Nitrogen-Fixing Purple Nonsulfur Bacteria Originating from Acid Saline Soils of a Rice-Shrimp Farm
DOI:
https://doi.org/10.32734/injar.v7i1.14726Keywords:
nitrogen-fixing bacteria, purple nonsulfur bacteria, Rhodobacter sphaeroides, rice-shrimp paddy fieldsAbstract
The study was conducted to (i) isolate, select, and identify strains of purple nonsulfur bacteria (PNSB), which can fix nitrogen (N), from soil and water in a rice-shrimp integrated system, (ii) to determine the capacity of the selected potent PNSB strains in producing plant growth promoting substances. The isolation resulted in 57 pure PNSB strains from 36 soil samples and 36 water samples of rice-shrimp paddy fields in Thanh Phu - Ben Tre. Among them, 49 strains survived under pH 5.0 conditions, 24 of which grew well under microaerobic light (ML) and aerobic dark (AD) conditions in a basic isolation medium (BIM) containing NaCl 5‰. Two strains (S01 and S06) with the greatest N fixation were identified by 16S rRNA techniques as Rhodobacter sphaeroides. Their N production was 16.9 mg L-1 under the ML condition and 32.1 mg L-1 under the AD condition. Moreover, two R. sphaeroides S01 and S06 strains performed P solubilization at 0.382-2.954 mg L-1 from Al-P, 3.81-4.28 mg L-1 from Fe-P, and 3.87-4.74 mg L-1 from Ca-P, and production of plant growth promoting substances, such as IAA (12.3-15.5 mg L-1), EPS (1.09-1.58 mg L-1), siderophores (10.7-53.6%) and ALA (1.68-2.82 mg L-1) under both the incubating conditions.
Downloads
References
N. Van Tho, "Salinity intrusion in the Vietnamese Mekong delta, a threat: possible causes, effects on people’s life and production, and temporary solutions and adaptable strategies," in Sustain. Dev. Water Environ. Proc. ICSDWE2022. Cham, Springer International Publishing, 2022, pp. 1-10, doi: 10.1007/978-3-031-07500-1_1.
M. El-Sayed and W. M. Salem, "Hydrochemical assessments of surface Nile water and ground water in an industry area–South West Cairo," Egypt. J. Pet., vol. 24, no. 3, pp. 277-288, 2015, doi: 10.1016/j.ejpe.2015.07.014.
J. Kruse, M. Koch, C. M. Khoi, G. Braun, Z. Sebesvari, and W. Amelung, "Land use change from permanent rice to alternating rice-shrimp or permanent shrimp in the coastal Mekong Delta, Vietnam: Changes in the nutrient status and binding forms," Sci. Total Environ., vol. 703, pp. 134758, 2020, doi: 10.1016/j.scitotenv.2019.134758.
L. T. H. Phan and A. Kamoshita, "Salinity intrusion reduces grain yield in coastal paddy fields: case study in two estuaries in the Red River Delta, Vietnam," Paddy Water Environ., vol. 18, pp. 399-416, 2020, doi: 10.1007/s10333-020-00790-y.
Otlewska et al., "When salt meddles between plant, soil, and microorganisms," Front. Plant Sci., vol. 11, pp. 1429, 2020, doi: 10.3389/fpls.2020.553087.
W. Taratima, T. Chomarsa, and P. Maneerattanarungroj, "Salinity stress response of rice (Oryza sativa L. cv. Luem Pua) calli and seedlings," Scientifica, vol. 2022, Art. no. 5616683, 2022, doi: 10.1155/2022/5616683.
Zheng et al., "Effect of salinity stress on rice yield and grain quality: A meta-analysis," Eur. J. Agron., vol. 144, Art. no. 126765, 2023, doi: 10.1016/j.eja.2023.126765.
F. Gonçalo Filho et al., "Reclaiming tropical saline-sodic soils with gypsum and cow manure," Water, vol. 12, no. 1, pp. 57, 2019, doi: 10.3390/w12010057.
