The potency of endophytic bacteria isolated from Ficus septica as phytoremediation promoting agent of Cr (VI) contaminated soil
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Abstract. Rohmah NS, Suharjono, Jatmiko YD, Siswanto D, Mustafa I. 2020. The potency of endophytic bacteria isolated from Ficus septica as phytoremediation promoting agent of Cr (VI) contaminated soil. Biodiversitas 21: 1920-1927. Endophytic bacteria tolerant of chromium have the potential to reduce Cr (VI) to Cr (III) and produce compounds that can improve plant survival in Cr (VI) contaminated soils. This study was performed to isolate and identify Cr (VI)-tolerant bacteria from the endosphere of Ficus septica Burm.F growing on the tannery waste contaminated soil, Screening of bacteria was carried out based on the level of Cr (VI) tolerance. High tolerant isolates were tested for their potential of Indole Acetic Acid (IAA) and exopolysaccharide (EPS) production, phosphate solubilizing, and the presence of chromate reductase (ChR) genes. The most potential bacterial isolate was identified based on 16S rDNA sequences. The results showed that three isolates (E3, E4, and E8) were tolerant of Cr (VI) up to 900 mg/L. E8 isolates produced the highest IAA production (20.05 ?g/mL), phosphate solubilization (127.78 ?g/mL), and EPS production (9,70 ?g/mL), and all isolates had the ChR gene. E8 isolate was found to be 100% identical to Enterobacter cloacae ATCC 13047.
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References
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Cervantes C. Campos-Garcia J. Devars S. Gutierrez-Corona F. Loza-Tavera H. Torres- Guzman JC. Moreno-Sánchez R. 2001. Interactions of chromium with microorganisms and plants. FEMS Microbiology Reviews 25 335e347.
Cervantes CH, Ohtake L. Chu TK, Misra S, Silver. 1990. Cloning nucleotide sequence and expression of the chromate resistance determinants of Pseudomonas aeruginosa plasmid pUM505. J. Bacteriol 172:287–291.
Cheung KH, Gu JD. 2007. Mechanism of hexavalent chromium detoxi?cation by microorganisms and bioremediation application potential: a review. International Biodeterioration & Biodegradation 59: 8-15.
Chitraprabha KS, Sathyavathi. 2018. Phytoextraction of chromium from electroplating ef?uent by Tagetes erecta (L.). Sustainable Environment Research. 28:128-134.
Davies KL, Davies MS, Francis D. 2001. Zinc-induced vacuolation in root meristematic cells of Festuca rubra L. Plant Cell and Environment 14: 399–406.
Dimitroula H, Evdokia S, Eleni M, Nikolaos PN. Karatzas, Nicolas K. 2014. Mitigation measures for chromium-vi contaminated groundwater–the role of endophytic bacteria in rhizo?ltration. Journal of Hazardous Materials. http://dx.doi.org/10.1016/j.jhazmat.2014.08.005
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Glickmann E and Dessaux Y. 1995. A critical examination of the specificity of the salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Applied Environmental Microbiology 61:793-796.
Harish R, Jastin S, Mishra R, Chandrasekaran N, Mukherjee A. 2012. Bio-reduction of Cr(VI) by exopolysaccharides (EPS) from indigenous bacterial species of Sukinda chromite mine, India. Biodegradation (2012) 23:487–496.
Harley JP, Prescott LM. 2002. Laboratory Exercises in Microbiology Fifth Edition.T he McGraw?Hil.
Hynninen A, Virta M. 2009 Whole-cell bioreporters for the detection of bioavailable metals. Adv Biochem Eng Biotechnol. doi:10.1007/10_2009_9
Javaid M and Sikander S. 2012. Plant growth promotion traits and Cr (VI) reduction potentials of Cr (VI) resistant Streptomyces strains. Journal of Basic Microbiology 52: 1-10.
Khan MU, Angela S, Muhammad H, Kaneez F, Asma I, Muhammad A, Ghulam S, Qaiser MK, Muhammad A. 2015. Cr-resistant rhizo- and endophytic bacteria associated with Prosopis juli?ora and their potential as phytoremediation enhancing agents in metal-degraded soils. Frontiers in Plant Science 5:755.
Krishna KR, Philip L. 2005. Bioremediation of Cr(VI) in contaminated soils. Journal of Hazardous Materials 121: 109-117.
Kumar VR, Kothari SK, Tyagi. 2014. Biological hydrogen production by facultative anaerobic bacteria Enterobacter aerogens (MTCC 8100). Recent Advances in Bioenergy Research 3:25.
Laghlimi M, Baghdad B, El Hadi H, Bouabdli A. 2015. Phytoremediation mechanisms of heavy metal contaminated soils: A review Open journal of Ecology 5: 375-388.
