Heavy Metal Resistance by Endophytic Bacteria Isolated from Guava (Psidium Guajava) and Mango (Mangifera Indica) Leaves

  • Maryam Lami Riskuwa-Shehu Department of Microbiology, Faculty of Science, Usmanu Danfodiyo University Sokoto
  • Haruna Yahaya Ismail Department of Microbiology, Faculty of Science, University of Maiduguri http://orcid.org/0000-0003-0190-4338
  • Udem Joshua Josiah Ijah Department of Microbiology, Federal University of Technology, Minna, Niger State


Heavy metal resistant bacteria are widespread in nature and their application in decontamination of polluted ecosystems is promising. In this study, ability of endophytic bacteria isolated from Psidium guajava (Guava) and Mangifera indica (Mango) for heavy metal resistance was assessed. Leaves samples form the two plants were collected and processed according to the standard laboratory practices. Heavy metals were analyzed using Atomic absorption spectrophotometer. Endophytic bacteria were isolated and identified using morphological and biochemical characteristics; heavy metal resistance was determined by plate dilution method. Heavy metal analysis revealed that the leaves samples contained considerable quantities of Manganese (Mn), Lead (Pb) and Cadmium (Cd) ranging from 1.21±1.6 mg/Kg (for Cd in Guava leaves) to 116.58±1.3 mg/Kg (for Mn in Mango leaves). A total of six bacterial species were isolated from both of the plants leaves (3 each). Guava endophytes were identified as Streptococcus sp, Staphylococcus albus and Staphylococcus seiuri whereas Staphylococcus aureus, Staphylococcus xylulose and Staphylococcus intermedius were from Mango leaves. The identified isolates were tested for ability to resist heavy metals in-vitro and were capable of showing different patterns of resistance to MnCl2, PbCl2 and CdCl2.  All the endophytes were highly resistant to PbCl2 followed by MnCl2 but susceptible to CdCl2. The ability of plants and bacterial endophytes understudy to tolerate or resist heavy metals is a good indication of their phytoremediation potentials and thus, should be harnessed.

Keywords: Endophytes, Cadmium, Resistance, Manganese, Lead, Bioaccumulation


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  1. Lazo, E. Steinnes, F. Qarri, S. Allajbeu, S. Kane, T. Stafilov, M. V. Frontasyeva, H. Harmens. “Origin and spatial distribution of metals in moss samples in Albania: A hotspot of heavy metal contamination in Europe” Chemosphere, 9:135, 2017.

  2. Patel, N. Janardhana Raju, B. C. Sundara Raja Reddy. U. Suresh . D. B. Sankar . T. V. K. Reddy. “Heavy metal contamination in river water and sediments of the Swarnamukhi River Basin, India: risk assessment and environmental implications” Environ Geochem Health; 2017.

  3. N. Ihedioha . P. O. Ukoha . N. R. Ekere. “Ecological and human health risk assessment of heavy metal contamination in soil of a municipal solid waste dump in Uyo, Nigeria” Environ Geochem Health; 2016.

  4. Dash, S. S. Borah, A. Kalamdhad. “A modified indexing approach for assessment of heavy metal contamination in Deepor Beel, India” Ecological Indicators 106:105444; 2019.

  5. Heritage, Evans, E. G. V. and Killington, R. A. “The microbiology of soil and nutrient recycling” Inc. Microbiology in Action. Cambridge University Press, UK; 1999.

  6. Mishra, R. N. Bharagava, N. More, A. Yadav, S. Zainith, S. Mani, P. Chowdhary, “Heavy Metal Contamination: An Alarming Threat to Environment and Human Health” In: R. C. Sobti et al. (eds.), Environmental Biotechnology: For Sustainable Future, 2019.

  7. Koller, H. M. Saleh, “Introductory chapter: introducing heavy metals” In: M. H. Saleh, R. F. Aglan, (eds) “heavy metals“ IntechOpen, 2018.

  8. O. Duruibe, M. O. C. Ogwuegbu, J. N. Egwurugwu. “Heavy metal pollution and human biotoxic effects” International Journal of physical sciences; 2(5):112-118, 2007.

  9. WHO “Health risks of heavy metals from long-range transboundary air pollution” Joint WHO/Convention Task Force on the Health Aspects of Air Pollution. WHO, Regional Office, Europe; 2007.

  10. L-M. Cai, Q. Wang, J. Luo , L-G. Chen, R-L. Zhu, S. Wang, C. Tang, “Heavy metal contamination and health risk assessment for children near a large Cu-smelter in central China” Science of the Total Environment ;650: 725–733; 2019.

