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References

  1. Rajkumar M, Ae N, Prasad M, Freitas H. 2010. Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol. 28: 142-149.
    Pubmed CrossRef
  2. Vraspir JM, Butler A. 2009. Chemistry of marine ligands and siderophores. Annu. Rev. Mater. Sci. 1: 43-63.
    Pubmed PMC CrossRef
  3. Neilands JB. 1995. Siderophores: structure and function of microbial iron transport compounds. J. Biol. Chem. 270: 26723-26726.
    Pubmed CrossRef
  4. Saha M, Sarkar N, Sarkar B, Sharma BK, Bhattacharjee S, Tribedi B. 2016. Microbial siderophores and their potential applications: a review. Environ. Sci. Pollut. Res. 23: 3984-3999.
    Pubmed CrossRef
  5. Ma Y, Oliveira RS, Wu L, Luo Y, Rajkumar, M. 2015. Inoculation with metal-mobilizing plant growth-promoting rhizobacterium Bacillus sp. SC2b and its role in rhizoremediation. J. Toxicol. Environ. Health 78: 931-944.
    Pubmed CrossRef
  6. Rajkumar M, Freitas F. 2008. Effects of inoculation of plantgrowth promoting bacteria on Ni uptake by Indian mustard. Bioresour. Technol. 99: 3491-3498.
    Pubmed CrossRef
  7. Babu AG, Kim JD, Oh BT. 2013. Enhancement of heavy metal phytoremediation by Alnus firma with endophytic Bacillus thuringiensis GDB-1. J. Hazard. Mater. 250-251: 477-483.
    Pubmed CrossRef
  8. Bendale MS, Chaudhari BL, Chincholkar SB. 2009. Influence of environmental factors on siderophore production by Streptomyces fulvissimus ATCC 27431. Curr. Trends Biotechnol. Pharm. 3: 362-371.
  9. Santos S, Neto IFF, Machado MD, Soares HMVM, Soares EV. 2014. Siderophore production by Bacillus megaterium: effect of growth phase and cultural conditions. Appl. Biochem. Biotechnol. 172: 549-560.
    Pubmed CrossRef
  10. Shaikh SS, Wani SJ, Sayyed RZ. 2016. Statistical-based optimization and scale-up of siderophore production process on laboratory bioreactor. 3 Biotech. 6: 69.
    Pubmed PMC CrossRef
  11. Sayyed RZ, Badgujar MD, Sonawane HM, Mhaske MM, Chincholkar SB. 2005. Production of microbial iron chelators (siderophores) by fluorescent pseudomonads. Indian J. Biotechnol. 4: 484-490.
  12. Dimkpa CO, Svatos A, Dabrowska P, Schmidt A, Boland W, Kothe E. 2008. Involvement of siderophores in the reduction of metal-induced inhibition of auxin synthesis in Streptomyces spp. Chemosphere 74: 19-25.
    Pubmed CrossRef
  13. Gaonkar T, Bhosle S. 2013. Effect of metals on a siderophore producing bacterial isolate and its implications on microbial assisted bioremediation of metal contaminated soils. Chemosphere 93: 1835-1843.
    Pubmed CrossRef
  14. Braud A, Hoegy F, Jezequel K, Lebeau T, Schalk IJ. 2009. New insights into the metal specificity of the Pseudomonas aeruginosa pyoverdine-iron uptake pathway. Environ. Microbiol. 11: 1079-1091.
    Pubmed CrossRef
  15. Ren G, Jin Y, Zhang C, Gu H, Qu J. 2015. Characteristics of Bacillus sp. PZ-1 and its biosorption to Pb(II). Ecotoxicol. Environ. Saf. 117: 141-148.
    Pubmed CrossRef
  16. Payne SM. 1994. Detection, isolation and characterization of siderophores. Methods Enzymol. 235: 329.
    CrossRef
  17. Csaky TZ. 1948. On the estimation of bound hydroxylamine in biological materials. Acta Chem. Scand. 2: 450-454.
    CrossRef
  18. Arnow LE. 1937. Colorimetric determination of the components of 3,4-dihydroxy phenylalanine tyrosine mixtures. Circ. J. 118: 531-537.
  19. Shenker M, Oliver I, Helmann M, Hadar Y, Chen Y. 1992. Utilization by tomatoes of iron mediated by a siderophore produced by Rhizopus arrhizus. J. Plant Nutr. 15: 2173-2182.
    CrossRef
  20. Kuchenbuch R, Jung J. 1988. Changes in root-shoot ratio and ion uptake of maize (Zea mays L.) from soil as influenced by a plant growth regulator. Plant Soil 109: 151-157.
    CrossRef
  21. Mendez MO, Maier RM. 2008. Phytostabilization of mine tailings in arid and semiarid environments - an emerging remediation technology. Environ. Health Perspect. 116: 278-283.
    Pubmed PMC CrossRef
  22. Manwar AV, Khandelwal SR, Chaudhari BL, Meyer JM, Chincholkar SB. 2004. Siderophore production by a marine Pseudomonas aeruginosa and its antagonistic action against phytopathogenic fungi. Appl. Biochem. Biotechnol. 118: 243.
    CrossRef
  23. Chakraborty U, Chankrabopty B, Basnet M. 2006. Plant growth promotion and induction of resistance in Camellia sinensis by Bacillus megaterium. J. Basic Microbiol. 46: 186-195.
    Pubmed CrossRef
