Abstract
Arsenic (As) contamination is a major problem affecting soil and groundwater in India, harming agricultural crops and human health. Plant growth-promoting rhizobacteria (PGPR) have emerged as promising agents for reducing As toxicity in plants. This study aimed to isolate and characterize As-tolerant PGPR from rice field soils with varying As levels in five districts of West Bengal, India. A total of 663 bacterial isolates were obtained from the different soil samples, and 10 bacterial strains were selected based on their arsenite (As-III) and arsenate (As-V) tolerant ability and multiple PGP traits, including phosphate solubilization, production of siderophore, indole acetic acid, biofilm formation, alginate, and exopolysaccharide. These isolates were identified by 16S rRNA gene sequencing analysis as Staphylococcus sp. (4), Niallia sp. (2), Priestia sp. (1), Bacillus sp. (1), Pseudomonas sp. (1), and Citricoccus sp. (1). Among the selected bacterial strains, Priestia flexa NBRI4As1 and Pseudomonas chengduensis NBRI12As1 demonstrated significant improvement in rice growth by alleviating arsenic stress under greenhouse conditions. Both strains were also able to modulate photosynthetic pigments, soluble sugar content, proline concentration, and defense enzyme activity. Reduction in As-V accumulation inoculated with NBRI4As1 was recorded highest by 53.02% and 31.48%, while As-III by NBRI12As1 38.84% and 35.98% in the roots and shoots of rice plants, respectively. Overall, this study can lead to developing efficient As-tolerant bacterial strains–based bioinoculant application packages for arsenic stress management in rice.
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References
Abedin MJ, Cresser MS, Meharg AA, Feldmann J, Cotter-Howells J (2002) Arsenic accumulation and metabolism in rice (Oryza sativa L.) Environ Sci Technol 36:962–968
Aebi HI (1984) Purification, characterization, and assay of antioxygenic enzymes: catalase in vitro. Methods Enzymol 105:121–126
Ahmad S, Cui W, Kamran M, Ahmad I, Meng X, Wu X, Han Q (2021) Exogenous application of melatonin induces tolerance to salt stress by improving the photosynthetic efficiency and antioxidant defense system of maize seedling. J Plant Growth Regul 40:1270–1283. https://doi.org/10.1007/s00344-020-10187-0
Ahmed SF, Kumar PS, Rozbu MR, Chowdhury AT, Nuzhat S, Rafa N (2022) Heavy metal toxicity, sources, and remediation techniques for contaminated water and soil. Environ Technol Innov 25:102114. https://doi.org/10.1016/j.eti.2021.102114
Ali S, Tyagi A, Mushtaq M, Al-Mahmoudi H, Bae H (2022) Harnessing plant microbiome for mitigating arsenic toxicity in sustainable agriculture. Environ Pollut. https://doi.org/10.1016/j.envpol.2022.118940
Alka S, Shahir S, Ibrahim N, Chai TT, Bahari ZM, Abd Manan F (2020) The role of plant growth promoting bacteria on arsenic removal: a review of existing perspectives. Environ Technol Innov. https://doi.org/10.1016/j.eti.2020.100602
Anand V, Kaur J, Srivastava S, Bist V, Dharmesh V, Kriti K, Srivastava S (2023) Potential of methyltransferase containing Pseudomonas oleovorans for abatement of arsenic toxicity in rice. Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2022.158944
Awasthi S, Chauhan R, Dwivedi S, Srivastava S, Srivastava S, Tripathi RD (2018) A consortium of alga (Chlorella vulgaris) and bacterium (Pseudomonas putida) for amelioration of arsenic toxicity in rice: a promising and feasible approach. Environ Exp Bot 150:115–126. https://doi.org/10.1016/j.envexpbot.2018.03.001
Bali AS, Sidhu GPS (2021) Arsenic acquisition, toxicity and tolerance in plants-From physiology to remediation: a review. Chemosphere 283:131050. https://doi.org/10.1016/j.chemosphere.2021.131050
