Skip to main content
Log in

Indole-3-acetic Acid Production from Alginate by Vibrio sp. dhg: Physiology and Characteristics

  • Research Paper
  • Published:
Biotechnology and Bioprocess Engineering Aims and scope Submit manuscript

Abstract

The production of indole-3-acetic acid (IAA) by bacteria has attracted considerable attention in plant studies due to its significant role as a plant growth regulator. In this study, it was confirmed that Vibrio sp. dhg, a novel microbial platform capable of assimilating alginate, can naturally synthesize IAA. The effects of L-tryptophan and the carbon sources obtained from brown algae (glucose, mannitol, and alginate) were also examined to characterize the IAA biosynthesis in Vibrio sp. dhg. The highest IAA production (9.32 ± 0.25 mg/L) was observed in the alginate medium containing 0.8 g/L of L-tryptophan. Interestingly, alginate was found to be a favorable option for IAA production due to the rapid uptake of L-tryptophan during the exponential phase. By adding external NADH, this study demonstrated that the low net reducing equivalents in the alginate medium were linked to this phenomenon. This study is the first to provide alginate as the sole carbon source for IAA production and to propose that the oxidoreduction potentials of the carbon source can affect bacterial IAA biosynthesis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Lim, H. G., D. H. Kwak, S. Park, S. Woo, J.-S. Yang, C. W. Kang, B. Kim, M. H. Noh, S. W. Seo, and G. Y. Jung (2019) Vibrio sp. dhg as a platform for the biorefinery of brown macroalgae. Nat. Commun. 10: 2486.

    PubMed  PubMed Central  Google Scholar 

  2. Oh, Y., X. Xu, J. Y. Kim, and J. M. Park (2015) Maximizing the utilization of Laminaria japonica as biomass via improvement of alginate lyase activity in a two-phase fermentation system. Biotechnol. J. 10: 1281–1288.

    CAS  PubMed  Google Scholar 

  3. Woo, S., J. H. Moon, J. Sung, D. Baek, Y. J. Shon, and G. Y. Jung (2022) Recent advances in the utilization of brown macroalgae as feedstock for microbial biorefinery. Biotechnol. Bioprocess Eng. 27: 879–889.

    CAS  Google Scholar 

  4. Woo, S., H. G. Lim, Y. H. Han, S. Park, M. H. Noh, D. Baek, J. H. Moon, S. W. Seo, and G. Y. Jung (2022) A Vibrio-based microbial platform for accelerated lignocellulosic sugar conversion. Biotechnol. Biofuels. Bioprod. 15: 58.

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Woodward, A. W. and B. Bartel (2005) Auxin: regulation, action, and interaction. Ann. Bot. 95: 707–735.

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Duca, D., J. Lorv, C. L. Patten, D. Rose, and B. R. Glick (2014) Indole-3-acetic acid in plant–microbe interactions. Antonie Van Leeuwenhoek 106: 85–125.

    CAS  PubMed  Google Scholar 

  7. Mohite, B. (2013) Isolation and characterization of indole acetic acid (IAA) producing bacteria from rhizospheric soil and its effect on plant growth. J. Soil Sci. Plant Nutr. 13: 638–649.

    Google Scholar 

  8. Hernández-Montiel, L. G., C. J. Chiquito Contreras, B. Murillo Amador, L. Vidal Hernández, E. E. Quiñones Aguilar, and R. G. Chiquito Contreras (2017) Efficiency of two inoculation methods of Pseudomonas putida on growth and yield of tomato plants. J. Soil Sci. Plant Nutr. 17: 1003–1012.

    Google Scholar 

  9. Egamberdieva, D. (2009) Alleviation of salt stress by plant growth regulators and IAA producing bacteria in wheat. Acta Physiol. Plant. 31: 861–864.

    CAS  Google Scholar 

  10. Ona, O., J. Van Impe, E. Prinsen, and J. Vanderleyden (2005) Growth and indole-3-acetic acid biosynthesis of Azospirillum brasilense Sp245 is environmentally controlled. FEMS Microbiol. Lett. 246: 125–132.

    CAS  PubMed  Google Scholar 

  11. Apine, O. A. and J. P. Jadhav (2011) Optimization of medium for indole-3-acetic acid production using Pantoea agglomerans strain PVM. J. Appl. Microbiol. 110: 1235–1244.

    CAS  PubMed  Google Scholar 

  12. Chaiharn, M. and S. Lumyong (2011) Screening and optimization of indole-3-acetic acid production and phosphate solubilization from rhizobacteria aimed at improving plant growth. Curr. Microbiol. 62: 173–181.

    CAS  PubMed  Google Scholar 

  13. Bharucha, U., K. Patel, and U. B. Trivedi (2013) Optimization of indole acetic acid production by Pseudomonas putida UB1 and its effect as plant growth-promoting rhizobacteria on mustard (Brassica nigra). Agric. Res. 2: 215–221.

    CAS  Google Scholar 

  14. Ahmed, M., L. J. Stal, and S. Hasnain (2010) Production of indole-3-acetic acid by the cyanobacterium Arthrospira platensis strain MMG-9. J. Microbiol. Biotechnol. 20: 1259–1265.

