Characterization of endophytic bacteria isolated from wild rice plants in the Mekong Delta, Vietnam

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QUACH VAN CAO THI
NGUYEN LU KHOI MINH
NGUYEN PHUONG THUY
TRUONG QUOC TAT
THANH TRAN

Abstract

Abstract. Thi QVC, Minh NLK, Thuy NP, Tat TQ, Tran T. 2024. Characterization of endophytic bacteria isolated from wild rice plants in the Mekong Delta, Vietnam. Biodiversitas 25: 2576-2585. Endophytic bacteria bring many benefits to plants, such as stimulating plant growth and inhibiting many microbial pathogens that cause plant diseases. Hence, this investigation aimed to evaluate the association of endophytic bacteria with wild rice (Oryza rufipogon) that can fix nitrogen, solubilize phosphorus and produce indole-3-acetic acid (IAA). Twelve-five bacterial strains were recovered from wild rice stems and roots collected from Vinh Long and Tien Giang provinces of the Mekong Delta. Among these strains, six had phosphorus solubilizing and seven had nitrogen-fixing activity. Strain BR3.5 fixed the highest nitrogen, i.e. ammonia (NH4+) content of 0.109 ± 0.002 mg/L after eight-day incubation. However, the highest phosphorus solubilization was recorded in two isolates, RR3.7 and RR1.1, with clear zone diameters of 0.800 ± 0.020 mm and 0.800 ± 0.030 mm, respectively. In addition, bacterial strains could synthesize IAA, and BR2.5 produced the highest, i.e., 0.067 ± 0.002 ?g/mL, IAA after eight-day incubation. Notably, strain BR3.5 exhibited multiple activities like nitrogen fixation (0.109 ± 0.002 mg/L), phosphorus solubilization (1.02 ± 0.002 mm), and IAA synthesis (0.056 ± 0.00 ?g/mL). Strain BR3.5 was identified as Pantoea sp. based on 16S rRNA gene sequencing (92.69% similarity) together with morpho-physiological and biochemical characteristics. The findings indicate that strain BR3.5 may be used for the production of biofertilizers for rice farming.

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References
Aktar MW, Sengupta D, Chowdhury A. 2009. Impact of pesticides use in agriculture: their benefits and hazards. Interdiscip Toxicol 2(1): 1-12. DOI: 10.2478/v10102-009-0001-7.
Ali M, Ali Q, Sohail MA, Ashraf MF, Saleem MH, Hussain, S, Zhou L. 2021. Diversity and Taxonomic Distribution of Endophytic Bacterial Community in the Rice Plant and Its Prospective. Int J Mol Sci 22: 10165. DOI: 10.3390/ijms221810165.
Almuhayawi MS, Abdel-Mawgoud M, Al Jaouni SK, Almuhayawi SM, Alruhaili MH, Selim S, AbdElgawad H. 2021. Bacterial Endophytes as a Promising Approach to Enhance the Growth and Accumulation of Bioactive Metabolites of Three Species of Chenopodium Sprouts. Plants 10: 2745. DOI: 10.3390/plants10122745.
Ammar EE, Rady HA, Khattab AM, Amer MH, Mohamed SA, Elodamy NI, Farga AA, Aioub AA. 2023. A comprehensive overview of eco-friendly bio-fertilizers extracted from living organisms. Environ. Sci Pollut Res 30(53): 113119-113137. DOI: 10.1007/s11356-023-30260-x.
Andreote FD, Rossetto PB, Souza LC, Marcon J, Maccheroni WJr, Azevedo JL, Araújo WL. 2008. Endophytic population of Pantoea agglomerans in citrus plants and development of a cloning vector for endophytes. J Basic Microbiol 48(5): 338-46. DOI: 10.1002/jobm.200700341.
Baweja P, Kumar S, Kumar G. 2020. Fertilizers and pesticides: Their impact on soil health and environment. Soil health 265-285. DOI: 10.1007/978-3-030-44364-1_15.
Cappuccino J, Welsh C. 2017. Microbiology: A Laboratory Manual, 11th edition, Pearson Education, England.
Das SK, Das TK, Podder AK. 2021. Characterization of endophytic diazotrophic bacteria from wild rice of sundarbans for their inclusion in inm package for rice. Int J Curr Res 13(05): 17383-17386. DOI: 10.24941/ijcr.41415.05.2021.