Liphadzi MS. Kirkham MB, Paulsen GM.. 2006. Auxin-Enhanced Root Growth for Phytoremediation of Sewage-Sludge Amended Soil. Environmental Technology 27:695-704.
Lugtenberg B, Kamilova F. 2009. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol 63: 541–556.
Luo J, Cai L, Qi S, Wu J, Gu XS. 2018. Heavy metal remediation with Ficus microcarpa through transplantation and its environmental risks through field scale experiment. Chemosphere 193: 244–250.
Malik A. 2004. Metal bioremediation by growing cells. Environment International 30:261-278.
Morais PV, Branco R, Francisco R. 2011. Chromium resistance strategies and toxicity: what makes Ochrobactrum tritici 5bvl1 a strain highly resistant. Biometals 24: 401–410.
Oves M, Saghir KM, Zaidi A. 2013. Chromium reducing and plant growth promoting novel strain Pseudomonas aeruginosa OSG41 enhance chickpea growth in chromium amended soils. Eur. J. Soil Biol. 56: 72–8.
Patra RC, Malik S, Beer M, Megharaj M, Naidu R. 2010 Molecular characterization of chromium (VI) reducing potential in Gram positive bacteria isolated from contaminated sites. Soil Biol. Biochem 42: 1857–1863.
Premono ME, Moawad AM, Vlek PLG. 1996. Effect of phosphate-solubilizing Pseudomonas putida on the growth of maize and its survival in the rhizosphere. Indonesian Journal of Crop Science 11: 13–2.
Rida B, Kim Y, Kamran S, Nazia J, Shahida H. 2015. Production of EPS under Cr(VI) challenge in two indigenous bacteria isolated from a tannery ef?uent J. Basic Microbiol 54: 1–11.
Ramírez V, Antonino B, Primavera L,Rocío B, Miguel ÁV,Ricardo C,José LC,Jesús M, Luis EF, Javier M, José AM. 2019. Chromium Hyper-Tolerant Bacillus sp. MH778713 Assists Phytoremediation of Heavy Metals by Mesquite Trees (Prosopis laevigata). Frontiers in Microbiology. doi: 10.3389/fmicb.2019.01833.
Rosariastuti R, Prijambada ID, Ngadiman PGS, Putri AR. 2013. Isolation and identification of plant growth promoting and chromium uptake enhancing bacteria from soil contaminated by leather tanning industrial waste. Journal of Basic and Applied Sciences 9: 243-251.
Sanjay MS, Dorairaj S, Gnanaprakasam AR, Kathirvelu B. 2018. Isolation and identi?cation of chromium reducing bacteria from tannery ef?uent. Journal of King Saud University. https://doi.org/10.1016/j.jksus.2018.05.001
Schiavon M, Pilon-Smits MWR, Hell, Malagoli M. 2008. Interactions between chromium and sulfur metabolism in Brassica juncea. Jurnal of Environmental Quality 37: 1536-1545.
Sharma SBRZ, Sayyed MH, Trivedi TA, Gobi. 2013. Phosphate solubilising microbes:sustainable approach for managing phosphorus deficiency in agricultural soils. Springerplus 2:587.
Singh J, Carlisle DL, Pritchard DE, Patierno SR. 1998. Chromium-induced genotoxicity and apoptosis: relationship to chromium carcinogenesis (review). Oncology Report 5: 1307-1318.
Singh P, Kumar V, Agrawal S. 2014. Evaluation of phytase producing bacteria for their plant growth promoting activities.http://www.hindawi.com/journals/ijmicro/2014/426483/.
Srivastava VC, Mall ID, Mishra IM. 2006. Modelling Individual and Competitive Adsorption of Cadmium (II) and Zinc(II) Metal Ions from Aqueous Solution Onto Bagasse Fly Ash. Sep. Sci. Technol 41: 2685–2710.
Tallgren AH, Airaksinen U, von Weissenberg R, Ojamo H J, Kuusisto, Leisola M. 1999. Exopolysaccharide-producing bacteria from sugar beets. Journal Applied Environmental Microbiology 65: 862-864.
Thakuria D, Talukdar NC, Goswami C, Hazarika S, Boro RC, Khan MR. 2004. Charcterization and screening of bacteria from rhizosphere of rice grown in acidic soils of Assam. Current Science 7: 978-985.
Tirry NN, Tahri Joutey H, Sayel A, Kouchou W, Baha?d M, Asri N, El G. 2018. Screening of plant growth promoting traits in heavy metals resistant bacteria: Prospects in phytoremediation. Journal of Genetic Engineering and Biotechnolog. www.elsevier.com/locate/jgeb.
Wani PA, Adeosun BO. 2017. Cr (VI) removal by indigenous Klebsiella species PB6 isolated from contaminated soil under the influence of various factors. Current Research in Bacteriology 8: 62-69.
