Abstract
Low-cost microbial remediation strategies serve as a viable and potent weapon for curbing the arsenic menace. In the present study, two arsenic-resistant bacteria were isolated from the contaminated lentil rhizosphere in Gangetic plain of eastern India. LAR-21 (Burkholderia cepacia, MW356875) and LAR-25 (Burkholderia cenocepacia, MW356894) could remove 87.6% and 85.9% of arsenite (10 mM) from the liquid culture medium in laboratory condition. They were highly resistant to arsenate and arsenite and also had a high arsenite oxidase activity. LAR-21 showed the highest level of minimum inhibitory concentration value of 390 mM for arsenate and 31 mM for arsenite. The same strain was found to show highest arsenite oxidase activity, i.e., 5.2 nM min−1 mg−1of protein. These two strains further possess potential plant growth-promoting characteristics like indole acetic acid production (5–15 mM IAA mL−1), 1-aminocyclopropane-1-carboxylate deaminase (8–21 nM α-keto butyrate mg protein−1 h−1), nitrogenase activity (3–8.99 nM ethylene mg cell protein−1 h−1), siderophore production (17–22.1 µM deferoxamine mesylate mL−1), phosphate solubilization (261–453 µg mL−1) under arsenic stress condition. The plant growth promotion of the strains was further validated by pot study of lentil by assessing their agronomic and growth-related traits, and potential to recover from arsenic stress (17.2–21.2% arsenic reduction in root and shoot, 16–19.2% in leaf and pod, and 15–23% reduction in seeds). The LAR-21 strain, thus, emerged as the most suited candidate for bioremediation and plant (lentil) growth promotion in arsenic polluted environment.
Similar content being viewed by others
References
Armendariz AL, Talano MA, Nicotra MFO, Escudero L, Breser ML, Porporatto C, Agostini E (2019) Impact of double inoculation with Bradyrhizobium japonicum E109 and Azospirillum brasilense Az39 on soybean plants grown under arsenic stress. Plant Physiol Biochem 138:26–35
B’hymer C, Caruso JA (2004) Arsenic and its speciation analysis using high-performance liquid chromatography and inductively coupled plasma mass spectrometry. J Chromatogr A 1045(1–2):1–13
Bhattacharyya K, Sengupta S, Pari A, Halder S, Bhattacharya P, Pandian BJ, Chinchmalatpure AR (2021a) Characterization and risk assessment of arsenic contamination in soil–plant (vegetable) system and its mitigation through water harvesting and organic amendment. Environ Geochem Health 43:2819–2834
Bhattacharyya K, Sengupta S, Pari A, Halder S, Bhattacharya P, Pandian BJ, Chinchmalatpure AR (2021b) Assessing the human risk to arsenic through dietary exposure-a case study from West Bengal, India. J Environ Biol 42:353–365
Bhattacharyya K, Sengupta S (2020). Arsenic management options in soil–plant–food chain. In: Prasad Bishun D, Mandal Jajati, Kumar Sunil, Sohane RK (eds) Proceedings of the National Webinar On Arsenic Mitigation: A Nexus approach, pp 17–23. ISBN 978-93-5407-684-8
Biswas JK, Mondal M, Rinklebe J, Sarkar SK, Chaudhuri P, Rai M, Shaheen SM, Song H, Rizwan M (2017) Multi-metal resistance and plant growth promotion potential of a wastewater bacterium Pseudomonas aeruginosa and its synergistic benefits. Environ Geochem Health 39(6):1583–1593
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
Chiboub M, Saadani O, Fatnassi IC, Abdelkrim S, Abid G, Jebara M, Jebara SH (2016) Characterization of efficient plant-growth-promoting bacteria isolated from Sulla coronaria resistant to cadmium and to other heavy metals. C R Biol 339(9–10):391–398