Elbeltagy A, Nishioka K, Suzuki H, Sato T, Sato YI, Morisaki H, Mitsui H, Minamisawa K. 2000. Isolation and Characterization of Endophytic Bacteria from Wild and Traditionally Cultivated Rice Varieties. Soil Sci Plant Nutr 46: 617–629. DOI: 10.1080/00380768.2000.10409127.
Gao JL, Xue J, Yan H, Tong S, Sayyar Khan M, Wang LW, Mao XJ, Zhang X, Sun JG. 2019. Pantoea endophytica sp. nov., novel endophytic bacteria isolated from maize planting in different geographic regions of northern China. Syst Appl Microbiol 42(4): 488-494. DOI: 10.1016/j.syapm.2019.06.001.
Giang NV, Dao TT, An TTT. 2016. Isolation and Characteristics of Some Bacterial Endophytes from Root of Aloe Vera. Vietnam J Agri Sci 14(5): 772-778.
Gordon SA, Weber RP. 1951. Colorimetric estimation of indoleacetic acid. Plant Physiol 26(1): 192-195. DOI: 10.1104/pp.26.1.192.
Hai PT, Son NT, Thach NQ. 2017. Isolation and selection of endophytic bacteria capable of fixing nitrogen, degrading phosphorus, and synthesizing IAA from rice plants. Vietnam Journal of Agriculture and Rural Development 1: 28-34. DOI: 10.26459/hueunijard.v131i3B.6540.
Hao J, Zhang X, Qiu S, Song F, Lyu X, Ma Y, Peng H. 2024. Species Diversity, Nitrogen Fixation, and Nutrient Solubilization Activities of Endophytic Bacteria in Pea Embryos. Appl Sci 14: 788. DOI: 10.3390/app14020788.
Hassan E, Alikhani HA, Hosseini HM. 2015. Indole-3-acetic acid (IAA) production trait, a useful screening to select endophyte and rhizosphere competent bacteria for rice growth promoting agents. MethodsX 2(2015): 72-78. DOI: 10.1016/j.mex.2015.02.008.
Herlina L, Pukan KK, Mustikaningtyas D. 2017. The endophytic bacteria producing IAA (Indole Acetic Acid) in Arachis hypogaea. Cell Biol Dev 1: 31-35. DOI: 10.13057/cellbioldev/v010106.
Hernández I, Taulé C, Pérez-Pérez R, Battistoni F, Fabiano E, Villanueva-Guerrero A, Nápoles MC, Herrera H. 2023. Endophytic Seed-Associated Bacteria as Plant Growth Promoters of Cuban Rice (Oryza sativa L.). Microorganisms 11: 2317. DOI: 10.3390/microorganisms11092317.
Hien PH, Tuoi VT, Linh VT, Giang NV. 2021. Isolation and evaluation of biological characteristics of endophytic bacteria from roots of river mangrove. Journal of Vietnam Agricultural Science and Technology 07(128): 71-75.
Kaneko T, Minamisawa K, Isawa T, Nakatsukasa H, Mitsui H, Kawaharada Y, Nakamura Y, Watanabe A, Kawashima K, Ono A, Shimizu Y, Takahashi C, Minami C, Fujishiro T, Kohara M, Katoh M, Nakazaki N, Nakayama S, Yamada M, Tabata S, Sato S. 2010. Complete genomic structure of the cultivated rice endophyte Azospirillum sp. B510. DNA Res 17(1): 37-50. DOI: 10.1093/dnares/dsp026.
Karas MA, Wdowiak-Wróbel S, Soko?owski W. 2021. Selection of Endophytic Strains for Enhanced Bacteria-Assisted Phytoremediation of Organic Pollutants Posing a Public Health Hazard. Int J Mol Sci 22: 9557. DOI: 10.3390/ijms22179557.
Khan A, Doty SL. 2009. Characterization of bacterial endophytes of sweet potato plants. Plan Soil 322:197–207. DOI: 10.1007/s11104-009-9908-1.
Khan SS, Verma V, Rasool S. 2020. Diversity and the role of endophytic bacteria: a review. Botanica Serbica 44(2), 103-120. DOI: 10.2298/BOTSERB2002103K.
