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.
Similar content being viewed by others
References
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.
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.
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.
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.
Woodward, A. W. and B. Bartel (2005) Auxin: regulation, action, and interaction. Ann. Bot. 95: 707–735.
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.
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.
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.
Egamberdieva, D. (2009) Alleviation of salt stress by plant growth regulators and IAA producing bacteria in wheat. Acta Physiol. Plant. 31: 861–864.
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.
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.
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.
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.
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.
Wagi, S. and A. Ahmed (2019) Bacillus spp.: potent microfactories of bacterial IAA. PeerJ. 7: e7258.
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.
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.
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.
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.
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.
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.
Bitter, T. and H. M. Muir (1962) A modified uronic acid carbazole reaction. Anal. Biochem. 4: 330–334.
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.
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.
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.
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.
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.
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.
Kucuk, C. and C. Cevheri (2015) In vitro antagonism of Rhizobium strains isolated from various legumes. J. Pure Appl. Microbiol. 9: 503–511.
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.
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.
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.
Bouknight, R. R. and H. L. Sadoff (1975) Tryptophan catabolism in Bacillus megaterium. J. Bacteriol. 121: 70–76.
Colabroy, K. L. and T. P. Begley (2005) Tryptophan catabolism: identification and characterization of a new degradative pathway. J. Bacteriol. 187: 7866–7869.
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.
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.
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.
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.
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.
Botsford, J. L. and R. D. DeMoss (1971) Catabolite repression of tryptophanase in Escherichia coli. J. Bacteriol. 105: 303–312.
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.
Salcher, O. and F. Lingens (1980) Metabolism of tryptophan by Pseudomonas aureofaciens and its relationship to pyrrolnitrin biosynthesis. J. Gen. Microbiol. 121: 465–471.
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.
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.
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.
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
Corresponding authors
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
About this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12257-023-0056-x