Wang PC, Mori T, Toda K, Ohtake H. 1990. Membrane associated chromate reductase activity from Enterobacter cloacae. J. Bacteriol 172: 1670–1672.
Yeo CK, Tan HTWW. 2011. Ficus stranglers and melastoma malabathricum: potential tropical woody plants for phytoremediation of metals in wetlands. Nature in Singapore4: 213–226.
Bric JM, Bostock RM, Silverstone SE. 1991. Rapid in situ assay for Indole Acetic Acid production by bacteria immobilized on a nitrocellulose membrane. Applied and Environmental Microbiology 57: 535-538.
Camargo FAO, Bento FM, Okeke BC. Frankenberger WT. 2003. Chromate reduction by chromium resistant bacteria isolated from soils contaminated with dichromate. Journal of Environmental Quality 32, 1228e1233.
Cervantes C. Campos-Garcia J. Devars S. Gutierrez-Corona F. Loza-Tavera H. Torres- Guzman JC. Moreno-Sánchez R. 2001. Interactions of chromium with microorganisms and plants. FEMS Microbiology Reviews 25 335e347.
Cervantes CH, Ohtake L. Chu TK, Misra S, Silver. 1990. Cloning nucleotide sequence and expression of the chromate resistance determinants of Pseudomonas aeruginosa plasmid pUM505. J. Bacteriol 172:287–291.
Cheung KH, Gu JD. 2007. Mechanism of hexavalent chromium detoxi?cation by microorganisms and bioremediation application potential: a review. International Biodeterioration & Biodegradation 59: 8-15.
Chitraprabha KS, Sathyavathi. 2018. Phytoextraction of chromium from electroplating ef?uent by Tagetes erecta (L.). Sustainable Environment Research. 28:128-134.
Davies KL, Davies MS, Francis D. 2001. Zinc-induced vacuolation in root meristematic cells of Festuca rubra L. Plant Cell and Environment 14: 399–406.
Dimitroula H, Evdokia S, Eleni M, Nikolaos PN. Karatzas, Nicolas K. 2014. Mitigation measures for chromium-vi contaminated groundwater–the role of endophytic bacteria in rhizo?ltration. Journal of Hazardous Materials. http://dx.doi.org/10.1016/j.jhazmat.2014.08.005
Dogan NM, Kantar VS, Gulcan CJ, Dodge BC, Yilmaz, Mazmanci MA. 2011. Chromium(VI) Bioremoval by Pseudomonas Bacteria: Role of Microbial Exudates for Natural Attenuation and Biotreatment of Cr(VI) Contamination. Environmental Science and Technology 45:2278–2285.
Glickmann E and Dessaux Y. 1995. A critical examination of the specificity of the salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Applied Environmental Microbiology 61:793-796.
Harish R, Jastin S, Mishra R, Chandrasekaran N, Mukherjee A. 2012. Bio-reduction of Cr(VI) by exopolysaccharides (EPS) from indigenous bacterial species of Sukinda chromite mine, India. Biodegradation (2012) 23:487–496.
Harley JP, Prescott LM. 2002. Laboratory Exercises in Microbiology Fifth Edition.T he McGraw?Hil.
Hynninen A, Virta M. 2009 Whole-cell bioreporters for the detection of bioavailable metals. Adv Biochem Eng Biotechnol. doi:10.1007/10_2009_9
Javaid M and Sikander S. 2012. Plant growth promotion traits and Cr (VI) reduction potentials of Cr (VI) resistant Streptomyces strains. Journal of Basic Microbiology 52: 1-10.
Khan MU, Angela S, Muhammad H, Kaneez F, Asma I, Muhammad A, Ghulam S, Qaiser MK, Muhammad A. 2015. Cr-resistant rhizo- and endophytic bacteria associated with Prosopis juli?ora and their potential as phytoremediation enhancing agents in metal-degraded soils. Frontiers in Plant Science 5:755.
Krishna KR, Philip L. 2005. Bioremediation of Cr(VI) in contaminated soils. Journal of Hazardous Materials 121: 109-117.
Kumar VR, Kothari SK, Tyagi. 2014. Biological hydrogen production by facultative anaerobic bacteria Enterobacter aerogens (MTCC 8100). Recent Advances in Bioenergy Research 3:25.
Laghlimi M, Baghdad B, El Hadi H, Bouabdli A. 2015. Phytoremediation mechanisms of heavy metal contaminated soils: A review Open journal of Ecology 5: 375-388.
Liphadzi MS. Kirkham MB, Paulsen GM.. 2006. Auxin-Enhanced Root Growth for Phytoremediation of Sewage-Sludge Amended Soil. Environmental Technology 27:695-704.
Lugtenberg B, Kamilova F. 2009. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol 63: 541–556.
Luo J, Cai L, Qi S, Wu J, Gu XS. 2018. Heavy metal remediation with Ficus microcarpa through transplantation and its environmental risks through field scale experiment. Chemosphere 193: 244–250.