  11. Vassilev, Schwitzguébel, J., Thewys, T., Lelie, D. V. and Vangronsveld, J. “The use of plants for remediation of metal- contaminated soils” The Scientific World Journal 4, 9–34, 2004.

  12. Xiao, S. Wang, R. Li, J. J. Wang, Z. Zhang, “Soil heavy metal contamination and health risks associated with artisanal gold mining in Tongguan, Shaanxi, China” Ecotoxicology and Environmental Safety, 141:17–24; 2017.

  13. Masindi, and K. L. Muedi, ‘’Environmental contamination by heavy metals” In: H. F. Saleh, and R. F. Aglan (eds) Heavy metals. Intechopen, 2018.

  14. Volesky, “Biosorption and Biosorbents”. In: Biosorption of heavy metals. B. Volesky (ed.) CRC Press, Boca Raton, Florida) 3-5, 1990.

  15. L. Riskuwa-Shehu, H. Y. Ismail, M. Suleiman, “Biosorption of Heavy Metals by Oscillatoria Species” Microbiology Research Journal International; 27(6): 1-8, 2019.

  16. K. Bhattacharya, Manda, S. N. and Das, S. K. “Heavy metals accumulation in water sediment and tissues of different edible fishes in upper stretch of gangetic west Bengal” Trends in Applied Science Research 3, 61-68, 2008.

  17. M. Ogbo, and J. A. Okhuoya, “Bio-absorption of some heavy metals by Pleurotus tuber-regium Fr. Singer (an Edible Mushroom) from crude oil polluted soils amended with fertilizers and cellulosic wastes” International Journal of Soil science; 6, 34-48, 2011.

  18. C. Patel, Goulhen, F., Boothman, C., Gault, A. G., Charnock, J. M., Kalia, K. and J. R. Lloyd, “Arsenate detoxification in a Pseudomonad hypertolerant to arsenic. Archives of Microbiology, 187: 171–183, 2007.

  19. Banerjee, Gothalwal, R., Sah, P. K. and S. Sao, “Microbial observation in bioaccumulation of heavy metals from the ash dyke of thermal power plants of chhattisgarh, India” Adv. in Bioscience and Biotech. 6, 131-138, 2015.

  20. Li, D. Meng, J. Li, H. Yin, H. Liu, X. Liu, C. Cheng, Y. Xiao, Z. Liu, M. Yan, “Response of soil microbial communities and microbial interactions to long-term heavy metal contamination” Environmental Pollution 231: 908e917, 2017.

  21. Issazadeh, Pahlaviani, M. K. and A. Massiha, Bioremediation of toxic heavy metals pollutants by Bacillus spp. isolated from Guilan Bay sediments, North of Iran. International Conference on Biotechnology and Environment Management ICBEE, 18, 67-71, 2011.

  22. Tang, J. Zhang, L. Ren, Y. Zhou, J. Gao, L. Luoa, Y. Yang, Q. Peng, H. Huang, A. Chen, “Diagnosis of soil contamination using microbiological indices: A review on heavy metal pollution” Journal of Environmental Management 242:121–130, 2019.

  23. A. C. Da Costa, and P. F. Duta, "Bioaccumulation of Copper, Zinc, Cadmium and Lead by Bacillus sp., Bacillus cereus, Bacillus sphaerecus and Bacillus subtilis” Brazilian Journal of Microbiology 32, 1-5, 2001.

  24. Pardo, Herguedas, M. and E. Barrado, “Biosorption of cadmium, copper, lead and zinc by inactive biomass of Pseudomonas putida” Analytical and Bioanalytical Chemistry, 376: 26-32, 2003.

  25. Sevgi, Coral, G., Gizir, A. M. and A. Sangun, “Investigation of heavy metal resistance in some bacterial strains isolated from industrial soils” Turkish Journal of Biology, 34: 423-43, 2010.

  26. A. Oyewole, S. S. L. Zobeashi, E. O. Oladoja, R. O. Raji, E. E. Odiniya, A. M. Musa. “Biosorption of heavy metal polluted soil using bacteria and fungi isolated from soil” SN Applied Sciences, 1:857; 2019.

  27. Volesky, and Z. R. Holan, “Biosorption of heavy metals. Biotechnology Progress, 11:235–250, 1995.

  28. M. Sulaimon, Odeyemi, A. T., Ogunjobi, A. A. and I. O. Ibrahim, “Bioaccumulation of heavy metals using selected heavy metal tolerant organisms isolated from dumpsite leachate” Nature and Science, 12(10):101-106, 2014.

  29. N. Azizi, Colagar, A. H. and S. M. Hafeziyan, “Removal of Cd (II) from Aquatic System Using Oscillatoria sp. Biosorbent” The Scientific World Journal, 1-7, 2012.