  24. Lebeau T, Braud A, Jézéquel K. 2008. Performance of bioaugmentation-assisted phytoextraction applied to metal contaminated soils: a review. Environ. Pollut. 153: 497-522.
    Pubmed CrossRef
  25. Fuloria A, Saraswat S, Rai JPN. 2009. Effect of Pseudomonas fluorescens on metal phytoextraction from contaminated soil by Brassica juncea. Chem. Ecol. 25: 385-396.
    CrossRef
  26. Sullivan TS, Ramkissoon S, Garrison VH, Ramsubhag A, Thies JE. 2012. Siderophore production of African dust microorganisms over Trinidad and Tobago. Aerobiologia 28:391-401.
    CrossRef
  27. Xiao R, Kisaalita WS. 1998. Fluorescent pseudomonad pyoverdines bind and oxidize ferrous ion. Appl. Environ. Microbiol. 64: 1472-1476.
  28. Mahmoud ALE, Abd-Alla MH. 2011. Siderophore production by some microorganisms and their effect on BradyrhizobiumMung bean symbiosis. Int. J. Agric. Biol. 3: 157-162.
  29. Yu X, Ai C, Xin L, Zhou G. 2011. The siderophore-producing bacterium, Bacillus subtilis CAS15, has a biocontrol effect on Fusarium wilt and promotes the growth of pepper. Eur. J. Soil Biol. 47: 138-145.
    CrossRef
  30. Rachid D, Ahmed B. 2005. Effect of iron and growth inhibitors on siderophores production by Pseudomonas fluorescens. Afr. J. Biotechnol. 4: 697-702.
    CrossRef
  31. Naik MM, Dubey SK. 2011. Lead-enhanced siderophore production and alteration in cell morphology in a Pbresistant Pseudomonas aeruginosa strain 4EA. Curr. Microbiol. 62: 409-414.
    Pubmed CrossRef
  32. Clarke SE, Stuart J, Sanders-Loehr J. 1987. Induction of siderophore activity in Anabaena spp. and its moderation of copper toxicity. Appl. Environ. Microbiol. 53: 917-922.
  33. Waldron KJ, Tottey S, Yanagisawa S, Dennison C, Robinson NJ. 2007. A periplasmic iron-binding protein contributes toward inward copper supply. J. Biol. Chem. 282: 3837-3846.
    Pubmed CrossRef
  34. Sinha S, Mukherjee SK. 2008. Cadmium-induced siderophore production by a high Cd-resistant bacterial strain relieved Cd toxicity in plants through root colonization. Curr. Microbiol.56: 55-60.
    Pubmed CrossRef
  35. Rossbach S, Wilson TL, Kukuk ML, Carty HA. 2000. Elevated zinc induces siderophore biosynthesis genes and a zntA-like gene in Pseudomonas fluorescens. FEMS Microbiol.Lett. 191: 61-70.
    CrossRef
  36. Duffy BK, Defago G. 1999. Environmental factors modulating antibiotic and siderophore biosynthesis by Pseudomonas fluorescens biocontrol strains. Appl. Environ. Microbiol. 65:2429-2438.
  37. Abd-Alla MH. 1998. Growth and siderophore production in vitro of Bradyrhizobium (Lupin) strains under iron limitation. Folia Microbiol. 44: 196-200.
    CrossRef
  38. Saha R, Saha N, Donofrio RS, Bestervelt LL. 2013. Microbial siderophores: a mini review. J. Basic. Microbiol. 53: 303-317.
    Pubmed CrossRef
  39. Federspiel A, Schuler R, Haselwandter K. 1991. Effect of pH, L-ornithine and L-proline on the hydroxamate siderophore production by Hymenoscyphus ericae, a typical ericoid mycorrhizal fungus. Plant Soil 130: 259-261.
    CrossRef
  40. Ugwu DI, Ezema BE, Eze FU, Ayogu JI, Ezema CG, Ugwuja DI. 2014. Synthesis and biological applications of hydroxamates. Cheminform 4: 26-51.
    Pubmed PMC CrossRef
  41. Wu CH, Wood TK, Mulchandani A, Chen W. 2006. Engineering plant-microbe symbiosis for rhizoremediation of heavy metals. Appl. Environ. Microbiol. 72: 1129-1134.
    Pubmed PMC CrossRef
  42. Gadd GM. 2004. Microbial influence on metal mobility and application for bioremediation. Geoderma 122: 109-119.
    CrossRef
  43. Nadeem SM, Ahmad M, Zahir ZA, Javaid A, Ashraf M. 2014. The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol. Adv. 32: 429-448.
    Pubmed CrossRef
  44. Ernst WH. 2000. Evolution of metal hyperaccumulation and phytoremediation hype. New Phytol. 146: 357-358.
    CrossRef
  45. Davies JFT, Puryear JD, Newton RJ, Egilla JN, Saraiva Grossi JA. 2001. Mycorrhizal fungi enhance accumulation and tolerance of chromium in sunflower (Helianthus annuus). J. Plant Physiol. 158: 777-786.
    CrossRef
  46. Compant S, Clement C, Sessitsch A. 2010. Plant growthpromoting bacteria in the rhizo- and endosphere of plants:their role, colonization, mechanisms involved and prospects for utilization. Soil Biol. Biochem. 42: 669-678.
    CrossRef
  47. Ahemad M, Kibret M. 2014. Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J. King Saud Univ. Sci. 26: 1-20.
    CrossRef

