls RW, Bohn HL. Sorption of cadmium, nickel, and zinc by kaolinite and montmorillonite suspensions1. Soil Sci Soc Am J. 1988; 52: 1289. Ref.:  https://tinyurl.com/y9lqz7py
  48. Hall PL. Adsorption of water by homoionic exchange forms of Wyoming montmorillonite (SWy-1). Clays Clay Miner. 1989; 37: 355-363. Ref.:   https://tinyurl.com/ycfxn6wj    
  49. Leitao JH, Sa-Correia I. Effects of growth-inhibitory concentrations of copper on alginate biosynthesis in highly mucoid Pseudomonas aeruginosa. Microbiology. 1997; 143: 481-488. Ref.: https://tinyurl.com/ybhup42z
  50. Masuda G, Tomioka S, Uchida H, Hasegawa M. Bacteriostatic and bactericidal activities of selected Beta-Lactam antibiotics studied on agar plates. Antimicrob Agents Chemother. 1977; 11: 376-382. Ref.:  https://tinyurl.com/yb6uqfvk
  51. Panda J, Sarkar P. Bioremediation of chromium by novel strains Enterobacter aerogenes T2 and Acinetobacter sp PD 12 S2. Environ Sci Pollut Res. 2011; 19: 1809-1817. Ref.:  https://tinyurl.com/y996ak4h
  52. Sundar K, Sadiq M, Mukherjee A, Chandrasekaran N. Bioremoval of trivalent chromium using Bacillus biofilms through continuous flow reactor. Hazard Mater. 2011; 196: 44-51. Ref.:  https://tinyurl.com/y7nu5yub
  53. Bhaskar RK. Pollutants induced cancer in experimental animals. Int J Sci Res. 2016; 5: 2221-2225. Ref.:  https://tinyurl.com/ya7no6lg
  54. Cenci C, Morozzi G. Evaluation of the toxic effect of Cd2+ and Cd(CN)42− ions on the growth of mixed microbial population of activated sludges. Sci Total Environ. 1977; 7: 131-143. Ref.: https://tinyurl.com/y8xztqyp
  55. Ji G, Silver S. Reduction of arsenate to arsenite by the ArsC protein of the arsenic resistance operon of Staphylococcus aureus plasmid pI258. Proc Natl Acad Sci. 1992; 89: 9474-9478. Ref.: https://tinyurl.com/y73cdwkk
  56. Babai R. An Escherichia coli gene responsive to heavy metals. FEMS Microbiol Lett. 1998; 167: 107-111. Ref.: https://tinyurl.com/y7wgac4q
  57. Tempest DW, Hunter JR, Sykes J. Magnesium-limited growth of Aerobacter aerogenes in a chemostat. J Gen Microbiol. 1965; 39: 355-366. Ref.: https://tinyurl.com/y9ee43vx
  58. Tsai KP. Management of target algae by using copper-based algaecides: effects of algal cell density and sensitivity to copper. Water Air Soil Pollut. 2016; 227: 238. Ref.: https://tinyurl.com/yaz5pwf2
  59. Al-Masoudi WA, Faaz RA, Al-Asadi RH, Jabbar HS. Synthesis, antimicrobial activity and modelling studies of some new metal complexes of Schiff base derived from sulphonamide drug in vitro. Eur J Chem. 2016; 7: 102-106. Ref.: https://tinyurl.com/y7yewfx6
  60. Smit H, van der Goot H, Nauta WT, Timmerman H, de Bolster MW, et al. Mode of action of the copper(I) complex of 2,9-dimethyl-1,10-phenanthroline on Mycoplasma gallisepticum. Antimicrob Agents Chemother. 1981; 20: 455-462. Ref.: https://tinyurl.com/ycszynn2
  61. Harris CM, Patil HRH, Sinn E. Nitrogenous chelate complexes of transition metals. IV Pseudo-tetrahedral copper (II) complexes containing 2,2’-biquinolyl. Inorg Chem. 1967; 6: 1102-1105. Ref.: https://tinyurl.com/y7jvruh8
  62. Milacic V, Jiao P, Zhang B, Dou QP. Novel 8-hydroxylquinoline analogs induce copper-dependent proteasome inhibition and cell death in human breast cancer cells. Int J Oncol. 2009; 35: 1481-1491. Ref.:  https://tinyurl.com/yd4nt7wv
  63. Naka K, Ando D, Chujo Y. Effect of substituent groups for formation of organic-metal hybrid nanowires by charge-transfer of tetrathiafulvalene derivatives with metal ion. Synth Met. 2009; 159: 931-934. Ref.: https://tinyurl.com/yah5oera
  64. Dipu S, Kumar AA, Thanga SG. Effect of chelating agents in phytoremediation of heavy metals. Remed J. 2012; 22: 133-146. Ref.:  https://tinyurl.com/y76gajop
