Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Production of Exopolysaccharides and İndole Acetic Acid (IAA) by Rhizobacteria and Their Potential against Drought Stress in Upland Rice

  • Tetty Marta Linda (Department of Biology, Faculty of Mathematics and Natural Sciences, Riau University) ;
  • Jusinta Aliska (Department of Biology, Faculty of Mathematics and Natural Sciences, Riau University) ;
  • Nita Feronika (Department of Biology, Faculty of Mathematics and Natural Sciences, Riau University) ;
  • Ineiga Melisa (Department of Biology, Faculty of Mathematics and Natural Sciences, Riau University) ;
  • Erwina Juliantari (Department of Biology, Faculty of Mathematics and Natural Sciences, Riau University)
  • Received : 2024.01.31
  • Accepted : 2024.04.26
  • Published : 2024.06.28
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Abstract

Peatlands are marginal agricultural lands due to highly acidic soil conditions and poor drainage systems. Drought stress is a big problem in peatlands as it can affect plants through poor root development, so technological innovations are needed to increase the productivity and sustainability of upland rice on peatlands. Rhizobacteria can overcome the effects of drought stress by altering root morphology, regulating stress-responsive genes, and producing exopolysaccharides and indole acetic acid (IAA). This study aimed to determine the ability of rhizobacteria in upland rice to produce exopolysaccharides and IAA, identify potential isolates using molecular markers, and prove the effect of rhizobacteria on viability and vigor index in upland rice. Rhizobacterial isolates were grown on yeast extract mannitol broth (YEMB) medium for exopolysaccharides production testing and Nutrient Broth (NB)+L-tryptophan medium for IAA production testing. The selected isolates identify using sequence 16S rRNA. The variables observed in testing the effect of rhizobacteria were germination ability, vigour index, and growth uniformity. EPS-1 isolate is the best production of exopolysaccharides (41.6 mg/ml) and IAA (60.83 ppm). The isolate EPS-1 was identified as Klebsiella variicola using 16S rRNA sequencing and phylogenetic analysis. The isolate EPS-1 can increase the viability and vigor of upland rice seeds. K. variicola is more adaptive and has several functional properties that can be developed as a potential bioagent or biofertilizer to improve soil nutrition, moisture and enhance plant growth. The use of rhizobacteria can reduce dependence on the use of synthetic materials with sustainable agriculture.

Keywords

Acknowledgement

The authors would like to thank all authors and researchers who have assisted in the research, administrative and technical processes.

References

  1. Surahman A, Soni P, Shivakoti G. 2018. Reducing CO2 emissions and supporting food security in Central Kalimantan, Indonesia, with improved peatland management. Land Use Policy 72: 325-332.
  2. Pratiwi E, Satwika TD, Akhdiya A, Agus F. 2020. Characteristics of bacteria from Jambi's peatlands and their potential as bio fertilizers. J. Tanah Iklim. 44: 1-10.
  3. Simatupang D, Astiani D, Widyastuti T. 2018. The influence of high groundwater levels on several physical and chemical properties of peat soil in Kuala Dua Village, Kubu Raya District. J. Hut. Les. 6: 988-1008.
  4. Munir N, Hanif M, Abideen Z, Sohail M, El-Keblawy A. 2022. Mechanisms and strategies of plant microbiome interactions to mitigate abiotic stresses. Agronomy 12: 2069.
  5. Pang Z, Zhao Y, Xu P, Yu D. 2020. Microbial diversity of upland rice roots and their influence on rice growth and drought tolerance. Microorganisms 8: 1329.
  6. Razack SA, Velayutham V, Thangavelu V. 2013. Medium optimization for the production of exopolysaccharide by Bacillus subtilis using synthetic sources and agro wastes. Turkish J. Bio. 37: 280-288.
  7. Kim AY, Shahzad R, Kang SM, Seo CW, Park YG. 2017. IAA producing Klebsiella variicola AY13 reprograms soybean growth during flooding stress. J. Crop Sci. Biotechnol. 20: 235-242.
