Characterization of Pb-tolerant Plant-growth-promoting Endophytic Bacteria for Biosorption Potential, Isolated from Roots of Pb Excluders Grown in Different Habitats DOI: 10.32526/ennrj.18.3.2020.25
Article Sidebar
Published:
Jun 2, 2020
Keywords:
Pb biosorption Endophytic bacteria Plant-growth-promoting traits Phytostabilizer
Main Article Content
Abstract
Bioremediation using metal-tolerant plant-growth-promoting endophytic bacteria has been studied. The biosorption potential of endophytic bacteria isolated from roots of non-metalliferous Pb excluders (Acacia mangium and Eucalyptus camaldulensis), and a metalliferous Pb excluder (Pityrogramma calomelanos) was evaluated. Five isolates were selected and designated as “Pc”, “Pe”, “Ai”, “Aj”, and “El”. Phylogenetic reconstruction suggested that strain Ai was closely related to Serratia proteamaculans, Aj to Pseudomonas sp., El to Bacillus cereus, Pc to Pseudomonas psychrophila, and Pe to Pseudomonas veronii. They could equally tolerate Pb. Most of them had the capacity to produce siderophores and solubilize phosphate, except B. cereus. However, B. cereus showed high capacity of Pb uptake (4.54±0.38 mg/g) and removal (8.36±0.70%) with no significant difference (p>0.05) from the other strains, except P. psychrophila (1.36±0.23 mg/g of Pb uptake, and 2.60±0.44% Pb removal). The results suggest that biosorption capacity may not involve the habitat of a plant host. Plant-growth-promoting traits were not the only factor for biosorption by endophytic bacteria. S. proteamaculans, B. cereus, and P. veronii showed the same Pb biosorption. Strains closely related to P. veronii could be promoted as candidates for the removal of Pb in polluted environments.
Article Details
How to Cite
Yongpisanphop, J. ., & Babel, S. . (2020). Characterization of Pb-tolerant Plant-growth-promoting Endophytic Bacteria for Biosorption Potential, Isolated from Roots of Pb Excluders Grown in Different Habitats: DOI: 10.32526/ennrj.18.3.2020.25. Environment and Natural Resources Journal, 18(3), 268–274. Retrieved from https://ph02.tci-thaijo.org/index.php/ennrj/article/view/240998
Section
Original Research Articles
Published articles are under the copyright of the Environment and Natural Resources Journal effective when the article is accepted for publication thus granting Environment and Natural Resources Journal all rights for the work so that both parties may be protected from the consequences of unauthorized use. Partially or totally publication of an article elsewhere is possible only after the consent from the editors.
References
1. Abdel-Ghani NT, El-Chaghaby GA. Biosorption for metal ions removal from aqueous solutions: A review of recent studies. International Journal of Latest Research in Science and Technology 2014;3(1):24-42.
2. Abdia O, Kazemi M. A review study of biosorption of heavy metals and comparison between different biosorbents. Journal of Materials and Environmental Science 2015;6(5):1386-99.
3. Afzal I, Iqrar I, Shinwari ZK, Yasmin A. Plant growth-promoting potential of endophytic bacteria isolated from roots of wild Dodonaea viscosa L. Plant Growth Regulation 2017;81:399-408.
4. Ahemad M. Phosphate-solubilizing bacteria-assisted phyto-remediation of metalliferous soils: A review. Biotechnology 2015;5:111-21.
5. Ali H, Khan E, Sajad MA. Phytoremediation of heavy metals-concepts and applications. Chemosphere 2013;91:869-81.
6. Alzubaidy SK. The resistance of locally isolated Serratia marcescens to heavy metals chlorides and optimization of some environmental factors. Journal of Environmental and Occupational Science 2012;1(1):37-42.
7. Aslam MZ, Ramzan N, Naveed S, Feroze N. Ni(II) removal by biosorption using Ficus religiosa (peepal) leaves. Journal of the Chilean Chemical Society 2010;55(1):81-4.
8. Bano A, Hussain J, Akbar A, Mehmood K, Anwar M, Hasni MS, Ullah S, Sajid S, Ali I. Biosorption of heavy metals by obligate halophilic fungi. Chemosphere 2018;199:218-22.
9. Bhatnagar S, Kumari R. Bioremediation: A sustainable tool for environmental management: A review. Annual Research and Review in Biology 2013;3(4):974-93.
10. Coelho LM, Rezende HC, Coelho LM, de Sousa PAR, Melo DFO, Coelho NMM. Bioremediation of polluted waters using microorganisms [Internet]. 2015 [cited 2019 Sep 13]. Available from: https://www.intechopen.com/books/advances-in-bioremediation-of-wastewater-and-polluted-soil/ bioremediation-of-polluted-waters-using-microorganisms.