  65. Madoni P, Esteban G, Gorbi G. Acute toxicity of cadmium, copper, mercury, and zinc to ciliates from activated sludge plants. Bull Environ Contam Toxicol. 1992; 49: 900-905. Ref.:  https://tinyurl.com/yd9fkowq
  66. Morgan-Sagastume F, Nielsen JL, Nielsen PH. Substrate-dependent denitrification of abundant probe-defined denitrifying bacteria in activated sludge. FEMS Microbiol Ecol. 2008; 66: 447-461. Ref.: https://tinyurl.com/yau2yrhk
  67. Gu Z, Aikebaier Y, Arefieva V, Mazirov M. Using microbiological leaching method to remove heavy metals from sludge. Eurasian J Soil Sci. 2017; 6: 51-51. Ref.: https://tinyurl.com/y8ptc6j8
  68. Abdulaziz A, Jasmin C, Sheeba VA, Gireeshkumar TR, Shanta N. Heavy metals pollution influence the community structure of Cyanobacteria in nutrient rich tropical estuary. Oceanogr. 2017; 3: 137. Ref.: https://tinyurl.com/yajlpdg3
  69. Chen J, Weimer PJ. Competition among three predominant ruminal cellulolytic bacteria in the absence or presence of non-cellulolytic bacteria. Microbiol. 2001; 147: 21-30. Ref.: https://tinyurl.com/ycqrydhb
  70. Vardy DW, Doering JA, Santore R, Ryan D, Giesy JP, et al. Assessment of Columbia river sediment toxicity to White Sturgeon: concentrations of metals in sediment, pore water and overlying water. J Environ Anal Toxicol. 2014; 5: 263. Ref.: https://tinyurl.com/ybnde9x5
  71. Meger SA. Polluted precipitation and the geochronology of mercury deposition in lake sediment of northern Minnesota. Water Air Soil Pollut. 1986; 30: 411-419. Ref.: https://tinyurl.com/yab68f4l
  72. Sarkar T, Hussain A. Photocytotoxicity of curcumin and its iron complex. Enzyme Eng. 2016; 5: 143. Ref.:  https://tinyurl.com/ya3nzon6
  73. Ottow JCG. Evaluation of iron-reducing bacteria in soil and the physiological mechanism of iron-reduction in Aerobacter aerogenes. Z Allg Mikrobiol. 2007; 8: 441-443. Ref.:   https://tinyurl.com/y8l8hxot
  74. Grass G. Iron Transport in Escherichia Coli: All has not been said and Done. Biometals. 2006; 19: 159-172. Ref.: https://tinyurl.com/y978dbfc
  75. Atieh MA, Ji Y, Kochkodan V. Metals in the environment: toxic metals removal. Bioinorg Chem Appl. 2017; 2017: 1-2. Ref.: https://tinyurl.com/ycx8ftlm
  76. Pongratz R, Heumann KG. Production of methylated mercury, lead, and cadmium by marine bacteria as a significant natural source for atmospheric heavy metals in polar regions. Chemosphere. 1999; 39: 89-102. Ref.: https://tinyurl.com/y7kpgjrp
  77. Maher WA. Determination of inorganic and methylated arsenic species in marine organisms and sediments. Anal Chim Acta. 1981; 126: 157-165. Ref.: https://tinyurl.com/y98qtw6t
  78. Farmer JG. Lead concentration profiles in lead-210 dated Lake Ontario sediment cores. Sci Total Environ. 1978; 10: 117-127. Ref.: https://tinyurl.com/yct52zds
  79. Kobza J. Soil and plant pollution by potentially toxic elements in Slovakia. Plant Soil Environ. 2018; 51: 243-248. Ref.:  https://tinyurl.com/yb7lqkly
  80. Clarkson TW, Stockinger H. Recent advances in the toxicology of mercury with emphasis on the alkylmercurials. Crit Rev Toxicol. 1972; 1: 203-234. Ref.: https://tinyurl.com/ya4mbb6b
  81. Lambertsson L, Nilsson M. Organic material:  the primary control on mercury methylation and ambient methyl mercury concentrations in estuarine sediments. Environ Sci Technol. 2006; 40: 1822-1829. Ref.: https://tinyurl.com/ybus2bxp
  82. Baralkiewicz D, Gramowska H, Gołdyn R. Distribution of total mercury and methyl mercury in water, sediment and fish from Swarze dzkie lake. Chem Ecol. 2006; 22: 59-64. Ref.: https://tinyurl.com/y8xhp5rp