Das J, Sarkar P (2018) Remediation of arsenic in mung bean (Vigna radiata) with growth enhancement by unique arsenic-resistant bacterium Acinetobacter lwoffii. Sci Total Environ 624:1106–1118
Das S, Jean JS, Kar S, Chou ML, Chen CY (2014) Screening of plant growth-promoting traits in arsenic-resistant bacteria isolated from agricultural soil and their potential implication for arsenic bioremediation. J Hazard Mater 272:112–120
Das S, Bora SS, Yadav RNS, Barooah M (2017) A metagenomic approach to decipher the indigenous microbial communities of arsenic contaminated groundwater of Assam. Genom Data 12:89–96
Datta SP, Subba Rao A, Ganesha Murthy AN (1997) Effect of electrolytes coupled with variable stirring on soil pH. J Indian Soc Soil Sci 45:185–187
de-Bashan LE, Hernandez JP, Bashan Y (2012) The potential contribution of plant growth-promoting bacteria to reduce environmental degradation—A comprehensive evaluation. Appl Soil Ecol 61:171–189
Dell’Amico E, Cavalca L, Andreoni V (2008) Improvement of Brassica napus growth under cadmium stress by cadmium-resistant rhizobacteria. Soil Biol Biochem 40(1):74–84
Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM (2008) Phylogeny. Fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36(suppl_2):W465–W469
Ghosh P, Rathinasabapathi B, Ma LQ (2011) Arsenic-resistant bacteria solubilized arsenic in the growth media and increased growth of arsenic hyperaccumulator Pteris vittata L. Bioresour Technol 102(19):8756–8761
Ghosh PK, Maiti TK, PramanikK GSK, Mitra S, De TK (2018) The role of arsenic resistant Bacillus aryabhattai MCC3374 in promotion of rice seedlings growth and alleviation of arsenic phytotoxicity. Chemosphere 211:407–419
Govindarajan M, Balandreau J, Muthukumarasamy R, Revathi G, Lakshminarasimhan C (2006) Improved yield of micropropagated sugarcane following inoculation by endophytic Burkholderia vietnamiensis. Plant Soil 280(1):239–252
Han YH, Fu JW, Chen Y, Rathinasabapathi B, Ma LQ (2016) Arsenic uptake, arsenite efflux and plant growth in hyperaccumulator Pteris vittata: role of arsenic-resistant bacteria. Chemosphere 144:1937–1942
Johnston S, Barnard WM (1979) Comparative effectiveness of fourteen solutions for extracting arsenic from four western New York soils. Soil Sci Soc Am J 43:304–308
Kaushal M, Kaushal R (2015) Acetylene reductase activity and molecular characterization of plant growth promoting rhizobacteria to know efficacy in integrated nutrient management system. Indian J Biotechnol 14:221–227
Khambalkar P, Sridar R (2015) Isolation and characterization of nitrogen fixing Burkholderia sp. Int J Environ Agric Biotech 8(3):681–689
Kim SJ, Kremer RJ (2005) Scanning and transmission electron microscopy of root colonization of morning glory (lpomoea spp.) seedlings by rhizobacteria. Symbiosis 39:117–124
Kinegam S, Yingprasertchai T, Tanasupawat S, Leepipatpiboon N, Akaracharanya A, Kim KW (2008) Isolation and characterization of As(III)-oxidizing bacteria from As-contaminated soils in Thailand. World J Microbiol Biotechnol 24(12):3091–3096
Kuklinsky-Sobral J, Araújo WL, Mendes R, Geraldi IO, Pizzirani-Kleiner AA, Azevedo JL (2004) Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ Microbiol 6(12):1244–1251
Laha A, Bhattacharyya S, Sengupta S, Bhattacharyya K, GuhaRoy S (2021a) Rhizobium leguminosarum: a model arsenic resistant, arsenite oxidizing bacterium possessing plant growth promoting attributes. Curr World Environ 16:84–93