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44(1):276–287. https://doi.org/10.1016/0003-2697(71)90370-8
Bhat JA, Shivaraj SM, Singh P, Navadagi DB, Tripathi DK, Dash PK, Deshmukh R (2019) Role of silicon in mitigation of heavy metal stresses in crop plants. Plants. https://doi.org/10.3390/plants8030071
Bisht N, Chauhan PS (2020) Comparing the growth-promoting potential of Paenibacillus lentimorbus and Bacillus amyloliquefaciens in Oryza sativa L. var. Sarju-52 under suboptimal nutrient conditions. Plant Physiol Biochem 146:187–197. https://doi.org/10.1016/j.plaphy.2019.11.023
Bist V, Anand V, Srivastava S, Kaur J, Naseem M, Mishra S, Srivastava S (2022) Alleviative mechanisms of silicon solubilizing Bacillus amyloliquefaciens mediated diminution of arsenic toxicity in rice. J Hazard Mater. https://doi.org/10.1016/j.jhazmat.2021.128170
Biswas JK, Warke M, Datta R, Sarkar D (2020) Is arsenic in rice a major human health concern. Curr Pollut Rep 6:37–42. https://doi.org/10.1007/s40726-020-00148-2
Bric JM, Bostock RM, Silverstone SE (1991) Rapid in situ assay for indoleacetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl Environ Microbiol 57(2):535–538. https://doi.org/10.1128/aem.57.2.535-538.1991
Butt AS, Rehman A (2011) Isolation of arsenite-oxidizing bacteria from industrial effluents and their potential use in wastewater treatment. World J Microbiol Biotechnol 27:2435–2441
Cavalca L, Zanchi R, Corsini A, Colombo M, Romagnoli C, Canzi E, Andreoni V (2010) Arsenic-resistant bacteria associated with roots of the wild Cirsium arvense (L.) plant from an arsenic polluted soil, and screening of potential plant growth-promoting characteristics. Syst Appl Microbiol 33(3):154–164. https://doi.org/10.1016/j.syapm.2010.02.004
Chandrakar V, Naithani SC, Keshavkant S (2016) Arsenic-induced metabolic disturbances and their mitigation mechanisms in crop plants: a review. Biologia 71(4):367–377. https://doi.org/10.1515/biolog-2016-0052
Chauhan R, Awasthi S, Tripathi P, Mishra S, Dwiedi S, Niranjan A, Mallick S, Tripathi P, Pande V, Tripathi RD (2017) Selenite modulates the level of phenolics and nutrient elements to alleviate the toxicity of arsenite in rice (Oryza: saliva L). Ecotoxicol Environ Saf 138:47–55. https://doi.org/10.1016/j.ecoenv.2016.11.015
Chauhan PS, Mishra SK, Misra S, Dixit VK, Pandey S, Khare P, Lehri A (2018) Evaluation of fertility indicators associated with arsenic-contaminated paddy fields soil. Int J Environ Sci Technol 15:2447–2458
Das I, Sanyal SK, Ghosh K (2018) Environmental chemistry, fate and speciation of arsenic in groundwater-soil-crop systems. Mechanisms of Arsenic Toxicity and Tolerance in Plants
Dhuldhaj UP, Yadav IC, Singh S, Sharma NK (2012) Microbial interactions in the arsenic cycle: adoptive strategies and applications in environmental management. Rev Environ Contam Toxicol 224:1–38. https://doi.org/10.1007/978-1-4614-5882-1_1
Diep P, Mahadevan R, Yakunin AF (2018) Heavy metal removal by bioaccumulation using genetically engineered microorganisms. Front Bioeng Biotechnol. https://doi.org/10.3389/fbioe.2018.00157
Dixit VK, Misra S, Mishra SK, Tewari SK, Joshi N, Chauhan PS (2020) Characterization of plant growth-promoting alkalotolerant Alcaligenes and Bacillus strains for mitigating the alkaline stress in Zea mays. Anton Leeuw Int J 113:889–905
Drewniak L, Styczek A, Majder-Lopatka M, Sklodowska A (2008) Bacteria, hypertolerant to arsenic in the rocks of an ancient gold mine, and their potential role in dissemination of arsenic pollution. Environ Pollut 156(3):1069–1074. https://doi.org/10.1016/j.envpol.2008.04.019