Khianngam S, Meetum P, Chiangmai PN, Tanasupawat S. 2023. Identification and Optimisation of Indole-3-Acetic Acid Production of Endophytic Bacteria and Their Effects on Plant Growth. Trop Life Sci Res 34(1): 219-239. DOI: 10.21315/tlsr2023.34.1.12.
Kirui CK, Njeru EM, Runo S. 2022. Diversity and Phosphate Solubilization Efficiency of Phosphate Solubilizing Bacteria Isolated from Semi-Arid Agroecosystems of Eastern Kenya. Microbiol Insights 15: 11786361221088991. DOI:10.1177/11786361221088991.
Kong P, Hong C. 2020. Endophytic Burkholderia sp. SSG as a potential biofertilizer promoting boxwood growth. PeerJ 8: e9547. DOI: 10.7717/peerj.9547.
Loiret FG, Ortega E, Kleiner D, Ortega-Rodés P, Rodés R, Dong Z. 2004. A putative new endophytic nitrogen-fixing bacterium Pantoea sp. from sugarcane. J Appl Microbiol 97(3): 504-11. doi: 10.1111/j.1365-2672.2004.02329.x.
Lu L, Chang M, Han X, Wang Q, Wang J, Yang H, Guan Q, Dai S. 2021. Beneficial effects of endophytic Pantoea ananatis with ability to promote rice growth under saline stress. J Appl Microbiol 131(4): 1919-1931. DOI: 10.1111/jam.15082.
Luynh NHN, Hiep NH. 2019. Selection of nitrogen fixing, phosphate solubilizing and IAA synthesizing bacterial endophytes in Coffea canephora Pierre ex A. Froehner grown in Dak Lak province. CTU Journal of Science (2): 34-40. DOI: 10.22144/ctu.jsi.2019.041.
Ma Q, He S, Wang X, Rengel Z, Chen L, Wang X, Pei S, Xin X, Zhang X. 2023. Isolation and characterization of phosphate-solubilizing bacterium Pantoea rhizosphaerae sp. nov. from Acer truncatum rhizosphere soil and its effect on Acer truncatum growth. Front Plant Sci 14:1218445. DOI: 10.3389/fpls.2023.1218445.
Majda M, Robert S. 2018. The Role of Auxin in Cell Wall Expansion. Int J Mol Sci 19(4): 951. DOI: 10.3390/ijms19040951.
Mano H, Morisaki H. 2008. Endophytic bacteria in the rice plant. Microbes Environ 23(2): 109-17. DOI: 10.1264/jsme2.23.109.
Mei C, Chretien RL, Amaradasa BS, He Y, Turner A, Lowman S. 2021. Characterization of Phosphate Solubilizing Bacterial Endophytes and Plant Growth Promotion In Vitro and in Greenhouse. Microorganisms 9: 1935. DOI: 10.3390/microorganisms9091935.
Melini F, Luziatelli F, Bonini P, Ficca AG, Melini V, Ruzzi M. 2023. Optimization of the growth conditions through response surface methodology and metabolomics for maximizing the auxin production by Pantoea agglomerans C1. Front Microbiol 14: 1022248. DOI: 10.3389/fmicb.2023.1022248.
Mugiastuti E, Suprayogi, Prihatiningsih N, Soesanto L. 2020. Isolation and characterization of the endophytic bacteria, and their potential as maize disease control. Biodiversitas 21(5): 1809-1815. DOI: 10.13057/biodiv/d210506.
Nautiyal CS. (1999). An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiology Letters 170(1): 265-270. DOI: 10.1111/j.1574-6968.1999.tb13383.x.
Nhu VTP, Diep CN. 2014b. Effects of Azospirillum amazonense and Burkholderia kururiensison high-yielding Rice (cv. Ma Lam 213) cultivated on Sandy Loam soil of Tuy Hoa City, Phu Yen Province. CTU Journal of Science 33(2014): 85-96. DOI: 10.11648/j.jps.20140206.20
Nhu VTP, Diep CN. 2014. Isolation, Charcaterization and Phylogenetic Analysis of Endophytic Bacteria in Rice Plant Cultivated on Soil of Phu Yen Province, Vietnam. Am J Life Sci 2(3): 117-127. DOI: 10.11648/j.ajls.20140203.11.