P. Gangwar, R. Singh, M. Trivedi, and R. K. Tiwari, "Sodic soil: Management and reclamation strategies." in Environmental Concerns and Sustainable Development: Volume 2: Biodiversity, Soil and Waste Management, V. Shukla, N. Kumar, Ed., Singapore, Springer, 2020, pp. 175-190, doi: 10.1007/978-981-13-6358-0_8.
Kumar, S. Singh, A. Mukherjee, R. P. Rastogi, and J. P. Verma, "Salt-tolerant plant growth-promoting Bacillus pumilus strain JPVS11 to enhance plant growth attributes of rice and improve soil health under salinity stress," Microbiol. Res., vol. 242, Art. no. 126616, 2021, doi: 10.1016/j.micres.2020.126616.
P. Sheoran et al., "Ameliorants and salt tolerant varieties improve rice-wheat production in soils undergoing sodification with alkali water irrigation in Indo–Gangetic Plains of India," Agric. Water Manag., vol. 243, Art. no. 106492, 2021, doi: 10.1016/j.agwat.2020.106492.
M. Cerruti, "Harnessing the metabolic versatility of purple non-sulfur bacteria," PhD dissertation, Delft Univ. Technol., The Netherlands, 2022, doi: 10.4233/uuid:c98876c1-aa83-4c8d-9816-191daf5cc423.
E. Touloupakis, A. Chatziathanasiou, D. F. Ghanotakis, P. Carlozzi, and I. Pecorini, "Poly (3-hydroxybutyrate) production by Rhodopseudomonas sp. S16-VOGS3 cells grown in digested sludge," Environ. Technol. Innov., vol. 30, Art. no. 103058, 2023. doi: 10.1016/j.eti.2023.103058.
N.Q. Khuong, D. Kantachote, J. Onthong, L. N. T. Xuan, and A. Sukhoom, "Enhancement of rice growth and yield in actual acid sulfate soils by potent acid-resistant Rhodopseudomonas palustris strains for producing safe rice," Plant Soil, vol. 429, pp. 403-501, 2018, doi: 10.1007/s11104-018-3705-7.
N. Q. Khuong, D. Kantachote, P. Nookongbut, J. Onthong, L. N. T. Xuan, and A. Sukhoom, "Mechanisms of acid-resistant Rhodopseudomonas palustris strains to ameliorate acidic stress and promote plant growth," Biocatal. Agric. Biotechnol., vol. 24, Art. no. 101520, 2020, doi: 10.1016/j.bcab.2020.101520.
N.Q. Khuong et al., "Two strains of Luteovulum sphaeroides (purple nonsulfur bacteria) promote rice cultivation in saline soils by increasing available phosphorus," Rhizosphere, vol. 20, Art. no. 100456, 2021, doi: 10.1016/j.rhisph.2021.100456.
N. Q. Khuong et al., "Potential of potent purple nonsulfur bacteria isolated from rice-shrimp systems to ameliorate rice (Oryza sativa L.) growth and yield in saline acid sulfate soil," J. Plant Nutr., vol. 46, no. 3, pp. 473-494, 2023, doi: 10.1080/01904167.2022.2087089.
J. Sakpirom, D. Kantachote, T. Nunkaew, and E. Khan, "Characterizations of purple non-sulfur bacteria isolated from paddy fields, and identification of strains with potential for plant growth-promotion, greenhouse gas mitigation and heavy metal bioremediation," Res. Microbiol., vol. 168, no. 3, pp. 266-275, 2017, doi: 10.1016/j.resmic.2016.12.001.
P. Nookongbut, D. Kantachote, M. Megharaj, and R. Naidu, "Reduction in arsenic toxicity and uptake in rice (Oryza sativa L.) by As-resistant purple nonsulfur bacteria," Environ. Sci. Pollut. Res., vol. 25, pp. 36530-36544, 2018, doi: 10.1007/s11356-018-3568-8.