Dwivedi S, Kumar A, Mishra S, Sharma P, Sinam G, Bahadur L, Goyal V, Jain N, Tripathi RD (2020) Orthosilic1c acid (OSA) reduced grain arsenic accumulation and enhanced yield by modulating the level of trace element, antioxidants, and thiols in rice. Environ Sci Pollut Res 27:24025–24038 https://www.researchgate.net/publication/340998390
Etesami H, Maheshwari DK (2018) Use of plant growth promoting rhizobacteria (PGPRs) with multiple plant growth promoting traits in stress agriculture: action mechanisms and future prospects. Ecotoxicol Environ Saf 156:225–246. https://doi.org/10.1016/j.ecoenv.2018.03.013
Hamza M, Alam S, Rizwan M, Naz A (2022) Health risks associated with arsenic contamination and its biotransformation mechanisms in environment: a review. Hazardous Environmental Micro-pollutants, Health Impacts and Allied Treatment Technologies
Hare V, Chowdhary P, Baghel VS (2017) Influence of bacterial strains on Oryza sativa grown under arsenic tainted soil: accumulation and detoxification response. Plant Physiol Biochem 119:93–102. https://doi.org/10.1016/j.plaphy.2017.08.021
Hemeda HM, Klein BP (1990) Efects of naturally occurring antioxidants on peroxidase activity of vegetable extracts. J Food Sci 55:184–185. https://doi.org/10.1111/j.1365-2621.1990.tb06048.x
Islam MS, Kormoker T, Idris AM, Proshad R, Kabir MH, Ustaoğlu F (2021) Plant–microbe–metal interactions for heavy metal bioremediation: a review. Crop Pasture Sci. https://doi.org/10.1071/CP21322
Jackson CR, Dugas SL, Harrison KG (2005) Enumeration and characterization of arsenate-resistant bacteria in arsenic free soils. Soil Biol Biochem 3712:2319–2322. https://doi.org/10.1016/j.soilbio.2005.04.010
Joshi H, Mishra SK, Prasad V, Chauhan PS (2023) Bacillus amyloliquefaciens modulate sugar metabolism to mitigate arsenic toxicity in Oryza sativa L. var Saryu-52. Chemosphere. https://doi.org/10.1016/j.chemosphere.2022.137070
Kaur J, Anand V, Srivastava S, Bist V, Tripathi P, Naseem M, Srivastava S (2020) Yeast strain Debaryomyces hansenii for amelioration of arsenic stress in rice. Ecotoxicol Environ Saf. https://doi.org/10.1016/j.ecoenv.2020.110480
Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:112–120
Kofroňová M, Hrdinová A, Mašková P, Soudek P, Tremlová J, Pinkas D, Lipavská H (2019) Strong antioxidant capacity of horseradish hairy root cultures under arsenic stress indicates the possible use of Armoracia rusticana plants for phytoremediation. Ecotoxicol Environ Saf 174:295–304. https://doi.org/10.1016/j.ecoenv.2019.02.028
Maghsoudi K, Arvin MJ, Ashraf M (2020) Mitigation of arsenic toxicity in wheat by the exogenously applied salicylic acid, 24-epi-brassinolide and silicon. J Soil Sci Plant Nutr 20:577–588
Mandal D, Sonar R, Saha I, Ahmed S, Basu A (2021) Isolation and identification of arsenic resistant bacteria: a tool for bioremediation of arsenic toxicity. Int J Environ Sci Technol. https://doi.org/10.1007/s13762-021-03673-9
Marwa N, Mishra N, Singh N, Mishra A, Saxena G, Pandey V, Singh N (2020) Effect of rhizospheric inoculation of isolated arsenic (As) tolerant strains on growth, As-uptake and bacterial communities in association with Adiantum capillus-veneris. Ecotoxicol Environ Saf. https://doi.org/10.1016/j.ecoenv.2020.110498
Mayer C, Muras A, Parga A, Romero M, Rumbo-Feal S, Poza M, Otero A (2020) Quorum sensing as a target for controlling surface associated motility and biofilm formation in Acinetobacter baumannii ATCC® 17978TM. Front Microbiol 11:565548
Meyer JA, Abdallah MA (1978) The fluorescent pigment of Pseudomonas fluorescens: biosynthesis, purification and physicochemical properties. Microbiology 10(2):319–328. https://doi.org/10.1099/00221287-107-2-319
Mishra SK, Khan MH, Misra S, Dixit VK, Khare P, Srivastava S, Chauhan PS (2017) Characterisation of Pseudomonas spp. and Ochrobactrum sp. isolated from volcanic soil. Anton Leeuw Int J 110:253–270