Olanrewaju OS, Glick BR, Babalola OO. 2017. Mechanisms of action of plant growth promoting bacteria. World J Microbiol Biotechnol 33: 197. DOI: 10.1007/s11274-017-2364-9.
Oteino N, Lally RD, Kiwanuka S, Lloyd A, Ryan D, Germaine KJ, Dowling DN. 2015. Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates. Front Microbiol 6: 745. DOI: 10.3389/fmicb.2015.00745.
Pal G, Saxena S, Kumar K, Verma A, Sahu PK, Pandey A, White JF, Verma SK. 2022. Endophytic Burkholderia: Multifunctional roles in plant growth promotion and stress tolerance. Microbiol Res 265: 127201. DOI: 10.1016/j.micres.2022.127201.
Pande A, Pandey P, Mehra S, Singh M, Kaushik S. 2017. Phenotypic and genotypic characterization of phosphate solubilizing bacteria and their efficiency on the growth of maize. J Genet Eng Biotechnol 15(2): 379-391. DOI: 10.1016/j.jgeb.2017.06.005.
Park M, Kim C, Yang J, Lee H, Shin W, Kim S, Sa T. 2005. Isolation and characterization of diazotrophic growth promoting bacteria from rhizosphere of agricultural crops of Korea. Microbiological Research 160: 127-133. DOI: 10.1016/j.micres.2004.10.003.
Parveen S, Mohiddin FA, Bhat MA, Baba ZA, Jeelani F, Bhat MA, El Sabagh A. 2023. Characterization of Endophytic Microorganisms of Rice (Oryza sativa L.) Potentials for Blast Disease Biocontrol and Plant Growth Promoting Agents. Phyton-Int J Exp Bot 92(11): 3021-3041. DOI: 10.32604/phyton.2023.030921.
Pathak R, Paudel V, Shrestha A, Lamichhane J, Gauchan DP. 2018. Isolation of phosphate solubilizing bacteria and their use for plant growth promotion in tomato seedling and Plant. Kathmandu Univ J Sci Eng Technol 13: 61-70. DOI: 10.3126/kuset.v13i2.21284.
Paul D, Sinha SN. 2016. Isolation and characterization of phosphate solubilizing bacterium
Pseudomonas aeruginosa KUPSB12 with antibacterial potential from river Ganga, India. Ann Agrar Sci 15: 130–6. DOI: 10.1016/j.aasci.2016.10.001.
Prodhan MY, Rahman MB, Rahman A, Akbor MA, Ghosh S, Nahar MN-E-N, Simo, Shamsuzzoha M, Cho KM, Haque MA. 2023. Characterization of Growth-Promoting Activities of Consortia of Chlorpyrifos Mineralizing Endophytic Bacteria Naturally Harboring in Rice Plants—A Potential Bio-Stimulant to Develop a Safe and Sustainable Agriculture. Microorganisms 11: 1821. DOI: 10.3390/microorganisms11071821.
Quecine MC, Araújo WL, Rossetto PB, Ferreira A, Tsui S, Lacava PT, Mondin M, Azevedo JL, Pizzirani-Kleiner AA. 2012. Sugarcane growth promotion by the endophytic bacterium Pantoea agglomerans 33.1. Appl Environ Microbiol 78(21): 7511-8. DOI: 10.1128/AEM.00836-12.
Rangjaroen C, Rerkasem B, Teaumroong N, Noisangiam R, Lumyong S. 2015. Promoting plant growth in a commercial rice cultivar by endophytic diazotrophic bacteria isolated from rice landraces. Annals of microbiology 65: 253-266. DOI 10.1007/s13213-014-0857-4
Sambrook J, Fritsch EF, Maniatis T. 1989. Molecu-lar Cloning: A Laboratory Manual.Cold Spring Harbor, NY, Cold Spring Harbor Laboratory Press 11: 31.
Singh P, Singh RK, Li H-B, Guo D-J, Sharma A, Lakshmanan P, Malviya MK, Song X-P, Solanki MK, Verma KK, Yang L-T, Li Y-R. 2021. Diazotrophic Bacteria Pantoea dispersa and Enterobacter asburiae Promote Sugarcane Growth by Inducing Nitrogen Uptake and Defense-Related Gene Expression. Front Microbiol 11: 600417. DOI: 10.3389/fmicb.2020.600417.