Laha A, Bhattacharyya S, Sengupta S, Bhattacharyya K, GuhaRoy S (2021b) Study on Burkholderia sp: arsenic resistant bacteria isolated from contaminated soil. Appl Ecol Environ Sci 9(2):144–148
Laha A, Bhattacharyya S, Sengupta S, Bhattacharyya K, GuhaRoy S (2021c) Investigation of arsenic-resistant, arsenite-oxidizing bacteria for plant growth promoting traits isolated from arsenic contaminated soils. Arch Microbiol 203:4677–4692
Laha A, Sengupta S, Bhattacharya P, Mandal J, Bhattacharyya S, Bhattacharyya K (2022) Recent advances in the bioremediation of arsenic-contaminated soils: a mini review. World J Microbiol Biotechnol 38(11):189
Laha A, Sengupta S, Mandal J, Bhattacharyya K, Bhattacharyya S (2023) The role of plant growth promoting bacteria on arsenic removal: a review of existing perspectives. In: Nitish Kumar, Sanjeev Kumar (Ed.) Arsenic toxicity remediation: biotechnological approaches. Springer, Cham, pp 3–14
Ma Y, Prasad MNV, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29(2):248–258
Madhaiyan M, Poonguzhali S, Sa T (2007) Metal tolerating methylotrophic bacteria reduces nickel and cadmium toxicity and promotes plant growth of tomato (Lycopersicon esculentum L.). Chemosphere 69(2):220–228
Majumder A, Bhattacharyya K, Bhattacharyya S, Kole SC (2013) Arsenic-tolerant, arsenite-oxidising bacterial strains in the contaminated soils of West Bengal, India. Sci Total Environ 463:1006–1014
Mallick I, Bhattacharyya C, Mukherji S, Dey D, Sarkar SC, Mukhopadhyay UK, Ghosh A (2018) Effective rhizoinoculation and biofilm formation by arsenic immobilizing halophilic plant growth promoting bacteria (PGPB) isolated from mangrove rhizosphere: a step towards arsenic rhizoremediation. Sci Total Environ 610:1239–1250
Mandal J, Golui D, Datta SP (2019) Assessing equilibria of organo-arsenic complexes and predicting uptake of arsenic by wheat grain from organic matter amended soils. Chemosphere 234:419–426
Mandal J, Sengupta S, Sarkar S, Mukherjee A, Wood MD, Hutchinson SM, Mondal D (2021) Meta-analysis enables prediction of the maximum permissible arsenic concentration in Asian paddy soil. Front Environ Sci 9:547
Mandal J, Jain V, Sengupta S, Rahman MA, Bhattacharyya K, Rahman MM, Golui D, Wood MD, Mondal D (2023) Determination of bioavailable arsenic threshold and validation of modeled permissible total arsenic in paddy soil using machine learning. J Environ Qual 52(2):315–327
Meharg AA (2004) Arsenic in rice—understanding a new disaster for south-east Asia. Trends Plant Sci 9:415–417
Pandey N, Bhatt R (2016) Role of soil associated Exiguobacterium in reducing arsenic toxicity and promoting plant growth in Vigna radiata. Eur J Soil Biol 75:142–150
Pramanik K, Mitra S, Sarkar A, Maiti TK (2018) Alleviation of phytotoxic effects of cadmium on rice seedlings by cadmium resistant PGPR strain Enterobacter aerogenes MCC 3092. J Hazard Mater 351:317–329
Ruuskanen MO (2019) Lake sediment microbial communities in the anthropocene (Doctoral dissertation, Université d'Ottawa/University of Ottawa)
Sanz E, Munoz-Olivas R, Camara C, Sengupta MK, Ahamed S (2007) Arsenic speciation in rice, straw, soil, hair and nails samples from the arsenic-affected areas of Middle and Lower Ganga plain. J Environ Sci Health A 42(12):1695–1705
Sengupta S, Bhattacharyya K, Mandal J, Bhattacharya P, Halder S, Pari A (2021) Deficit irrigation and organic amendments can reduce dietary arsenic risk from rice: introducing machine learning-based prediction models from field data. Agric Ecosyst Environ 319:107516