Mohsin H, Shafique M, Rehman Y (2021) Genes and biochemical pathways involved in microbial transformation of arsenic. In: Kumar N (ed) Arsenic toxicity: challenges and solutions. Springer, Singapore. https://doi.org/10.1007/978-981-33-6068-6_15
Moradi Pour M, Saberi Riseh R, Ranjbar-Karimi R, Hassanisaadi M, Rahdar A, Baino F (2022) Microencapsulation of Bacillus velezensis using alginate-gum polymers enriched with TiO2 and SiO2 nanoparticles. Micromachines 13(9):1423
Moulick D, Samanta S, Sarkar S, Mukherjee A, Pattnaik BK, Saha S, Santra SC (2021) Arsenic contamination, impact and mitigation strategies in rice agro-environment: an inclusive insight. Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2021.149477
Muleta D, Assefa F, Börjesson E, Granhall U (2013) Phosphate-solubilising rhizobacteria associated with Coffea arabica L. in natural coffee forests of southwestern Ethiopia. J Saudi Soc Agric Sci 12(1):73–84. https://doi.org/10.1016/j.jssas.2012.07.002
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specifc peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Nath A, Samanta S, Banerjee S, Danda AA, Hazra S (2021) Threat of arsenic contamination, salinity and water pollution in agricultural practices of Sundarban Delta, India, and mitigation strategies. N Appl Sci 3:1–15. https://doi.org/10.1007/s42452-021-04544-1
Nautiyal CS (1997) Rhizosphere competence of Pseudomonas sp. NBRI9926 and Rhizobium sp. NBRI9513 involved in the suppression of chickpea (Cicer arietinum L.) pathogenic fungi. FEMS Microbiol Lett 23(2):145–158. https://doi.org/10.1111/j.1574-6941.1997.tb00398.x
Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170(1):265–270. https://doi.org/10.1111/j.1574-6968.1999.tb13383.x
Nautiyal CS, Srivastava S, Chauhan PS, Seem K, Mishra A, Sopory SK (2013) Plant growth-promoting bacteria Bacillus amyloliquefaciens NBRISN13 modulates gene expression profile of leaf and rhizosphere community in rice during salt stress. Plant Physiol Biochem. https://doi.org/10.1016/j.plaphy.2013.01.020
Naveed S, Li C, Lu X, Chen S, Yin B, Zhang C, Ge Y (2019) Microalgal extracellular polymeric substances and their interactions with metal (loid) s: a review. Crit Rev Environ Sci Technol 49(19):1769–1802. https://doi.org/10.1080/10643389.2019.1583052
Park JH, Bolan N, Megharaj M, Naidu R (2011) Isolation of phosphate solubilizing bacteria and their potential for lead immobilization in soil. J Hazard Mater 185(2-3):829–836. https://doi.org/10.1016/j.jhazmat.2010.09.095
Patra H, Mishra D (1979) Pyrophosphatase, peroxidase and polyphenoloxidase activities during leaf development and senescence. Plant Physiol 63(2):318–323. https://doi.org/10.1104/pp.63.2.318
Roychowdhury T, Uchino T, Tokunaga H, Ando M (2002) Arsenic and other heavy metals in soils from an arsenic-affected area of West Bengal, India. Chemosphere 49(6):605–618. https://doi.org/10.1016/S0045-6535(02)00309-0
Saberi Riseh R, Skorik YA, Thakur VK, Moradi Pour M, Tamanadar E, Noghabi SS (2021a) Encapsulation of plant biocontrol bacteria with alginate as a main polymer material. Int J Mol Sci 22(20):11165
Saberi Riseh R, Ebrahimi-Zarandi M, Tamanadar E, Moradi Pour M, Thakur VK (2021b) Salinity stress: toward sustainable plant strategies and using plant growth-promoting rhizobacteria encapsulation for reducing it. Sustainability 13(22):12758
Saberi Riseh R, Ebrahimi-Zarandi M, Gholizadeh Vazvani M, Skorik YA (2021c) Reducing drought stress in plants by encapsulating plant growth-promoting bacteria with polysaccharides. Int J Mol Sci 22(23):12979
Saberi Riseh R, Moradi Pour M, Ait Barka E (2022) A Novel route for double-layered encapsulation of Streptomyces fulvissimus Uts22 by alginate–Arabic gum for controlling of Pythium aphanidermatum in Cucumber. Agronomy 12(3):655