    CAS  PubMed  Google Scholar 

  15. Wagi, S. and A. Ahmed (2019) Bacillus spp.: potent microfactories of bacterial IAA. PeerJ. 7: e7258.

    PubMed  PubMed Central  Google Scholar 

  16. Lee, Y.-G., Y. Ju, L. Sun, S. Park, Y.-S. Jin, and S. R. Kim (2022) Acetate-rich cellulosic hydrolysates and their bioconversion using yeasts. Biotechnol. Bioprocess Eng. 27: 890–899.

    CAS  Google Scholar 

  17. Emami, S., H. A. Alikhani, A. A. Pourbabaei, H. Etesami, F. Sarmadian, and B. Motessharezadeh (2019) Assessment of the potential of indole-3-acetic acid producing bacteria to manage chemical fertilizers application. Int. J. Environ. Res. 13: 603–611.

    CAS  Google Scholar 

  18. Mujahid, M., C. Sasikala, and C. V. Ramana (2013) Carbon catabolite repression-independent and pH-dependent production of indoles by Rubrivivax benzoatilyticus JA2. Curr. Microbiol. 67: 399–405.

    CAS  PubMed  Google Scholar 

  19. Sasirekha, B., S. Shivakumar, and S. B. Sullia (2012) Statistical optimization for improved indole-3-acetic acid (iaa) production by Pseudomonas aeruginosa and demonstration of enhanced plant growth promotion. J. Soil Sci. Plant Nutr. 12: 863–873.

    Google Scholar 

  20. Jeyanthi, V. and P. Ganesh (2013) Production, optimization and characterization of phytohormone indole acetic acid by Pseudomonas fluorescence. Int. J. Pharm. Biol. Sci. Arch. 4: 514–520.

    Google Scholar 

  21. Sergeeva, E., D. L. M. Hirkala, and L. M. Nelson (2007) Production of indole-3-acetic acid, aromatic amino acid aminotransferase activities and plant growth promotion by Pantoea agglomerans rhizosphere isolates. Plant Soil. 297: 1–13.

    CAS  Google Scholar 

  22. Bitter, T. and H. M. Muir (1962) A modified uronic acid carbazole reaction. Anal. Biochem. 4: 330–334.

    CAS  PubMed  Google Scholar 

  23. Gang, S., S. Sharma, M. Saraf, M. Buck, and J. Schumacher (2019) Analysis of indole-3-acetic acid (IAA) production in Klebsiellaby LC-MS/MS and the Salkowski method. Bio Protoc. 9: e3230.

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Szkop, M. and W. Bielawski (2013) A simple method for simultaneous RP-HPLC determination of indolic compounds related to bacterial biosynthesis of indole-3-acetic acid. Antonie Van Leeuwenhoek 103: 683–691.

    CAS  PubMed  Google Scholar 

  25. Górka, B. and P. P. Wieczorek (2017) Simultaneous determination of nine phytohormones in seaweed and algae extracts by HPLC-PDA. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 1057: 32–39.

    PubMed  Google Scholar 

  26. Hoffart, E., S. Grenz, J. Lange, R. Nitschel, F. Müller, A. Schwentner, A. Feith, M. Lenfers-Lücker, R. Takors, and B. Blombach (2017) High substrate uptake rates empower Vibrio natriegens as production host for industrial biotechnology. Appl. Environ. Microbiol. 83: e01614–e01617.

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Ghosh, S., C. Sengupta, T. K. Maiti, and P. S. Basu (2008) Production of 3-indolylacetic acid in root nodules and culture by a Rhizobium species isolated from root nodules of the leguminous pulse Phaseolus mungo. Folia Microbiol. (Praha) 53: 351–355.

    CAS  PubMed  Google Scholar 

  28. Gutierrez, C. K., G. Y. Matsui, D. E. Lincoln, and C. R. Lovell (2009) Production of the phytohormone indole-3-acetic acid by estuarine species of the genus Vibrio. Appl. Environ. Microbiol. 75: 2253–2258.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Kucuk, C. and C. Cevheri (2015) In vitro antagonism of Rhizobium strains isolated from various legumes. J. Pure Appl. Microbiol. 9: 503–511.

    Google Scholar 

  30. Patten, C. L., A. J. C. Blakney, and T. J. D. Coulson (2013) Activity, distribution and function of indole-3-acetic acid biosynthetic pathways in bacteria. Crit. Rev. Microbiol. 39: 395–415.

    CAS  PubMed  Google Scholar 

  31. Yang, S., Q. Zhang, J. Guo, A. O. Charkowski, B. R. Glick, A. M. Ibekwe, D. A. Cooksey, and C.-H. Yang (2007) Global effect of indole-3-acetic acid biosynthesis on multiple virulence factors of Erwinia chrysanthemi 3937. Appl. Environ. Microbiol. 73: 1079–1088.