Article

Research article

J. Microbiol. Biotechnol. 2017; 27(8): 1500-1512

Published online August 28, 2017 https://doi.org/10.4014/jmb.1705.05021

Copyright © The Korean Society for Microbiology and Biotechnology.

Optimization of Siderophore Production by Bacillus sp. PZ-1 and Its Potential Enhancement of Phytoextration of Pb from Soi

Sumei Yu , Chunying Teng , Xin Bai , Jinsong Liang , Tao Song , Liying Dong , Yu Jin and Juanjuan Qu *

College of Resources and Environmental Science, Northeast Agricultural University, P.R. China

Received: May 8, 2018; Accepted: June 16, 2017

Abstract

In this study, the siderophore-producing characteristics and conditions of Bacillus sp. PZ-1
were investigated and the enhancement of siderophores on Pb uptake and translocation in
Brassica juncea were determined. Results of single factor experiment showed that glucose, pH,
and Pb(NO3)2 could stimulate PZ-1 growth and siderophore production. The maximum
siderophore production of 90.52% siderophore units was obtained by response surface
methodology optimization at the glucose concentration of 21.84 g/l, pH 6.18, and Pb(NO3)2
concentration of 245.04 μmol/l. The type of siderophore was hydroxamate and its concentration
in the fermentation broth amounted to 32.24 μg/ml. Results of pot experiments indicated that
the siderophores enhanced B. juncea to assimilate more Pb from soil with the uptake ratio from
1.04 to 2.74, and to translocate more Pb from underground to overground with the TF values
from 1.21 to 1.48. The results revealed that Bacillus sp. PZ-1 could produce abundant
siderophores and might be potentially used to augment the phytoextraction of Pb from soil.

Keywords: Bacillus sp. PZ-1, siderophore, response surface methodology, Pb, phytoextraction