Sandalio LM, Rodríguez-Serrano M, del Río LA, Romero-Puertas M (2009) Reactive oxygen species and signaling in cadmium toxicity. In: Rio L, Puppo A (eds) Reactive oxygen species in plant signaling. Signaling and communication in plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-00390-5_11
Semwal P, Misra S, Misra A, Kar S, Majhi B, Mishra SK, Chauhan PS (2023) Endophytic Bacillus strains enhance biomass and bioactive metabolites of Gloriosa superba. Ind Crop Prod 204:117296. https://doi.org/10.1016/j.indcrop.2023.117296
Sharma A, Kumar V, Shahzad B, Ramakrishnan M, Singh SGP, Bali AS, Zheng B (2020) Photosynthetic response of plants under different abiotic stresses: a review. J Plant Growth Regul 39:509–531. https://doi.org/10.1007/s00344-019-10018-x
Sher S, Rehman A (2019) Use of heavy metals resistant bacteria: a strategy for arsenic bioremediation. Appl Microbiol Biotechnol 103:6007–6021. https://doi.org/10.1007/s00253-019-09933-6
Sil P, Das P, Biswas S, Mazumdar A, Biswas AK (2019) Modulation of photosynthetic parameters, sugar metabolism, polyamine and ion contents by silicon amendments in wheat (Triticum aestivum L.) seedlings exposed to arsenic. Environ Sci Pollut Res 26:13630–13648. https://doi.org/10.1007/s11356-019-04896-7
Singh N, Srivastava S, Rathaur S, Singh N (2016) Assessing the bioremediation potential of arsenic tolerant bacterial strains in rice rhizosphere interface. J Environ Sci 48:112–119. https://doi.org/10.1016/j.jes.2015.12.034
Srivastava S, Yadav A, Seem K, Mishra S, Chaudhary V, Nautiyal CS (2008) Effect of high temperature on Pseudomonas putida NBRI0987 biofilm formation and expression of stress sigma factor RpoS. Curr Microbiol 56:453–457
Titus S, Gasnkar N, Srivastava KB, Karande AA (1995) Exopolymer production by a fouling marine bacterium Pseudomonas alcaligenes. Indian J Mar Sci 24:45–48
Upadhyay MK, Majumdar A, Barla A, Bose S, Srivastava S (2019) An assessment of arsenic hazard in groundwater–soil–rice system in two villages of Nadia district, West Bengal, India. Environ Geochem Health 41:2381–2395
Vuppula RR, Tirumkudulu MS, Venkatesh KV (2010) Chemotaxis of Escherichia coli to L-serine. Phys Biol 7(2):026007 http://iopscience.iop.org/1478-3975/7/2/026007
Wang Y, Yuan JH, Chen H, Zhao X, Wang D, Wang SQ, Ding SM (2019) Small-scale interaction of iron and phosphorus in flooded soils with rice growth. Sci Total Environ 669:911–919. https://doi.org/10.1016/j.scitotenv.2019.03.054
Acknowledgements
The authors are thankful to the Director, CSIR-NBRI, Lucknow, for providing the necessary resources to conduct this study. CSIR-NBRI allotted the manuscript number CSIR-NBRI_MS/2023/10/22.
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The study was financially supported by the In-house project OLP116 funded by the Council of Scientific and Industrial Research, New Delhi, India. Basudev Majhi is grateful for the scholarship he received from CSIR, New Delhi, India.
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Basudev Majhi: methodology, writing—original draft, investigation. Pradeep Semwal: writing—review and editing, formal analysis. Shashank Kumar Mishra: methodology, investigation, validation. Sankalp Misra: validation, visualization. Puneet Singh Chauhan: conceptualization, supervision, funding acquisition.
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Majhi, B., Semwal, P., Mishra, S.K. et al. Arsenic stress management through arsenite and arsenate-tolerant growth-promoting bacteria in rice. Int Microbiol (2023). https://doi.org/10.1007/s10123-023-00447-w
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DOI: https://doi.org/10.1007/s10123-023-00447-w