  83. Wright DR, Hamilton RD. Release of methyl mercury from sediments: effects of mercury concentration, low temperature, and nutrient addition. Can J Fish Aquat Sci. 1982; 39: 1459-1466. Ref.: https://tinyurl.com/yd9ugadg
  84. Oswald CJ, Carey SK. Total and methyl mercury concentrations in sediment and water of a constructed wetland in the Athabasca Oil Sands Region. Environ Pollut. 2016; 213: 628-637. Ref.: https://tinyurl.com/ycfsq9wh
  85. Furukawa K, Tonomura K. Induction of metallic mercury-releasing enzyme in mercury-resistant pseudomonas. Agric Biol Chem. 1972; 36: 2441-2448. Ref.: https://tinyurl.com/y8puseek
  86. Furukawa K, Tonomura K. Enzyme system involved in the decomposition of phenyl mercuric acetate by mercury-resistant pseudomonas. Agric Biol Chem. 1971; 35: 604-610. Ref.: https://tinyurl.com/y7z2uaau
  87. Matsumura F, Gotoh Y, Boush GM. Phenylmercuric acetate: metabolic conversion by microorganisms. Science. 1971; 173: 49-51. Ref.: https://tinyurl.com/yamjhjkw
  88. Graham AM, Bullock AL, Maizel AC, Elias DA, Gilmour CC. Detailed assessment of the kinetics of Hg-cell association, Hg methylation, and methylmercury degradation in several Desulfovibrio species. Appl Environ Microbiol. 2012; 78: 7337-7346. Ref.: https://tinyurl.com/y9f52eeg
  89. Alekhin YV, Zagrtdenov NR, Mukhamadiyarova RV. Hg0(liq)-Hg0(solution) equilibrium and solubility of elementary mercury in water. Moscow Univ Geol Bull. 2011; 66: 439-441. Ref.: https://tinyurl.com/y8725ndh
  90. Krul J. Some factors affecting floc formation by Zoogloea ramigera, strain I-16-M. Water Res. 1977; 11: 51-56. Ref.:  https://tinyurl.com/yctttc7l
  91. Bitton G, Freihofer V. Influence of extracellular polysaccharides on the toxicity of copper and cadmium toward Klebsiella aerogenes. Microb Ecol. 1977; 4: 119-125. Ref.:  https://tinyurl.com/ycts6oog
  92. Brandt KK, Petersen A, Holm PE, Nybroe O. Decreased abundance and diversity of culturable Pseudomonas spp. populations with increasing copper exposure in the sugar beet rhizosphere. FEMS Microb Ecol. 2006; 56: 281-291. Ref.: https://tinyurl.com/ydx6oxn9
  93. Tornabene TG, Edwards HW. Microbial uptake of lead. Science. 1972; 176: 1334-1335. Ref.: https://tinyurl.com/y9v7m2hj
  94. Kim SJ. Research papers: Estimation of active nitrosomonas and nitrobacter concentrations in activated sludge using nitrogenous oxygen uptake rate. Environ Eng Res. 2004; 9: 130-142. Ref.: https://tinyurl.com/ycc43336
  95. Yu R, Lai B, Vogt S, Chandran K. Elemental profiling of single bacterial cells as a function of copper exposure and growth phase. PLoS ONE. 2011; 6: e21255. Ref.: https://tinyurl.com/y856j8r2
  96. Tyagi RD. Microbialleachingof metals frommunicipal sludge: Effects of sludge solids concentration. Process Biochem. 1992; 27: 89-96. Ref.: https://tinyurl.com/ydf6lgkg
  97. Komura I, Funaba T, Izaki K. Mechanism of mercuric chloride resistance in microorganisms: II. NADPH-dependent reduction of mercuric chloride and vaporization of mercury from mercuric chloride by a multiple drug resistant strain of Escherichia coli. J Biochem. 1971; 70: 895-901. Ref.:  https://tinyurl.com/y92wdb8x
  98. Rochelle PA, Fry JC, Day MJ. Factors affecting conjugal transfer of plasmids encoding mercury resistance from pure cultures and mixed natural suspensions of Epilithic Bacteria. Microbiol. 1989; 135: 409-424. Ref.: https://tinyurl.com/y9dgtbvu
  99. Guha C, Mookerjee A. RNA synthesis and degradation during preferential inhibition of protein synthesis by cobalt chloride in Escherichia coli K-12. Mol Biol Rep. 1981; 7: 217-220. Ref.: https://tinyurl.com/y9g5sjge