11. El Aafi N, Brhada F, Dary M, Maltouf AF, Pajuelo E. Rhizostabilization of metals in soils using Lupinus luteus inoculated with the metal resistant rhizobacterium Serratia sp. MSMC541. International Journal of Phytoremediation 2012;14(3):261-74.
12. Fan M, Liu Z, Nan L, Wang E, Chen W, Lin Y, Wei G. 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;217:51-9.
13. Felsenstein J. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 1985;39:783-91.
14. Francesconi K, Visoottiviseth P, Sridokchan W, Goessler W. Arsenic species in an arsenic hyperaccumulating fern, Pityrogramma calomelanos: A potential phytoremediator of arsenic-contaminated soils. Science of the Total Environment 2002;284:27-35.
15. Gillani RA, Shenaz N, Matloob S, Haq F, Ngah WSW, Nasim W, Munis MFH, Rehman A, Chaudhary HJ. Biosorption of Cr(III) and Pb(II) by endophytic Agrobacterium tumefaciens 12b3: Equilibrium and kinetic studies. Desalination and Water Treatment 2017;67:206-14.
16. Govarthanan M, Mythili R, Selvankumar T, Kamala-Kannan S, Rajasekar A, Chang Y-C. Bioremediation of heavy metals using an endophytic bacterium Paenibacillus sp. RM isolated from the roots of Tridax procumbens. 3 Biotech 2016;6:242.
17. Gupta A, Joia J, Sood A, Sood R, Sidhu C, Kaur G. Microbes as potential tool for remediation of heavy metals: A review. Journal of Microbial and Biochemical Technology 2016;8(4):364-72.
18. Jarosławiecka A, Piotrowska-Seget Z. Lead resistance in microorganisms. Microbiology 2014;160:12-25.
19. Jeong S, Moon HS, Nama K, Kim JY, Kim TS. Application of phosphate-solubilizing bacteria for enhancing bioavailability and phytoextraction of cadmium (Cd) from polluted soil. Chemosphere 2012;88:204-10.
20. Kimura M. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 1980;16:111-20.
21. Kumar S, Stecher G, Tamura K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 2016;33:1870-4.
22. Kumar P, Fulekar MH. Rhizosphere bioremediation of heavy metals (Copper and Lead) by Cenchrus ciliaris. Research Journal of Environmental Sciences 2018;12(4):166-76.
23. Li H-Y, Wei D-Q, Shen M, Zhou Z-P. Endophytes and their role in phytoremediation. Fungal Diversity 2012;54:11-8.
24. Liotti RG, da Silva Figueiredoa MI, da Silvac GF, de Mendonçad EAF, Soaresa MA. Diversity of cultivable bacterial endophytes in Paullinia cupana and their potential for plant growth promotion and phytopathogen control. Microbiological Research 2018;207:8-18.
25. Lodewyckx C, Vangronsveld J, Porteous F, Moore ERB, Taghavi S, Mezgeay M, der Lelie DV. Endophytic bacteria and their potential applications. Critical Reviews in Plant Sciences 2002;21:583-606.
26. Luo SL, Chen L, Chen JL, Xiao X, Xu TY, Wan Y, Rao C, Liu CB. Analysis and characterization of cultivable heavy metal-resistant bacterial endophytes isolated from Cd-hyperaccumulator Solanum nigrum L. and their potential use for phytoremediation. Chemosphere 2011;85(7):1130-8.
27. Ma Y, Rajkumar M, Zhang C, Freitas H. Beneficial role of bacterial endophytes in heavy metal phytoremediation. Journal of Environmental Management 2016;174:14-25.
28. Meeinkuirt W, Pokethitiyook P, Kruatrachue M, Tanhan P, Chaiyarat R. Phytostabilization of a Pb-contaminated mine tailing by various tree species in pot and field trial experiments. International Journal of Phytoremediation 2012;14:925-38.
29. Montes C, Altimira F, Canchignia H, Castro Á, Sánchez E, Miccono M, et al. A draft genome sequence of Pseudomonas veronii R4: A grapevine (Vitis vinifera L.) root-associated strain with high biocontrol potential. Standards in Genomic Sciences 2016;11:76.
30. Nalik MM, Dubey SK. Lead resistant bacteria: Lead resistance mechanisms, their applications in lead bioremediation and biomonitoring. Ecotoxicology and Environmental Safety 2013;98:1-7.