  30. U. Mustapha, N. Halimoon, “Microorganisms and biosorption of heavy metals in the environment: a review Paper” J Microb Biochem Technol 7:253–256, 2015.

  31. Wang, and C. Chen, “Biosorbents for heavy metals removal and their future” Biotechnology Advances, 27(2):195–226, 2009.

  32. Diep, R. Mahadevan, A. F. Yakunin, “Heavy Metal Removal by Bioaccumulation Using Genetically Engineered Microorganisms” Frontiers in Bioengineering and Biotechnology, 6(157):1-20; 2018.

  33. Ahmed, and A. Malik, “Bioaccumulation of heavy metals by zinc resistant bacteria isolated from agricultural soils irrigated with wastewater” Bacteriology Journal, 2, 12-21, 2011.

  34. E. Elsilk, Elshanshoury, A. R. and P. S. Ateya, “Accumulation of heavy metal resistant avirulent Bacillus anthracis PS2010 isolated from Egypt” African Journal of Microbiology Research, 8(12):1266-1276, 2014.

  35. Mishra, A., and Malik, A. Recent advances in microbial metal bioaccumulation. Crit. Rev. Environ. Sci. Technol. 43, 1162–1222, 2013.

  36. K. Singh, P. P. Singh, A. Gupta, A. K. Singh, J. Keshri, “Tolerance of Heavy Metal Toxicity Using PGPR Strains of Pseudomonas Species” In: PGPR Amelioration in Sustainable Agriculture, 2019.

  37. Z. Alam and S. Ahmad, “Chromium removal through biosorption and bioaccumulation by bacteria from tannery effluents contaminated soil” Clean-Soil Air Water, 39: 226-237, 2011.

  38. Congeevaram, Dhanarani, S., Park, J., M. Dexilin, and K. Thamaraiselvi, “Biosorption of chromium and nickel by heavy metal resistant fungal and bacterial isolates” J. of Hazardous Materials, 146: 270-277. 2007.

  39. Usmani, and H. Sultana, “Use of microalgae for the removal of environmental pollutants” International Journal of Scientific World, 3 (1): 1-11, 2015.

  40. Inuwa, Abdulrahman, F. W., Birnin-Yauri, U. A. and S. A. Ibrahim, “Analytical Assessment of some Trace Metals in Soils around Industrial Areas of North West Nigeria” Trends in Applied Science Research, 2(6):515-521, 2007.

  41. Khan, S. Z., Doty, L., Brian, O., Gang, X., Jun, W. K., Glenda, S., Azra, V. and James, T. S. “Diazotrophic endophytes of native black cottonwood and willow” Symbiosis 47(1):23-33, 2005.

  42. Fan, Z. Liu, L. Nan, E. Wang, W. Chen, Y. Lin, G. Wei, “Isolation, characterization, and selection of heavy metal-resistant and plant growth-promoting endophytic bacteria from root nodules of Robinia pseudoacacia in a Pb/Zn mining area” Microbiological Research, 2018.

  43. B. Oyeleke, and S. B. Manga, “Essentials of Laboratory Practicals in Microbiology” Tobest Publisher Minna, Nigeria, 2008.

  44. I. Barrow, and K. A. Feltham, “Cowan and Steel’s manual for identification of medical bacteria” 33rd  edition. London, Cambridge University Press, 1993.

  45. H. Ibrahim, Birnin-Yauri, U. A., Muhammad, C. and A. Umar, “Assessment of pollution potentialities of some portland cement” Nigerian Journal of Basic and Applied Science 20(2): 182-184, 2012.

  46. Basset, Denny, R. C., Jeffery, G. H. and J. Mendham, “Vogel’s Textbook of quantitative inorganic analysis including elementary instrumental analysis” 4th edition, Longman Publishing Co. Inc. London PP 35 – 40, 1997.

  47. U. Khan, Angela, S., Muhammad, H., Kaneez, F., AsmaImran, M. A., Ghulam, S., Qaiser, M. K. and A. Muhammad, “Cr-resistant rhizo- and endophytic bacteria associated with Prosopis juliflora and their potential as phytoremediation enhancing agents in metal-degraded soils” Frontiers in Plant Science 5(755):1-10, 2015.

  48. Liu, H. Lin, Y. Dong, B. Li, L. Wang, “Identification and characterization of plant growth–promoting endophyte RE02 from Trifolium repens L. in mining smelter” Environmental Science and Pollution Research, 26:17236–17247; 2019.

  49. Stępniewska, and A. Kuźniar, “Endophytic microorganisms— promising applications in bioremediation of greenhouse gases” Appl Microbiol Biotechnol. 97 (22):9589–96, 2013.