  100. Gotz F, Zabielski J, Philipson L, Lindberg M. DNA homology between the arsenate resistance plasmid pSX267 from Staphylococcus xylosus and the penicillinase plasmid pI258 from Staphylococcus aureus. Plasmid. 1983; 9: 126-137. Ref.: https://tinyurl.com/ybbt4uf7
  101. Diels L, Sadouk A, Mergeay M. Large plasmids governing multiple resistances to heavy metals: A genetic approach. Toxicol Environ Chem.1989; 23: 79-89. Ref.: https://tinyurl.com/yaqcrmoz
  102. Berger NA, Kociolek K, Pitha J. Steric factors in lymphocyte stimulation by organomercurials. Biochem Biophys Res Commun. 1979; 86: 1234-1240. Ref.: https://tinyurl.com/y76h4nuk
  103. Schwager S, Lumjiaktase P, Stöckli M, Weisskopf L, Eberl L. The genetic basis of cadmium resistance of Burkholderia cenocepacia. Environ Microbiol Rep. 2012; 4: 562-568. Ref.: https://tinyurl.com/yacvdrzs
  104. Gillis P. Investigating a potential mechanism of Cd resistance in Chironomus riparius larvae using kinetic analysis of calcium and cadmium uptake. Aquat. Toxicol. 2008; 89: 180-187. Ref.:https://tinyurl.com/y8xwjr5g
  105. Fujiwara K, Iwamoto M, Toda S, Fuwa K. Characteristics of Escherichia coli B resistant to cobaltous ion. Agric Biol Chem. 1977; 41: 313-322. Ref.: https://tinyurl.com/yanhrmjl
  106. Grabow WOK, van Zyl M, Prozesky OW. Behaviour in conventional sewage purification processes of coliform bacteria with transferable or non-transferable drug-resistance. Water Res. 1976; 10: 717-723. Ref.: https://tinyurl.com/y7anmj4m
  107. Varma MM, Thomas WA, Prasad C. Resistance to inorganic salts and antibiotics among sewage-borne enterobacteriaceae and achromobacteriaceae. J Appl Bacteriol. 1976; 41: 347-349. Ref.: https://tinyurl.com/y8hvo6f6
  108. Sinegani AAS, Younessi N. Antibiotic resistance of bacteria isolated from heavy metal-polluted soils with different land uses. J Glob Antimicrob Resist. 2017; 10: 247-255. Ref.: https://tinyurl.com/y8xsd7g3
  109. Nakahara H, Ishikawa T, Sarai Y, Kondo I, Kozukue H, et al. Mercury resistance and R Plasmids in Escherichia coli isolated from clinical lesions in Japan. Antimicrob Agents Chemother. 1977; 11: 999-1003. Ref.: https://tinyurl.com/ycaok7w2
  110. Baquero F. Low-level antibacterial resistance: a gateway to clinical resistance. Drug Resist Update. 2001; 4: 93-105. Ref.: https://tinyurl.com/ybg4xhwr
  111. Yamina B, Tahar B, Laure FM. Isolation and screening of heavy metal resistant bacteria from wastewater: a study of heavy metal co-resistance and antibiotics resistance. Water Sci Technol. 2012; 66: 2041. Ref.: https://tinyurl.com/y86gs5ok
  112. Wales A, Davies R. Co-selection of resistance to antibiotics, biocides and heavy metals, and its relevance to food borne pathogens. Antibiotics. 2015; 4: 567-604. Ref.:  https://tinyurl.com/ya7kogdh
  113. Altug G, Balkis N. Levels of some toxic elements and frequency of bacterial heavy metal resistance in sediment and sea water. Environ Monit Assess. 2008; 149: 61-69. Ref.: https://tinyurl.com/y86tm8gz
  114. Guo T, Baasner J. Technical Note: Using FIMS to determine mercury content in sewage sludge, sediment and soil samples. J Autom Chem. 1996; 18: 221-223. Ref.: https://tinyurl.com/yanwhpfh
  115. Hart M. Diversity amongst Bacillus merA genes amplified from mercury resistant isolates and directly from mercury polluted soil. FEMS Microbiol Ecol. 1998; 27: 73-84. Ref.: https://tinyurl.com/ycu33hfr
  116. Søgaard P. Resistance types in citrobacter freund II occurrence and resistance to ampicillin, carbenicillin, cephalothin and mecillinam. Transfer of ampicillin resistance. Acta Pathol Microbiol Scand B. 2009; 27: 79-83. Ref.: https://tinyurl.com/y7t5cfjk