  8. Saeed Q, Xiukang W, Haider FU, Kucerik J, Mumtaz MZ. 2021. Rhizosphere bacteria in plant growth promotion, biocontrol, and bioremediation of contaminated sites: a comprehensive review of effects and mechanisms. Int. J. Mol. Sci. 22:10529.
  9. Tiwari ON, Sasmal S, Kataria AK, Devi I. 2020. Application of microbial extracellular carbohydrate polymeric substances in food and allied industries. 3 Biotech. 10: 221-230.
  10. Shultana R, Kee Zuan AT, Yusop MR, Saud HM. 2020. Characterization of salt-tolerant plant growth-promoting rhizobacteria and the effect on growth and yield of saline-affected rice. PLoS One 15: e0238537.
  11. Astorga-Elo M, Gonzalez S, Acuna JJ, Sadowsky MJ, Jorquera MA. 2021. Rhizobacteria from 'flowering desert'events contribute to the mitigation of water scarcity stress during tomato seedling germination and growth. Sci. Rep. 11: 13745.
  12. Nadeem SM, Ahmad M, Tufail MA, Asghar HN, Nazli F, Zahir ZA. 2021. Appraising the potential of EPS-producing rhizobacteria with ACC-deaminase activity to improve growth and physiology of maize under drought stress. Physiol. Plant 172: 463-476.
  13. Naseem H, Bano A. 2014. Role of plant growth-promoting rhizobacteria and their exopolysaccharide in drought tolerance of maize. J. Plant Interac. 9: 689-701.
  14. Hindersah R, Rostini N, Harsono A, Nuryani. 2017. Population increase, growth and nitrogen uptake of soybean plants by administration of exopolysaccharide producing azotobacter. Indones. J. Agron. 45: 30-35.
  15. Harahap N, Santoso DA, Gofur N. 2018. The potential of exopolysaccharide-producing bacteria from rhizosphere of rubber plants for improving soil aggregate. J. Degrade. Min. Land. Manage. 5: 2502-2458.
  16. Sayyed RZ, Patel PR dan Shaikh SS. 2015. Plant growth promotion and root colonization by eps producing Enterobacter sp. RZS5 under heavy metal contaminated soil. Indian J. Exp. Bio. 53: 116-123.
  17. Gupta P, Diwan B. 2016. Bacterial exopolysaccharide mediated heavy metal removal: a review on biosynthesis, mechanism and remediation strategies. Biotechnol. Rep. 23: 58-71.
  18. Widyaningtias NMSR, Yustiantara PS, Paramita NLPV. 2014. Antibacterial activity test of purified extract of green betel leaf (Piper betle L.) against Propionibacterium acnes bacteria. J. Farm. Udayana 3: 50-55.
  19. Nazli F, Jamil M, Hussain A, Hussain T. 2020. Exopolysaccharides and indole-3-acetic acid producing Bacillus safensis strain FN13 potential candidate for phytostabilization of heavy metals. Environ. Monit. Assess. 192: 1-16.
  20. Cox CE, Brandl MT, de Moraes MH, Gunasekera S, Teplitski M. 2018. Production of the plant hormone auxin by Salmonella and its role in the interactions with plants and animals. Front. Microbiol. 8: 2668.
  21. Ma'unatin A, Harijono, Zubaidah E, Rifa'i M. 2020. The isolation of ecopolysaccharide-producing lactic acid bacteria from lontar (Borassus flabellifer L.) sap. Iran. J. Microbiol. 12: 437-444.
  22. Susilowati DN, Setyowati M. 2017. Screening and physiological characterization of rice rhizosphere bacteria from coastal soil that produce indol acetic acid in saline condition. Proc. The SATREPS Conf. 1: 153-160.
  23. Machado RG, de Sa ELS, Bruxel M, Giongo A, da Silva Santos N, Nunes AS. 2013. Indole acetic acid producing rhizobia promote growth of Tanzania grass (Panicum maximum) and Pensacola grass (Paspalum saurae). Int. J. Agric. Biol. 15: 827-834.