References

  1. Rajkumar M, Ae N, Prasad M, Freitas H. 2010. Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol. 28: 142-149.
    Pubmed CrossRef
  2. Vraspir JM, Butler A. 2009. Chemistry of marine ligands and siderophores. Annu. Rev. Mater. Sci. 1: 43-63.
    Pubmed KoreaMed CrossRef
  3. Neilands JB. 1995. Siderophores: structure and function of microbial iron transport compounds. J. Biol. Chem. 270: 26723-26726.
    Pubmed CrossRef
  4. Saha M, Sarkar N, Sarkar B, Sharma BK, Bhattacharjee S, Tribedi B. 2016. Microbial siderophores and their potential applications: a review. Environ. Sci. Pollut. Res. 23: 3984-3999.
    Pubmed CrossRef
  5. Ma Y, Oliveira RS, Wu L, Luo Y, Rajkumar, M. 2015. Inoculation with metal-mobilizing plant growth-promoting rhizobacterium Bacillus sp. SC2b and its role in rhizoremediation. J. Toxicol. Environ. Health 78: 931-944.
    Pubmed CrossRef
  6. Rajkumar M, Freitas F. 2008. Effects of inoculation of plantgrowth promoting bacteria on Ni uptake by Indian mustard. Bioresour. Technol. 99: 3491-3498.
    Pubmed CrossRef
  7. Babu AG, Kim JD, Oh BT. 2013. Enhancement of heavy metal phytoremediation by Alnus firma with endophytic Bacillus thuringiensis GDB-1. J. Hazard. Mater. 250-251: 477-483.
    Pubmed CrossRef
  8. Bendale MS, Chaudhari BL, Chincholkar SB. 2009. Influence of environmental factors on siderophore production by Streptomyces fulvissimus ATCC 27431. Curr. Trends Biotechnol. Pharm. 3: 362-371.
  9. Santos S, Neto IFF, Machado MD, Soares HMVM, Soares EV. 2014. Siderophore production by Bacillus megaterium: effect of growth phase and cultural conditions. Appl. Biochem. Biotechnol. 172: 549-560.
    Pubmed CrossRef
  10. Shaikh SS, Wani SJ, Sayyed RZ. 2016. Statistical-based optimization and scale-up of siderophore production process on laboratory bioreactor. 3 Biotech. 6: 69.
    Pubmed KoreaMed CrossRef
  11. Sayyed RZ, Badgujar MD, Sonawane HM, Mhaske MM, Chincholkar SB. 2005. Production of microbial iron chelators (siderophores) by fluorescent pseudomonads. Indian J. Biotechnol. 4: 484-490.
  12. Dimkpa CO, Svatos A, Dabrowska P, Schmidt A, Boland W, Kothe E. 2008. Involvement of siderophores in the reduction of metal-induced inhibition of auxin synthesis in Streptomyces spp. Chemosphere 74: 19-25.
    Pubmed CrossRef
  13. Gaonkar T, Bhosle S. 2013. Effect of metals on a siderophore producing bacterial isolate and its implications on microbial assisted bioremediation of metal contaminated soils. Chemosphere 93: 1835-1843.
    Pubmed CrossRef
  14. Braud A, Hoegy F, Jezequel K, Lebeau T, Schalk IJ. 2009. New insights into the metal specificity of the Pseudomonas aeruginosa pyoverdine-iron uptake pathway. Environ. Microbiol. 11: 1079-1091.
    Pubmed CrossRef
  15. Ren G, Jin Y, Zhang C, Gu H, Qu J. 2015. Characteristics of Bacillus sp. PZ-1 and its biosorption to Pb(II). Ecotoxicol. Environ. Saf. 117: 141-148.
    Pubmed CrossRef