31. Ngamau CN, Matiru VN, Tani A, Muthuri CW. Isolation and identification of endophytic bacteria of bananas (Musa spp.) in Kenya and their potential as biofertilizers for sustainable banana production. African Journal of Microbiology Research 2012;6(34):6414-22.
32. Paul D, Sinha SN. Isolation and characterization of a phosphate solubilizing heavy metal tolerant bacterium from River Ganga, West Bengal, India. Songklanakarin Journal of Science and Technology 2015;37(6):651-7.
33. Rajkumar M, Ae N, Prasad MNV, Freitas H. Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends in Biotechnology 2010;28(3):142-9.
34. Saitou N, Nei M. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 1987;4:406-25.
35. Sgroy V, Cassán F, Masciarelli O, del Papa FM, Lagares A, Luna V.Isolation and characterization of endophytic plant growth-promoting (PGPB) or stress homeostasis-regulating (PSHB) bacteria associated to the halophyte Prosopis strombulifera. Applied Microbiology and Biotechnology 2009;85(2):371-81.
36. Shamim S. Biosorption of heavy metals [Internet]. 2018 [cited 2019 Sep 13]. Available from: https://www.intechopen.com/ books/biosorption/biosorption-of-heavy-metals.
37. Sharma P, Dubey RS. Pb toxicity in plants. Brazilian Journal of Plant Physiology 2005;17:35-52.
38. Shin MN, Shim J, You Y, Myung H, Bang KS, Cho M, et al. Characterization of lead resistant endophytic Bacillus sp. MN3-4 and its potential for promoting lead accumulation in metal hyperaccumulator Alnus firma. Journal of Hazardous Materials 2012;199-200:314-20.
39. Soongsombat P, Kruatrachue M, Chaiyarat R, Pokethitiyook P, Ngernsansaruay C. Lead tolerance and accumulation in Pteris vittata and Pityrogramma calomelanos, and their potential for phytoremediation of lead-contaminated soil. International Journal of Phytoremediation 2009;11(4):396-412.
40. Tseveendorj E, Enkhdul T, Lin S, Dorj D, Oyungerel SH, Soyol-Erdene TO. Biosorption of lead (II) from an aqueous solution using biosorbents prepared from water plants. Mongolian Journal of Chemistry 2017;18(44):52-61.
41. Yongpisanphop J, Babel S, Kruatrachue M, Pokethitiyook P. Phytoremediation potential of plants growing on the Pb-contaminated soil at the Song Tho Pb Mine, Thailand. Soil Sediment Contamination: An International Journal 2017; 26(4):426-37.
42. Yongpisanphop J, Babel S, Kurisu F, Kruatrachue M, Pokethitiyook P. Isolation and characterization of Pb-resistant plant growth promoting endophytic bacteria and their role in Pb accumulation by fast-growing trees. Environmental Technology 2019;e1615933.
43. Weyens N, van der Lelie D, Taghavi S, Vangronsveld J. Phytoremediation: plant-endophyte partnerships take the challenge. Current Opinion in Biotechnology 2009;20:248-54.
44. Wierzba S, Latala A. Biosorption lead(II) and nickel(II) from an aqueous solution by bacterial biomass. Polish Journal of Chemical Technology 2010;12(3):72-8.
45. Wu W, Jin Y, Bai F, Jin S. Pseudomonas aeruginosa. In: Tang Y-W, Sussman M, Liu D, Poxton I, Schwartzman J, editors. Molecular Medical Microbiology. 2nd ed. USA: Academic Press; 2015.
46. Zhu L-J, Guan D-X, Luo J, Rathinasabapathi B, Ma LQ. Characterization of arsenic-resistant endophytic bacteria from hyperaccumulators Pteris vittata and Pteris multifida. Chemosphere 2014;113:9-16.
2. Abdia O, Kazemi M. A review study of biosorption of heavy metals and comparison between different biosorbents. Journal of Materials and Environmental Science 2015;6(5):1386-99.
3. Afzal I, Iqrar I, Shinwari ZK, Yasmin A. Plant growth-promoting potential of endophytic bacteria isolated from roots of wild Dodonaea viscosa L. Plant Growth Regulation 2017;81:399-408.
4. Ahemad M. Phosphate-solubilizing bacteria-assisted phyto-remediation of metalliferous soils: A review. Biotechnology 2015;5:111-21.
5. Ali H, Khan E, Sajad MA. Phytoremediation of heavy metals-concepts and applications. Chemosphere 2013;91:869-81.
6. Alzubaidy SK. The resistance of locally isolated Serratia marcescens to heavy metals chlorides and optimization of some environmental factors. Journal of Environmental and Occupational Science 2012;1(1):37-42.