    CAS  PubMed  Google Scholar 

  32. Ryu, R. J. and C. L. Patten (2008) Aromatic amino acid-dependent expression of indole-3-pyruvate decarboxylase is regulated by TyrR in Enterobacter cloacae UW5. J. Bacteriol. 190: 7200–7208.

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Bouknight, R. R. and H. L. Sadoff (1975) Tryptophan catabolism in Bacillus megaterium. J. Bacteriol. 121: 70–76.

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Colabroy, K. L. and T. P. Begley (2005) Tryptophan catabolism: identification and characterization of a new degradative pathway. J. Bacteriol. 187: 7866–7869.

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Bortolotti, P., B. Hennart, C. Thieffry, G. Jausions, E. Faure, T. Grandjean, M. Thepaut, R. Dessein, D. Allorge, B. P. Guery, K. Faure, E. Kipnis, B. Toussaint, and A. L. Gouellec (2016) Tryptophan catabolism in Pseudomonas aeruginosa and potential for inter-kingdom relationship. BMC Microbiol. 16: 137.

    PubMed  PubMed Central  Google Scholar 

  36. Bang, H. B., I. H. Choi, J. H. Jang, and K. J. Jeong (2021) Engineering of Escherichia coli for the economic production L-phenylalanine in large-scale bioreactor. Biotechnol. Bioprocess Eng. 26: 468–475.

    CAS  Google Scholar 

  37. Zhang, G., X. Ren, X. Liang, Y. Wang, D. Feng, Y. Zhang, M. Xian, and H. Zou (2021) Improving the microbial production of amino acids: from conventional approaches to recent trends. Biotechnol. Bioprocess Eng. 26: 708–727.

    CAS  Google Scholar 

  38. Enquist-Newman, M., A. M. E. Faust, D. D. Bravo, C. N. S. Santos, R. M. Raisner, A. Hanel, P. Sarvabhowman, C. Le, D. D. Regitsky, S. R. Cooper, L. Peereboom, A. Clark, Y. Martinez, J. Goldsmith, M. Y. Cho, P. D. Donohoue, L. Luo, B. Lamberson, P. Tamrakar, E. J. Kim, J. L. Villari, A. Gill, S. A. Tripathi, P. Karamchedu, C. J. Paredes, V. Rajgarhia, H. K. Kotlar, R. B. Bailey, D. J. Miller, N. L. Ohler, C. Swimmer, and Y. Yoshikuni (2014) Efficient ethanol production from brown macroalgae sugars by a synthetic yeast platform. Nature 505: 239–243.

    CAS  PubMed  Google Scholar 

  39. Ji, S.-Q., B. Wang, M. Lu, and F.-L. Li (2016) Direct bioconversion of brown algae into ethanol by thermophilic bacterium Defluviitalea phaphyphila. Biotechnol. Biofuels. 9: 81.

    PubMed  PubMed Central  Google Scholar 

  40. Botsford, J. L. and R. D. DeMoss (1971) Catabolite repression of tryptophanase in Escherichia coli. J. Bacteriol. 105: 303–312.

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Bertin, Y., C. Deval, A. de la Foye, L. Masson, V. Gannon, J. Harel, C. Martin, M. Desvaux, and E. Forano (2014) The gluconeogenesis pathway is involved in maintenance of enterohaemorrhagic Escherichia coli O157:H7 in bovine intestinal content. PLoS One 9: e98367.

    PubMed  PubMed Central  Google Scholar 

  42. Salcher, O. and F. Lingens (1980) Metabolism of tryptophan by Pseudomonas aureofaciens and its relationship to pyrrolnitrin biosynthesis. J. Gen. Microbiol. 121: 465–471.

    CAS  PubMed  Google Scholar 

  43. Li, Y., B. Liu, J. Guo, H. Cong, S. He, H. Zhou, F. Zhu, Q. Wang, and L. Zhang (2019) L-Tryptophan represses persister formation via inhibiting bacterial motility and promoting antibiotics absorption. Future Microbiol. 14: 757–771.

    CAS  PubMed  Google Scholar 

  44. Zhang, C., K. Ma, and X.-H. Xing (2009) Regulation of hydrogen production by Enterobacter aerogenes by external NADH and NAD+. Int. J. Hydrogen Energy 34: 1226–1232.

    CAS  Google Scholar 

  45. Wang, J., Y. M. Kim, H. S. Rhee, M. W. Lee, and J. M. Park (2013) Bioethanol production from mannitol by a newly isolated bacterium, Enterobacter sp. JMP3. Bioresour. Technol. 135: 199–206.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by Korea Institute of Marine Science & Technology Promotion (KIMST) funded by the Ministry of Oceans and Fisheries, Korea (20220258).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Gyoo Yeol Jung or Jong Moon Park.

Ethics declarations

The authors declare no conflict of interest. Neither ethical approval nor informed consent was required for this study.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shin, H.J., Woo, S., Jung, G.Y. et al. Indole-3-acetic Acid Production from Alginate by Vibrio sp. dhg: Physiology and Characteristics. Biotechnol Bioproc E 28, 695–703 (2023). https://doi.org/10.1007/s12257-023-0056-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12257-023-0056-x

Keywords

Navigation