  24. Bafana A. 2013. Diversity and metabolic potential of culturable root-associated bacteria from Origanum vulgare in sub-Himalayan region. World J. Microbiol. Biotechnol. 29: 63-74.
  25. Hindersah R, Sudirja R. 2010. Temperature and incubation time to optimize exopolysaccharide content and inoculant phytohormones. J. Natur. Indonesia 13: 67-71.
  26. Mu'minah, Baharuddin, Subair FH, Fahruddin. 2015. Isolation and screening bacterial exopolysaccharide (EPS) from potato rhizosphere in highland and the potential as a producer indole acetic acid (IAA). Proc. Food Sci. 3: 74-81.
  27. Patten CL, Glick BR. 2002. Role of Pseudomonas putida indole-3-acetic acid in development of the host plant root system. J. Appl. Environ. Microbiol. 68: 3795-3801.
  28. Mudi L, Muhidin, Rakian TC, Sutariati GAK, Leomo S, Yusuf DN. 2021. Effectivity of Pseudomonas fluorescens TBT214 in increasing soybean seed quality in different seed vigor. IOP Conf. Ser: Earth Environ. Sci. 807: 042069.
  29. Hardiansyah MH, Musa Y, Jaya AM. 2020. Identification plant growth promoting rhizobacteria on bambu duri rhizosfer with KOH 3%. Agrotech. Res. J. 4: 41-46.
  30. Hereher F, Elfallal A, Abou-Dobara M, Toson E, Abdelaziz MM. 2018. Cultural optimization of a new exopolysaccharide producer Micrococcus roseus. Beni Suef. Univ. J. Basic Appl. Sci. 7: 632-639.
  31. Abdul RS, Velayutham V, Thangavelu V. 2013. Medium optimization for the production of exopolysaccharide by Bacillus subtilis using synthetic sources and agro wastes. Turkish J. Bio. 37: 280-288.
  32. Zhang P, Jin T, Kumar Sahu S, Xu J, Shi Q. 2019. The distribution of tryptophan-dependent indole-3-acetic acid synthesis pathways in bacteria unraveled by large-scale genomic analysis. Molecules 24: 1411.
  33. Sukmadewi DKT, Suharjono, Antonius S. 2015. Potential test of iaa (indole acetic acid) hormone producing bacteria from rhizosphere soil in Cengkeh (Syzigium aromaticum L.). J. Biotrop. 3: 91-94.
  34. Hanafi A, Purwantisari S, Raharjo DB. 2017. Potential test of chitinolytic endophytic bacteria of rice plants (Oryza sativa L.) as IAA (Indole Acetic Acid) hormone producers. Bioma. 19: 76-82.
  35. Gang S, Sharma S, Saraf M, Buck M, Schumacher J. 2019. Analysis of Indole-3-acetic Acid (IAA) production in Klebsiella by LC-MS/MS and the Salkowski method. Bio. Protocol. 9: e3230.
  36. Srinivasan R, Karaoz U, Volegova M, MacKichan J, Kato-Maeda M. 2015. Use of 16S rRNA gene for identification of a broad range of clinically relevant bacterial pathogens. PLoS One 10: e0177617.
  37. Bhardwaj G, Shah R, Joshi B, Patel P. 2017. Klebsiella pneumoniae VRE36 as a PGPR isolated from Saccharum officinarum cultivar Co99004. J. Appl. Biol. Biotechnol. 5: 47-52.
  38. Rahma H, Nurbailis, Kristina N. 2019. Characterization and potential of plant growth-promoting rhizobacteria on rice seedling growth and the effect on Xanthomonas oryzae pv. oryzae. Biodiversitas 20: 3654-3661.