7. Aslam MZ, Ramzan N, Naveed S, Feroze N. Ni(II) removal by biosorption using Ficus religiosa (peepal) leaves. Journal of the Chilean Chemical Society 2010;55(1):81-4.
8. Bano A, Hussain J, Akbar A, Mehmood K, Anwar M, Hasni MS, Ullah S, Sajid S, Ali I. Biosorption of heavy metals by obligate halophilic fungi. Chemosphere 2018;199:218-22.
9. Bhatnagar S, Kumari R. Bioremediation: A sustainable tool for environmental management: A review. Annual Research and Review in Biology 2013;3(4):974-93.
10. Coelho LM, Rezende HC, Coelho LM, de Sousa PAR, Melo DFO, Coelho NMM. Bioremediation of polluted waters using microorganisms [Internet]. 2015 [cited 2019 Sep 13]. Available from: https://www.intechopen.com/books/advances-in-bioremediation-of-wastewater-and-polluted-soil/ bioremediation-of-polluted-waters-using-microorganisms.
11. El Aafi N, Brhada F, Dary M, Maltouf AF, Pajuelo E. Rhizostabilization of metals in soils using Lupinus luteus inoculated with the metal resistant rhizobacterium Serratia sp. MSMC541. International Journal of Phytoremediation 2012;14(3):261-74.
12. Fan M, Liu Z, Nan L, Wang E, Chen W, Lin Y, Wei G. 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;217:51-9.
13. Felsenstein J. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 1985;39:783-91.
14. Francesconi K, Visoottiviseth P, Sridokchan W, Goessler W. Arsenic species in an arsenic hyperaccumulating fern, Pityrogramma calomelanos: A potential phytoremediator of arsenic-contaminated soils. Science of the Total Environment 2002;284:27-35.
15. Gillani RA, Shenaz N, Matloob S, Haq F, Ngah WSW, Nasim W, Munis MFH, Rehman A, Chaudhary HJ. Biosorption of Cr(III) and Pb(II) by endophytic Agrobacterium tumefaciens 12b3: Equilibrium and kinetic studies. Desalination and Water Treatment 2017;67:206-14.
16. Govarthanan M, Mythili R, Selvankumar T, Kamala-Kannan S, Rajasekar A, Chang Y-C. Bioremediation of heavy metals using an endophytic bacterium Paenibacillus sp. RM isolated from the roots of Tridax procumbens. 3 Biotech 2016;6:242.
17. Gupta A, Joia J, Sood A, Sood R, Sidhu C, Kaur G. Microbes as potential tool for remediation of heavy metals: A review. Journal of Microbial and Biochemical Technology 2016;8(4):364-72.
18. Jarosławiecka A, Piotrowska-Seget Z. Lead resistance in microorganisms. Microbiology 2014;160:12-25.
19. Jeong S, Moon HS, Nama K, Kim JY, Kim TS. Application of phosphate-solubilizing bacteria for enhancing bioavailability and phytoextraction of cadmium (Cd) from polluted soil. Chemosphere 2012;88:204-10.
20. Kimura M. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 1980;16:111-20.
21. Kumar S, Stecher G, Tamura K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 2016;33:1870-4.
22. Kumar P, Fulekar MH. Rhizosphere bioremediation of heavy metals (Copper and Lead) by Cenchrus ciliaris. Research Journal of Environmental Sciences 2018;12(4):166-76.
23. Li H-Y, Wei D-Q, Shen M, Zhou Z-P. Endophytes and their role in phytoremediation. Fungal Diversity 2012;54:11-8.
24. Liotti RG, da Silva Figueiredoa MI, da Silvac GF, de Mendonçad EAF, Soaresa MA. Diversity of cultivable bacterial endophytes in Paullinia cupana and their potential for plant growth promotion and phytopathogen control. Microbiological Research 2018;207:8-18.
25. Lodewyckx C, Vangronsveld J, Porteous F, Moore ERB, Taghavi S, Mezgeay M, der Lelie DV. Endophytic bacteria and their potential applications. Critical Reviews in Plant Sciences 2002;21:583-606.
26. Luo SL, Chen L, Chen JL, Xiao X, Xu TY, Wan Y, Rao C, Liu CB. Analysis and characterization of cultivable heavy metal-resistant bacterial endophytes isolated from Cd-hyperaccumulator Solanum nigrum L. and their potential use for phytoremediation. Chemosphere 2011;85(7):1130-8.
27. Ma Y, Rajkumar M, Zhang C, Freitas H. Beneficial role of bacterial endophytes in heavy metal phytoremediation. Journal of Environmental Management 2016;174:14-25.