Malik A. 2004. Metal bioremediation by growing cells. Environment International 30:261-278.
Morais PV, Branco R, Francisco R. 2011. Chromium resistance strategies and toxicity: what makes Ochrobactrum tritici 5bvl1 a strain highly resistant. Biometals 24: 401–410.
Oves M, Saghir KM, Zaidi A. 2013. Chromium reducing and plant growth promoting novel strain Pseudomonas aeruginosa OSG41 enhance chickpea growth in chromium amended soils. Eur. J. Soil Biol. 56: 72–8.
Patra RC, Malik S, Beer M, Megharaj M, Naidu R. 2010 Molecular characterization of chromium (VI) reducing potential in Gram positive bacteria isolated from contaminated sites. Soil Biol. Biochem 42: 1857–1863.
Premono ME, Moawad AM, Vlek PLG. 1996. Effect of phosphate-solubilizing Pseudomonas putida on the growth of maize and its survival in the rhizosphere. Indonesian Journal of Crop Science 11: 13–2.
Rida B, Kim Y, Kamran S, Nazia J, Shahida H. 2015. Production of EPS under Cr(VI) challenge in two indigenous bacteria isolated from a tannery ef?uent J. Basic Microbiol 54: 1–11.
Ramírez V, Antonino B, Primavera L,Rocío B, Miguel ÁV,Ricardo C,José LC,Jesús M, Luis EF, Javier M, José AM. 2019. Chromium Hyper-Tolerant Bacillus sp. MH778713 Assists Phytoremediation of Heavy Metals by Mesquite Trees (Prosopis laevigata). Frontiers in Microbiology. doi: 10.3389/fmicb.2019.01833.
Rosariastuti R, Prijambada ID, Ngadiman PGS, Putri AR. 2013. Isolation and identification of plant growth promoting and chromium uptake enhancing bacteria from soil contaminated by leather tanning industrial waste. Journal of Basic and Applied Sciences 9: 243-251.
Sanjay MS, Dorairaj S, Gnanaprakasam AR, Kathirvelu B. 2018. Isolation and identi?cation of chromium reducing bacteria from tannery ef?uent. Journal of King Saud University. https://doi.org/10.1016/j.jksus.2018.05.001
Schiavon M, Pilon-Smits MWR, Hell, Malagoli M. 2008. Interactions between chromium and sulfur metabolism in Brassica juncea. Jurnal of Environmental Quality 37: 1536-1545.
Sharma SBRZ, Sayyed MH, Trivedi TA, Gobi. 2013. Phosphate solubilising microbes:sustainable approach for managing phosphorus deficiency in agricultural soils. Springerplus 2:587.
Singh J, Carlisle DL, Pritchard DE, Patierno SR. 1998. Chromium-induced genotoxicity and apoptosis: relationship to chromium carcinogenesis (review). Oncology Report 5: 1307-1318.
Singh P, Kumar V, Agrawal S. 2014. Evaluation of phytase producing bacteria for their plant growth promoting activities.http://www.hindawi.com/journals/ijmicro/2014/426483/.
Srivastava VC, Mall ID, Mishra IM. 2006. Modelling Individual and Competitive Adsorption of Cadmium (II) and Zinc(II) Metal Ions from Aqueous Solution Onto Bagasse Fly Ash. Sep. Sci. Technol 41: 2685–2710.
Tallgren AH, Airaksinen U, von Weissenberg R, Ojamo H J, Kuusisto, Leisola M. 1999. Exopolysaccharide-producing bacteria from sugar beets. Journal Applied Environmental Microbiology 65: 862-864.
Thakuria D, Talukdar NC, Goswami C, Hazarika S, Boro RC, Khan MR. 2004. Charcterization and screening of bacteria from rhizosphere of rice grown in acidic soils of Assam. Current Science 7: 978-985.
Tirry NN, Tahri Joutey H, Sayel A, Kouchou W, Baha?d M, Asri N, El G. 2018. Screening of plant growth promoting traits in heavy metals resistant bacteria: Prospects in phytoremediation. Journal of Genetic Engineering and Biotechnolog. www.elsevier.com/locate/jgeb.
Wani PA, Adeosun BO. 2017. Cr (VI) removal by indigenous Klebsiella species PB6 isolated from contaminated soil under the influence of various factors. Current Research in Bacteriology 8: 62-69.
Wang PC, Mori T, Toda K, Ohtake H. 1990. Membrane associated chromate reductase activity from Enterobacter cloacae. J. Bacteriol 172: 1670–1672.
Yeo CK, Tan HTWW. 2011. Ficus stranglers and melastoma malabathricum: potential tropical woody plants for phytoremediation of metals in wetlands. Nature in Singapore4: 213–226.
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