  50. V. Sturtz, Christie, B. R. and J. Nowak, “Bacterial endophytes: potential role in developing sustainable systems of crop         production” Journal of Critical Revolution on Plant Science 19: 1–30, 2000.

  51. Q. Hung, and K. Annapurna, “Isolation and characterization of endophytic bacteria in soybean (Glycine SP.)” Omonrice 12: 92-101, 2004.

  52. K. Zinniel, Lambrecht, P., Harris, N. B., Feng, Z., Kuczmarski, D., Higley, P., Ishimaru, C. A., Arunakumari, A., Barletta, R. G. and A. K. Vidaver, “Isolation and characterization of endophytic colonizing bacteria from agronomic crops and prairie plants” Appl. Environ. Microbiol. 68:2198-2208, 2002.

  53. K. Elbeltagy, Nishioka, H. S., Sato, T., Sato, Y. I., Morisaki, H., H. Mitsui, and K. Minamisawa, “Isolation and characterization of endophytic bacteria from wild and traditionally cultivated rice varieties” Soil Sci. Plant Nutr. 46:617-629, 2000.

  54. L. Riskuwa-Shehu, and H. Y. Ismail, “Isolation of endophytic bacteria and phytoremediation of soil contaminated with polycyclic aromatic hydrocarbons using Cajanus cajan and Lablab purpereus” Bioremediation Science and Technology Research; 6(1):26-30, 2018.

  55. R. Hardoim, Van Overbeek, L. S. and J. D. Elsas, “Properties of bacterial endophytes and their proposed role in plant growth”. Trends Microbiol. 16(10):463–71, 2008.

  56. Jan, Khan, M.A.; Asaf, S.; Lubna; Lee, I.-J.; K. M. Kim, “Metal Resistant Endophytic Bacteria Reduces Cadmium, Nickel Toxicity, and Enhances Expression of Metal Stress Related Genes with Improved Growth of Oryza Sativa, via Regulating Its Antioxidant Machinery and Endogenous Hormones” Plants, 8:363, 2019.

  57. H. Dalhat, A. R. Amale, M. Maimuna, I. Bashiru, K. Sirajo, “Comparative Study of Mineral and Phytochemical Analysis of Soil and Lactuca sativa Grown in the Vicinity of Cement Company of Northern Nigeria (Sokoto Cement) and Usmanu Danfodiyo University Sokoto (Kwalkwalawa)” Asian Journal of Research in Biochemistry, 1(1):1-10, 2017.

  58. Abdullahi, Usman, Y., Noma, S. S., Audu, M., Danmoma, N. M. and R. S. Shuaibu, “Fertility status of fadama soils in gantsare village, wamakko local government, sokoto state as affected by cement dust” Nig. J. Basic & Applied Sci. 18(1):58-64, 2010.

  59. Abdelkrim, S. H. Jebara, O. Saadani, Heavy metal accumulation in Lathyrus sativus growing Heavy metal accumulation in Lathyrus sativus growing Arch Microbiol. 201: 107. 2019.

  60. H. O. Ernst, Evolution of metal hyperaccumulation and phytoremediation hype. New Phytology, 146, 357– 358, 2000.

  61. Goris, De Vos, P., Coenye, T., Hoste, B., Janssens, D., Brim, H., Diels, L., Mergeay, M., Kersters, K. and P. Vandamme, “Classification of metal-resistant bacteria from industrial biotopes as Ralstonia campinensis sp. nov., Ralstonia metallidurans sp. nov. and Ralstonia basilensis” Int. J. of Syst. and Evol. Microbiol. 51:1773-1782, 2001.

  62. Gupta, Phung, L., Chakravarty, L. and S. Silver, “Mercury resistance in Bacillus cereus RC607: Transcriptional organization and two new open reading frames” Journal of Bacteriology, 181: 7080-7086, 1999.

  63. Zolgharnein, Azmi, M. L., Saad, M. Z., Mutalib, A. R. and C. A. R. Mohamed, “Detection of plasmids in heavy metal resistance bacteria isolated from the Persian Gulf and enclosed industrial areas” Iranian Journal of biotechnology, 5:232-239, 2007.

  64. E. Raja, Anbazhagan, K. and Selvam, G. S. “Isolation and characterization of a metal-resistant Pseudomonas aeruginosa strain”. World Journal of Microbiology & Biotechnology, 22: 577–585, 2006.

How to Cite
M. Riskuwa-Shehu, H. Ismail, and U. Ijah, “Heavy Metal Resistance by Endophytic Bacteria Isolated from Guava (Psidium Guajava) and Mango (Mangifera Indica) Leaves”, Int. Ann. Sci., vol. 9, no. 1, pp. 16-23, Nov. 2019.
Research Article