N. Q. Khuong et al., "Potential of Mn2+-resistant purple nonsulfur bacteria isolated from acid sulfate soils to act as bioremediators and plant growth promoters via mechanisms of resistance," J. Soil Sci. Plant Nutr., vol. 20, pp. 2364-2378, 2020, doi: 10.1007/s42729-020-00303-0.
J. Zeng et al., "Composition and aggregation of extracellular polymeric substances (EPS) in hyperhaline and municipal wastewater treatment plants," Sci. Reports, vol. 6, no. 1, Art. ID. 26721, 2016, doi: 10.1038/srep26721.
N. Q. Khuong et al., "Improvement of nutrient uptake, yield of black sesame (Sesamum indicum L.), and alluvial soil fertility in dyke by spent rice straw from mushroom cultivation as biofertilizer containing potent strains of Rhodopseudomonas palustris," Sci. World J., vol. 2023, Art. no. 1954632, 2023, doi: 10.1155/2023/1954632
L. Sparks, A. L. Page, P. A. Helmke, and R. H. Loeppert, Ed., Methods of soil analysis, part 3: Chemical methods, vol. 14, John Wiley & Sons, 2020.
J. W. Brown, Enrichment and isolation of purple non-sulfur bacteria, Raleigh: Department of Biological Sciences, College of Sciences, North Carolina State University, NC, USA, 2017.
R. S. Nelson, S. A. Ryan, and J. E. Harper, "Soybean mutants lacking constitutive nitrate reductase activity: I. Selection and initial plant characterization," Plant Physiol., vol. 72, no. 2, pp. 503-509, 1983, doi: 10.1104/pp.72.2.503.
J. A. M. E. S. Murphy and J. P. Riley, "A modified single solution method for the determination of phosphate in natural waters," Anal. Chim. Acta, vol. 27, pp. 31-36, 1962, doi: 10.1016/S0003-2670(00)88444-5.
Glickmann and Y. Dessaux, "A critical examination of the specificity of the Salkowski reagent for indolic compounds produced by phytopathogenic bacteria," Appl. Environ. Microbiol., vol. 61, no. 2, pp. 793-796, 1995, doi: 10.1128/aem.61.2.793-796.1995.
B. F. Burnham, “[14] δ-Aminolevulinic acid synthase (Rhodopseudomonas spheroides),” in Methods in enzymology, H. Tabor and C. W. Tabor, Ed., The US, Academic Press, 1970, vol. 17, pp. 195-200, doi: 10.1016/0076-6879(71)17179-0.
B. Schwyn and J. B. Neilands, "Universal chemical assay for the detection and determination of siderophores," Anal. Biochem., vol. 160, no. 1, pp. 47-56, pp. 1987, doi: 10.1016/0003-2697(87)90612-9.
K. E. Eboigbodin and C. A. Biggs, "Characterization of the extracellular polymeric substances produced by Escherichia coli using infrared spectroscopic, proteomic, and aggregation studies," Biomacromolecules, vol. 9, no. 2, pp. 686-695, 2008, doi: 10.1021/bm701043c.
Y. Suzuki, S. D. Kelly, K. M. Kemner, and J. F. Banfield, "Microbial populations stimulated for hexavalent uranium reduction in uranium mine sediment," Appl. Environ. Microbiol., vol. 69, no. 3, pp. 1337-1346, 2003, doi: 10.1128/AEM.69.3.1337-1346.2003.
T. A. Hall, “BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT,” Nucleic Acids Symp. Ser., vol 41, no. 41, pp. 95-98, 1999.
J. K. Guo et al., "Effects of EDTA and plant growth-promoting rhizobacteria on plant growth and heavy metal uptake of hyperaccumulator Sedum alfredii Hance," J. Environ. Sci., vol. 88, pp. 361-369, 2020, doi: 10.1016/j.jes.2019.10.001.