  39. Gavrilescu M. 2021. Water, soil, and plants interactions in a threatened environment. Water 13: 2746.
  40. Cheng C, Shang-Guan W, He L, Sheng X. 2020. Effect of exopolysaccharide-producing bacteria on water-stable macro-aggregate formation in soil. Geomicrobiol. J. 37: 738-745.
  41. Khan N, Bano A. 2019. Exopolysaccharide producing rhizobacteria and their impact on growth and drought tolerance of wheat grown under rainfed conditions. PLoS One 14: e0222302.
  42. Ahmad HM, Fiaz S, Hafeez S, Zahra S, Shah AN. 2022. Plant growth-promoting rhizobacteria eliminate the effect of drought stress in plants: a review. Front. Plant Sci. 13: 875774.
  43. Schmid J, Sieber V, Rehm B. 2015. Bacterial exopolysaccharides: biosynthesis pathways and engineering strategies. Front. Microbiol. 6: 496.
  44. Bhagat N, Raghav M, Dubey S, Bedi N. 2021. Bacterial exopolysaccharides: insight into their role in plant abiotic stress tolerance. J. Microbiol. Biotechnol. 31: 1045-1059.
  45. Negi R, Kaur T, Devi R, Kour D, Yadav AN. 2022. Assessment of nitrogen-fixing endophytic and mineral solubilizing rhizospheric bacteria as multifunctional microbial consortium for growth promotion of wheat and wild wheat relative Aegilops kotschyi. Heliyon 8: e12579.
  46. Karbowiak T, Ferret E, Debeaufort F, Voilley A, Cayot P. 2011. Investigation of water transfer across thin layer biopolymer films by infrared spectroscopy. J. Membrane Sci. 370: 82-90.
  47. Morcillo RJL, Manzanera M. 2021. The effects of plant-associated bacterial exopolysaccharides on plant abiotic stress tolerance. Metabolites J. 11: 1-29.
  48. Fatima T, Arora NK. 2020. Pseudomonas entomophila PE3 and its exopolysaccharides as biostimulants for enhancing growth, yield and tolerance responses of sunflower under saline conditions. Microbiol. Res. 244: 126671.
  49. Ismail B, Nampoothiri KM. 2010. Production, purification and structural characterization of an exopolysaccharide produced by a probiotic Lactobacillus plantarum MTCC 9510. Arch. Microbiol. 192: 1049-1057.
  50. Kenshiro OM. 2021. Plant fungal mutualism as a strategy for the bioremediation of hydrocarbon polluted soils [tesis]. Africa: Doctor of Philosophy (Enviromental Biotechnology) Program of Rhodes University.
  51. Zeng W, Li F, Wu C, Yu R, Wu X, Shen L, Liu Y, Qiu G, Li J. 2020. Role of extracellular polymeric substance (EPS) in toxicity response of soil bacteria Bacillus sp. S3 to multiple heavy metals. Bioprocess Biosyst. Eng. 43: 153-167
  52. Habib S, Ahmed A. 2021. Screening of bacteria for biosurfactants, exopolysaccharides and biofilms and their impact on growth stimulation of Zea mays grown under petrol stress. Int. J. Agric. Bio. 26: 309-316.
  53. Scisel JJ, Nowak A, Komaniecka I, Choma A, Wilkolazka AJ, Jaroszuk MO, et al. 2020. differences in production, composition, and antioxidant activities of exopolymeric substances (eps) obtained from cultures of endophytic Fusarium culmorum strains with different effects on cereals. Molecules 25: 616.
  54. Larosa SF, Kusdiyantini E, Raharjo B, Sarjiya A. 2013. Ability of indole acetic acid-producing bacterial isolates acid (iaa) producing bacterial isolates from peat soil sampit kalimantan central. J. Bio. 2: 41-45.
  55. Rover, Mayerni R, Yanti Y, Syarif A. 2019. Isolation and characterization of endofytic bacteria indigenus potentially producing IAA (indole acetic acid) in west sumatera and their effect on nursery palm oil (Elaeis guineensis jacq). J. Appl. Agric. Sci. Technol. 3: 257-267.