28. Meeinkuirt W, Pokethitiyook P, Kruatrachue M, Tanhan P, Chaiyarat R. Phytostabilization of a Pb-contaminated mine tailing by various tree species in pot and field trial experiments. International Journal of Phytoremediation 2012;14:925-38.
29. Montes C, Altimira F, Canchignia H, Castro Á, Sánchez E, Miccono M, et al. A draft genome sequence of Pseudomonas veronii R4: A grapevine (Vitis vinifera L.) root-associated strain with high biocontrol potential. Standards in Genomic Sciences 2016;11:76.
30. Nalik MM, Dubey SK. Lead resistant bacteria: Lead resistance mechanisms, their applications in lead bioremediation and biomonitoring. Ecotoxicology and Environmental Safety 2013;98:1-7.
31. Ngamau CN, Matiru VN, Tani A, Muthuri CW. Isolation and identification of endophytic bacteria of bananas (Musa spp.) in Kenya and their potential as biofertilizers for sustainable banana production. African Journal of Microbiology Research 2012;6(34):6414-22.
32. Paul D, Sinha SN. Isolation and characterization of a phosphate solubilizing heavy metal tolerant bacterium from River Ganga, West Bengal, India. Songklanakarin Journal of Science and Technology 2015;37(6):651-7.
33. Rajkumar M, Ae N, Prasad MNV, Freitas H. Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends in Biotechnology 2010;28(3):142-9.
34. Saitou N, Nei M. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 1987;4:406-25.
35. Sgroy V, Cassán F, Masciarelli O, del Papa FM, Lagares A, Luna V.Isolation and characterization of endophytic plant growth-promoting (PGPB) or stress homeostasis-regulating (PSHB) bacteria associated to the halophyte Prosopis strombulifera. Applied Microbiology and Biotechnology 2009;85(2):371-81.
36. Shamim S. Biosorption of heavy metals [Internet]. 2018 [cited 2019 Sep 13]. Available from: https://www.intechopen.com/ books/biosorption/biosorption-of-heavy-metals.
37. Sharma P, Dubey RS. Pb toxicity in plants. Brazilian Journal of Plant Physiology 2005;17:35-52.
38. Shin MN, Shim J, You Y, Myung H, Bang KS, Cho M, et al. Characterization of lead resistant endophytic Bacillus sp. MN3-4 and its potential for promoting lead accumulation in metal hyperaccumulator Alnus firma. Journal of Hazardous Materials 2012;199-200:314-20.
39. Soongsombat P, Kruatrachue M, Chaiyarat R, Pokethitiyook P, Ngernsansaruay C. Lead tolerance and accumulation in Pteris vittata and Pityrogramma calomelanos, and their potential for phytoremediation of lead-contaminated soil. International Journal of Phytoremediation 2009;11(4):396-412.
40. Tseveendorj E, Enkhdul T, Lin S, Dorj D, Oyungerel SH, Soyol-Erdene TO. Biosorption of lead (II) from an aqueous solution using biosorbents prepared from water plants. Mongolian Journal of Chemistry 2017;18(44):52-61.
41. Yongpisanphop J, Babel S, Kruatrachue M, Pokethitiyook P. Phytoremediation potential of plants growing on the Pb-contaminated soil at the Song Tho Pb Mine, Thailand. Soil Sediment Contamination: An International Journal 2017; 26(4):426-37.
42. Yongpisanphop J, Babel S, Kurisu F, Kruatrachue M, Pokethitiyook P. Isolation and characterization of Pb-resistant plant growth promoting endophytic bacteria and their role in Pb accumulation by fast-growing trees. Environmental Technology 2019;e1615933.
43. Weyens N, van der Lelie D, Taghavi S, Vangronsveld J. Phytoremediation: plant-endophyte partnerships take the challenge. Current Opinion in Biotechnology 2009;20:248-54.
44. Wierzba S, Latala A. Biosorption lead(II) and nickel(II) from an aqueous solution by bacterial biomass. Polish Journal of Chemical Technology 2010;12(3):72-8.
45. Wu W, Jin Y, Bai F, Jin S. Pseudomonas aeruginosa. In: Tang Y-W, Sussman M, Liu D, Poxton I, Schwartzman J, editors. Molecular Medical Microbiology. 2nd ed. USA: Academic Press; 2015.
46. Zhu L-J, Guan D-X, Luo J, Rathinasabapathi B, Ma LQ. Characterization of arsenic-resistant endophytic bacteria from hyperaccumulators Pteris vittata and Pteris multifida. Chemosphere 2014;113:9-16.