X. Cui et al., "A review on the thermal treatment of heavy metal hyperaccumulator: Fates of heavy metals and generation of products," J. Hazard. Mater., vol. 405, Art. no. 123832, 2021, doi: 10.1016/j.jhazmat.2020.123832.
S. Elnahal et al., "The use of microbial inoculants for biological control, plant growth promotion, and sustainable agriculture: A review," Eur. J. Plant Pathol, vol. 162, no. 4, pp. 759-792, 2022, doi: 10.1007/s10658-021-02393-7.
J. F. Imhoff JF, “The phototrophic alpha-proteobacteria,” in The Prokaryotes, M. Dworkin, S. Falkow, E. Rosenberg, K. H. Schleifer, and E. Stackebrandt, Ed., New York, NY, Springer, 2006, pp. 41-64, doi: 10.1007/0-387-30745-1_2.
T. Nunkaew, D. Kantachote, T. Nitoda, and H. Kanzaki, "The use of rice straw broth as an appropriate medium to isolate purple nonsulfur bacteria from paddy fields," Electron. J. Biotechnol., vol. 15, no. 6, pp. 7-7, 2012, doi: 10.2225/vol15-issue6-fulltext-8.
J. F. Imhoff JF and H. G. Truper, Bergey’s manual of determinative bacteriology, Michigan, Michigan State University, 2005.
M. T. Madigan, “Microbiology of nitrogen fixation by anoxygenic photosynthetic bacteria,” in Anoxygenic photosynthetic bacteria, R. E. Blankenship, M. T. Madigan, C. E. Bauer, Ed., Dordrecht, Springer, 1995, pp. 915-928, doi: 10.1007/0-306-47954-0_42.
M. George, A. S. Vincent, and H. R. Mackey, "An overview of anoxygenic phototrophic bacteria and their applications in environmental biotechnology for sustainable resource recovery," Biotechnol. Rep., vol. 28, Art. no. e00563, 2020, doi: 10.1016/j.btre.2020.e00563.
W. Larimer et al., "Complete genome sequence of the metabolically versatile photosynthetic bacterium Rhodopseudomonas palustris," Nat. Biotechnol., vol. 22, no. 1, pp. 55-61, 2004, doi: 10.1038/nbt923.
K. E. Luxem, A. M. L. Kraepiel, L. Zhang, J. R. Waldbauer, and X. Zhang, "Carbon substrate re‐orders relative growth of a bacterium using Mo‐, V‐, or Fe‐nitrogenase for nitrogen fixation," Environ. Microbiol., vol. 22, no. 4, pp. 1397-1408, 2020, doi: 10.1111/1462-2920.14955.
Hiraishi, "Distribution of phototrophic purple nonsulfur bacteria in massive blooms in coastal and wastewater ditch environments," Microorganisms, vol. 8, no. 2, pp. 150, 2020, doi: 10.3390/microorganisms8020150.
N. Q. Khuong, D. P. T. Minh, L. T. M. Thu, and L. V. Thuc, "The potential of bacterial strains of Luteovulum sphaeroides W22 and W47 for producing δ-aminolevulinic acid to improve soil quality, growth and yield of saline-irrigated rice cultivated in salt-contaminated soil," Agronomy, vol. 13, no. 5, pp. 1409, 2023, doi: 10.3390/agronomy13051409.
T. Nunkaew, D. Kantachote, T. Nitoda, H. Kanzaki, and R. J. Ritchie, "Characterization of exopolymeric substances from selected Rhodopseudomonas palustris strains and their ability to adsorb sodium ions," Carbohydr. Polym., vol. 115, pp. 334-341, 2015, doi: 10.1016/j.carbpol.2014.08.099.
Z. Wang et al., “Effect of salinity on extracellular polymeric substances of activated sludge from an anoxic–aerobic sequencing batch reactor,” Chemosphere, vol. 93, no. 11, pp.2789-2795, 2013, doi: 10.1016/j.chemosphere.2013.09.038.
Published
How to Cite
Issue
Section
Copyright (c) 2024 Indonesian Journal of Agricultural Research
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