  56. Wahyuni D, Linda TM, Lestari W. 2016. Potency of phosphate solubilizing bacterial isolate from peat soil in Riau in producing indole acetic acid (IAA) hormone and its effect on red chili seed (Capsicum annuum L.) Germination. Bio-Site 2: 32-38.
  57. Silitonga DM, Priyani N, Nurwahyuni I. 2012. Isolation and potential testing of isolates of phosphate-dissolving bacteria and IAA (Indole Acetic Acid) hormone-producing bacteria on the growth of soybean (Glycine max L.) on yellow soil. Saintia Bio. 1: 35-41.
  58. Jumadi O, Liawati, Hartono. 2015. IAA (indole acetic acid) growth regulatory substance production and phosphate dissolving capability of nitrogen fixing bacterial isolates from Takalar Regency. J. Bionat. 16: 43-48.
  59. Di DW, Zhang C, Luo P, An CW, Guo GQ. 2016. The biosynthesis of auxin: how many paths truly lead to IAA?. Plant Growth Regul. 78: 275-285.
  60. Saengsanga T. 2018. Isolation and characterization of indigenous plant growth-promoting rhizobacteria and their effects on growth at the early stage of Thai Jasmine Rice (Oryza sativa L. KDML105). Arab. J. Sci. Eng. 43: 3359-3369.
  61. Qurashi AW, Sabri AN. 2012. Bacterial exopolysaccharide and biofilm formation stimulate chickpea growth and soil aggregation under salt stress. Braz. J. Microbiol. 43: 1183-1191.
  62. Kapli H, Wahyudi AT, Husen E. 2017. Effect of growth promoting and drought tolerant rhizobakteria and soil microbial abundance and activity on corn (Zea mays L.). Biospecies 10: 25-36.
  63. Liu W, Wang Q, Hou J, Tu C, Luo Y, Christie P. 2016. Whole genome analysis of halotolerant and alkalotolerant plant growth-promoting rhizobacterium Klebsiella sp. D5A. Sci. Rep. 6: 26710.
  64. Mishra VK, Kumar A. 2015. Biosynthesis of indole-3-acetic acid by plant growth promoting rhizobacteria, Klebsiella pneumoniae, Bacillus amyloliquefaciens and Bacillus subtilis. Afric. J. Microbiol. Res. 9: 1139-1149.
  65. Poudel M, Mendes R, Costa LAS, Bueno CG, Meng Y. 2021. The role of plant-associated bacteria, fungi, and viruses in drought stress mitigation. Front. Microbiol. 12: 743512.
  66. Kumar A, Verma JP. 2018. Does plant microbe interaction confer stress tolerance in plants: a review. Microbiol. Res. 207: 41-52.
  67. Cassan F, Vanderleyden J, Spaepen S. 2014. Physiological and agronomical aspects of phytohormone production by model plant-growth-promoting rhizobacteria (PGPR) belonging to the genus Azospirillum. J. Plant Growth Regul. 33: 440-459.
  68. Sari M, Nawangsih AA, Wahyudi AT. 2021. Rhizosphere Streptomyces formulas as the biological control agent of phytopathogenic fungi Fusarium oxysporum and plant growth promoter of soybean. Biodiversitas 22: 3015-3023.
  69. Nontji M, Parawansa AK, Saida, Suriyanti, Galib M, Robbo A, et al. 2023. Increasing plant health using plant growth regulator from rice rhizobacteria. Online J. Biol. Sci. 23: 50-56.
  70. Gou W, Tian L, Ruan Z, Zheng P, Chen F. 2015. Accumulation of choline and glycine betaine and drought stress tolerance induced in maize (Zea mays) by three plant growth promoting rhizobacteria (PGPR) strains. Pakistan J. Bot. 47: 581-586.
  71. Yang L, Yang K. 2020. Biological function of Klebsiella variicola and its effect on the rhizosphere soil of maize seedlings. PeerJ. 8: e9894.