Sengupta S, Bhattacharyya K, Mandal J, Bhattacharya P, Chattopadhyay AP (2023a) Zinc and iron enrichment of vermicompost can reduce the arsenic load in rice grain: an investigation through pot and field experiments. J Clean Prod 419:138267
Sengupta S, Patra SK, Laha A, Poddar R, Bhattacharyya K, Dey P, Mandal J (2023b) Replacing conventional surface irrigation with micro-irrigation in vegetables can alleviate arsenic toxicity and improve water productivity. Groundw Sustain Dev 23:101012
Silver S, Phung LT (1996) Bacterial heavy metal resistance: new surprises. Annu Rev Microbiol 50(1):753–789
Sivasakthi S, Usharani G, Saranraj P (2014) Biocontrol potentiality of plant growth promoting bacteria (PGPR)-Pseudomonas fluorescens and Bacillus subtilis: a review. Afr J Agric Res 9(16):1265–1277
Sparks DL, Page AL, Helmke PA, Leoppert RH, Solthanpour PN, Tabatabai MA, Johnston CT, Sumner ME (2006) Methods of soil analysis. Part 3 chemical methods. Soil Science Society of America, Madison, pp 811–831
Srivastava S, Verma PC, Chaudhry V, Singh N, Abhilash PC, Kumar KV, Sharma N, Singh N (2013) Influence of inoculation of arsenic-resistant Staphylococcus arlettae on growth and arsenic uptake in Brassica juncea (L.) Czern. Var. R-46. J Hazard Mater 262:1039–1047
Subbiah B, Asija GL (1956) Alkaline permanganate method of available nitrogen determination. Curr Science 25:259
Sundararao WVB (1963) Phosphate dissolving organisms in the soil and rhizosphere. Indian J Agric Sci 33:272–278
Tirry N, Joutey NT, Sayel H, Kouchou A, Bahafid W, Asri M, El Ghachtouli N (2018) Screening of plant growth promoting traits in heavy metals resistant bacteria: prospects in phytoremediation. J Genet Eng Biotechnol 16(2):613–619
Tiwari S, Sarangi BK, Thul ST (2016) Identification of arsenic resistant endophytic bacteria from Pteris vittata roots and characterization for arsenic remediation application. J Environ Manag 180:359–365
Zhao FJ, Zhu YG, Meharg AA (2013) Methylated arsenic species in rice: geographical variation, origin, and uptake mechanisms. Environ Sci Technol 47(9):3957–3966
Acknowledgements
The authors are grateful to the ICAR-Niche area of Excellence-Arsenic Research Laboratory, Bidhan Chandra Krishi Viswavidyalaya (BCKV), Kalyani, Nadia as well as Department of Genetics & Plant Breeding and Department of Agronomy, Bidhan Chandra Krishi Viswavidyalaya (BCKV), Mohanpur, Nadia, West Bengal, India for providing technical and all other necessary assistance during the study.
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Author information
Authors and Affiliations
Contributions
A.L.: Methodology, Investigation, Data curation, Software and Writing-Original draft preparation; S.S.: Data curation, Visualization, Software, Writing-Reviewing and Editing; S.B.: Conceptualization, Methodology, Supervision; K.B.: Conceptualization, Methodology, Validation, Formal reviewing; S.G.: Conceptualization, Methodology, and Supervision.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Research involving human participants and/or animals
This article does not contain any studies with human participants or animals performed by any of the authors.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Laha, A., Sengupta, S., Bhattacharyya, S. et al. Isolation and characterization of rhizobacteria from lentil for arsenic resistance and plant growth promotion. 3 Biotech 14, 30 (2024). https://doi.org/10.1007/s13205-023-03873-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-023-03873-9