Singh RK, Singh P, Guo D-J, Sharma A, Li D-P, Li X, Verma KK, Malviya MK, Song X-P, Lakshmanan P, Yang L-T, Li Y-R. 2021. Root-Derived Endophytic Diazotrophic Bacteria Pantoea cypripedii AF1 and Kosakonia arachidis EF1 Promote Nitrogen Assimilation and Growth in Sugarcane. Front Microbiol 12: 774707. DOI: 10.3389/fmicb.2021.774707.
Solarzano L. 1969. Determination of ammonia in natural waters by the phenol hypochlorite methods. Limnol Oceanogr 14(5):799-801. DOI: 10.4319/lo.1969.14.5.0799.
Sudewi S, Ala A, Patandjengi B, M Farid BDR. 2020. Isolation of phosphate solubilizing bacteria from the rhizosphere of local aromatic rice in Bada Valley Central Sulawesi, Indonesia. In IOP Conference Series: Earth and Environmental Science 575(1): 012017. DOI: 10.1088/1755-1315/575/1/012017.
Suleimanova A, Bulmakova D, Sokolnikova L, Egorova E, Itkina D, Kuzminova O, Gizatullina A, Sharipova M. 2023. Phosphate Solubilization and Plant Growth Promotion by Pantoea brenneri Soil Isolates. Microorganisms 11(5) :1136. DOI: 10.3390/microorganisms11051136.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol Biol Evol 30(12): 725-2729. DOI: 10.1093/molbev/mst197.
Thanh DTN, My NTX, Diep C N. 2016. Indole acetic acid and siderophore production by selected isolates of plant associated bacteria and their effects on growth of maize (Zea mays L.) in pot experiments. CTU Journal of Science 47:59-67. DOI: 10.22144/ctu.jvn.2016.601.
Thuy HTN, Nhat ND, Ly NNC, Hai TM, Phuong TTX. 2022. Isolation and selection of endophytic bacteria strains on rice in Thua Thien Hue. HUAF Journal of Agricultural Science and Technology 6(1): 2859-2870.
Thuy DTB. 2021. Vietnam’s rice exports: opportunities and challenges. https://vioit.org.vn/en/strategy-policy/vietnam-s-rice-exports--opportunities-and-challenges-4404.4144.html (Accessed on May 7, 2024).
Trang NT, Ha TTT, Truong NX, Giang NV. 2018. Isolation and characterization of endophytic bacteria from roots of black pepper. Journal of Vietnam Agricultural Science and Technology 95 (10): 85-90.
Verma SK, Sahu PK, Kumar K, Pal G, Gond SK, Kharwar RN, White JF. 2021. Endophyte roles in nutrient acquisition, root system architecture development and oxidative stress tolerance. J Appl Microbiol 131(5): 2161-2177. DOI: 10.1111/jam.15111.
Walitang DI, Roy Choudhury A, Lee Y, Choi G, Jeong B, Jamal AR, Sa T. 2023. The Endophytic Plant Growth Promoting Methylobacterium oryzae CBMB20 Integrates and Persists into the Seed-Borne Endophytic Bacterial Community of Rice. Agriculture 13: 355. DOI: 10.3390/agriculture13020355.
Walpola BC, Kong WS, Yoon MH. 2013. Solubilization of inorganic phosphates and plant growth promotion by Pantoea strains. Korean J. Soil Sci Fert 46: 494-501. DOI: 10.7745/KJSSF.2013.46.6.494.
Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 1991. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173(2): 697-703. DOI: 10.1128/jb.173.2.697-703.1991.
Xuan LNT, Dung TV, Hung NN, Diep CN. 2016. Isolation and characterization of rice endophytic bacteria in acid sulphate soil of Mekong delta, Vietnam. World J Pharm Pharm Sci 5: 301-317. DOI: 10.20959/wjpps20168-7462.
Zhang Q, Gong M, Xu X, Li H, Deng W. 2022. Roles of Auxin in the Growth, Development, and Stress Tolerance of Horticultural Plants. Cells 11(17): 2761. DOI: 10.3390/cells11172761.

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