  16. Payne SM. 1994. Detection, isolation and characterization of siderophores. Methods Enzymol. 235: 329.
    CrossRef
  17. Csaky TZ. 1948. On the estimation of bound hydroxylamine in biological materials. Acta Chem. Scand. 2: 450-454.
    CrossRef
  18. Arnow LE. 1937. Colorimetric determination of the components of 3,4-dihydroxy phenylalanine tyrosine mixtures. Circ. J. 118: 531-537.
  19. Shenker M, Oliver I, Helmann M, Hadar Y, Chen Y. 1992. Utilization by tomatoes of iron mediated by a siderophore produced by Rhizopus arrhizus. J. Plant Nutr. 15: 2173-2182.
    CrossRef
  20. Kuchenbuch R, Jung J. 1988. Changes in root-shoot ratio and ion uptake of maize (Zea mays L.) from soil as influenced by a plant growth regulator. Plant Soil 109: 151-157.
    CrossRef
  21. Mendez MO, Maier RM. 2008. Phytostabilization of mine tailings in arid and semiarid environments - an emerging remediation technology. Environ. Health Perspect. 116: 278-283.
    Pubmed KoreaMed CrossRef
  22. Manwar AV, Khandelwal SR, Chaudhari BL, Meyer JM, Chincholkar SB. 2004. Siderophore production by a marine Pseudomonas aeruginosa and its antagonistic action against phytopathogenic fungi. Appl. Biochem. Biotechnol. 118: 243.
    CrossRef
  23. Chakraborty U, Chankrabopty B, Basnet M. 2006. Plant growth promotion and induction of resistance in Camellia sinensis by Bacillus megaterium. J. Basic Microbiol. 46: 186-195.
    Pubmed CrossRef
  24. Lebeau T, Braud A, Jézéquel K. 2008. Performance of bioaugmentation-assisted phytoextraction applied to metal contaminated soils: a review. Environ. Pollut. 153: 497-522.
    Pubmed CrossRef
  25. Fuloria A, Saraswat S, Rai JPN. 2009. Effect of Pseudomonas fluorescens on metal phytoextraction from contaminated soil by Brassica juncea. Chem. Ecol. 25: 385-396.
    CrossRef
  26. Sullivan TS, Ramkissoon S, Garrison VH, Ramsubhag A, Thies JE. 2012. Siderophore production of African dust microorganisms over Trinidad and Tobago. Aerobiologia 28:391-401.
    CrossRef
  27. Xiao R, Kisaalita WS. 1998. Fluorescent pseudomonad pyoverdines bind and oxidize ferrous ion. Appl. Environ. Microbiol. 64: 1472-1476.
  28. Mahmoud ALE, Abd-Alla MH. 2011. Siderophore production by some microorganisms and their effect on BradyrhizobiumMung bean symbiosis. Int. J. Agric. Biol. 3: 157-162.
  29. Yu X, Ai C, Xin L, Zhou G. 2011. The siderophore-producing bacterium, Bacillus subtilis CAS15, has a biocontrol effect on Fusarium wilt and promotes the growth of pepper. Eur. J. Soil Biol. 47: 138-145.
    CrossRef
  30. Rachid D, Ahmed B. 2005. Effect of iron and growth inhibitors on siderophores production by Pseudomonas fluorescens. Afr. J. Biotechnol. 4: 697-702.
    CrossRef
  31. Naik MM, Dubey SK. 2011. Lead-enhanced siderophore production and alteration in cell morphology in a Pbresistant Pseudomonas aeruginosa strain 4EA. Curr. Microbiol. 62: 409-414.
    Pubmed CrossRef
  32. Clarke SE, Stuart J, Sanders-Loehr J. 1987. Induction of siderophore activity in Anabaena spp. and its moderation of copper toxicity. Appl. Environ. Microbiol. 53: 917-922.
  33. Waldron KJ, Tottey S, Yanagisawa S, Dennison C, Robinson NJ. 2007. A periplasmic iron-binding protein contributes toward inward copper supply. J. Biol. Chem. 282: 3837-3846.
    Pubmed CrossRef
  34. Sinha S, Mukherjee SK. 2008. Cadmium-induced siderophore production by a high Cd-resistant bacterial strain relieved Cd toxicity in plants through root colonization. Curr. Microbiol.56: 55-60.
    Pubmed CrossRef
  35. Rossbach S, Wilson TL, Kukuk ML, Carty HA. 2000. Elevated zinc induces siderophore biosynthesis genes and a zntA-like gene in Pseudomonas fluorescens. FEMS Microbiol.Lett. 191: 61-70.
    CrossRef
  36. Duffy BK, Defago G. 1999. Environmental factors modulating antibiotic and siderophore biosynthesis by Pseudomonas fluorescens biocontrol strains. Appl. Environ. Microbiol. 65:2429-2438.
  37. Abd-Alla MH. 1998. Growth and siderophore production in vitro of Bradyrhizobium (Lupin) strains under iron limitation. Folia Microbiol. 44: 196-200.
    CrossRef
  38. Saha R, Saha N, Donofrio RS, Bestervelt LL. 2013. Microbial siderophores: a mini review. J. Basic. Microbiol. 53: 303-317.
    Pubmed CrossRef
  39. Federspiel A, Schuler R, Haselwandter K. 1991. Effect of pH, L-ornithine and L-proline on the hydroxamate siderophore production by Hymenoscyphus ericae, a typical ericoid mycorrhizal fungus. Plant Soil 130: 259-261.
    CrossRef
  40. Ugwu DI, Ezema BE, Eze FU, Ayogu JI, Ezema CG, Ugwuja DI. 2014. Synthesis and biological applications of hydroxamates. Cheminform 4: 26-51.
    Pubmed KoreaMed CrossRef
  41. Wu CH, Wood TK, Mulchandani A, Chen W. 2006. Engineering plant-microbe symbiosis for rhizoremediation of heavy metals. Appl. Environ. Microbiol. 72: 1129-1134.
    Pubmed KoreaMed CrossRef
  42. Gadd GM. 2004. Microbial influence on metal mobility and application for bioremediation. Geoderma 122: 109-119.
    CrossRef
  43. Nadeem SM, Ahmad M, Zahir ZA, Javaid A, Ashraf M. 2014. The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol. Adv. 32: 429-448.
    Pubmed CrossRef
  44. Ernst WH. 2000. Evolution of metal hyperaccumulation and phytoremediation hype. New Phytol. 146: 357-358.
    CrossRef
  45. Davies JFT, Puryear JD, Newton RJ, Egilla JN, Saraiva Grossi JA. 2001. Mycorrhizal fungi enhance accumulation and tolerance of chromium in sunflower (Helianthus annuus). J. Plant Physiol. 158: 777-786.
    CrossRef
  46. Compant S, Clement C, Sessitsch A. 2010. Plant growthpromoting bacteria in the rhizo- and endosphere of plants:their role, colonization, mechanisms involved and prospects for utilization. Soil Biol. Biochem. 42: 669-678.
    CrossRef
  47. Ahemad M, Kibret M. 2014. Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J. King Saud Univ. Sci. 26: 1-20.
    CrossRef