Abstract
Selenite reducing bacterial strain (GUSDM4) isolated from Mandovi estuary of Goa, India was identified as Halomonas venusta based on 16S rRNA gene sequence analysis. Its maximum tolerance level for sodium selenite (Na2SeO3) was 100 mM. The 2, 3-diaminonaphthalene-based spectroscopic analysis demonstrated 96 and 93% reduction of 2 and 4 mM Na2SeO3 respectively to elemental selenium (Se0) during the late stationary growth phase. Biosynthesis of Se nanoparticles (SeNPs) commenced within 4 h during the log phase, which was evident from the brick red color in the growth medium and a characteristic peak at 265 nm revealed by UV–Vis spectrophotometry. The intracellular periplasmic synthesis of SeNPs in GUSDM4 was confirmed by transmission electron microscopy (TEM). Characterization of SeNPs by X-ray crystallography, TEM and energy-dispersive X-ray analysis (EDAX) clearly demonstrated spherical SeNPs of 20–80 nm diameter with hexagonal crystal lattice. SeNPs (0.8 and 1 mg/L) primed seeds under arsenate [As(V)] stress showed increase in shoot length, root length and biomass by 1.4-, 1.5- and 1.1-fold respectively, as compared to As(V) primed seeds alone. The proline and phenolic content in seeds primed with SeNPs under arsenate stress showed alleviated levels proving its ameliorative potential. SeNPs also demonstrated anti-biofilm activity at 20 µg/mL against human pathogens which was evident by scanning electron microscopic (SEM) analysis. SeNPs interestingly revealed mosquito larvicidal activity also. Therefore, these studies have clearly demonstrated amazing potential of the marine bacterium, Halomonas venusta in biosynthesis of SeNPs and their applications as ameliorative, anti-biofilm and mosquito larvicidal agents which is the first report of its kind.
Similar content being viewed by others
Availability of data and material
The datasets generated during and/or analyzed during the current study are available in the GenBank repository (MG430411). All data generated or analyzed during this study are included in this published article (and its supplementary information files).
Code availability
All the software used in the current study has been mentioned in the article with appropriate reference.
References
Ábrahám E, Hourton-Cabassa C, Erdei L, Szabados L (2010) Methods for determination of proline inplants. In: Plant stress tolerance. Humana Press, pp 317–331
Akçay FA, Avcı A (2020) Effects of process conditions and yeast extract on the synthesis of selenium nanoparticles by a novel indigenous isolate Bacillus sp. EKT1 and characterization of nanoparticles. Arch Microbiol 202(8):2233–2243
Allan CB, Lacourciere GM, Stadtman TC (1999) Responsiveness of selenoproteins to dietary selenium. Ann Rev Nutr 19:1–16
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1999) Basic local alignment search tool. J Mol Biol 215:403–410
Arthur JR, McKenzie RC, Beckett GJ (2003) Selenium in the immune system. J Nutr 133:1457S-1459S
Cartes P, Gianfreda L, Paredes C, Mora ML (2011) Selenium uptake and its antioxidant role in ryegrass cultivars as affected by selenite seed pelletization. J Soil Sci Plant Nutr 11(4):1–14
Chen JS (2012) An original discovery: selenium deficiency and Keshan disease (an endemic heart disease). Asia Pac J Clin Nutr 21:320–326
Dhanjal S, Cameotra SS (2010) Aerobic biogenesis of selenium nanospheres by Bacillus cereus isolated from coalmine soil. Microb Cell Fact 9(1):1–11
Ellis RH, Roberts EH (1981) The quantification of ageing and survival in orthodox seeds. Seed Sci Technol (Netherlands)
Eswayah AS, Smith TJ, Gardiner PH (2016) Microbial transformations of selenium species of relevance to bioremediation. Appl Environ Microbiol 82(16):4848–4859
Forootanfar H, Adeli-Sardou M, Nikkhoo M, Mehrabani M, Amir-Heidari B, Shahverdi AR, Shakibaie M (2014) Antioxidant and cytotoxic effect of biologically synthesized selenium nanoparticles in comparison to selenium dioxide. J Trace Elem Med Bio 28:75–79
Ghosh A, Mohod AM, Paknikar KM, Jain RK (2008) Isolation and characterization of selenite-and selenate-tolerant microorganisms from selenium-contaminated sites. World J Microbiol Biotechnol 24:1607–1611
Ghosh A, Chowdhury N, Chandra G (2012) Plant extracts as potential mosquito larvicides. IJMR 135:581
Hunter WJ, Manter DK (2009) Reduction of selenite to elemental red selenium by Pseudomonas sp. strain CA5. Curr Microbiol 58:493–498
Javed S, Sarwar A, Tassawar M, Faisal M (2015) Conversion of selenite to elemental selenium by indigenous bacteria isolated from polluted areas. Chem Spec Bioavailab 7(4):162–168
Kessi J, Ramuz M, Wehrli E, Spycher M, Bachofen R (1999) Reduction of selenite and detoxification of elemental selenium by the Phototrophic Bacterium Rhodospirillum rubrum. Appl Environ Microbiol 65(11):4734–4740
Khaliq A, Ali S, Hameed A, Farooq MA, Farid M, Shakoor MB, Rizwan M (2016) Silicon alleviates nickel toxicity in cotton seedlings through enhancing growth, photosynthesis, and suppressing Ni uptake and oxidative stress. Arch Agron Soil Sci 62(5):633–647
Khanolkar DS, Dubey SK, Naik MM (2015) Biotransformation of tributyltin chloride to less toxic dibutyltin dichloridee and monobutyltin trichloride by Klebsiella pneumoniae strain SD9. Int Biodeter Biodegr 104:212–218
Klaus T, Joerger R, Olsson E, Granqvist C (1999) Silver-based crystalline nanoparticles, microbially fabricated. PNAS (0) 96(24):13611–13614
Mishra RR, Prajapati S, Das J, Dangar TK, Das N, Thatoi H (2011) Reduction of selenite to red elemental selenium by moderately halotolerant Bacillus megaterium strains isolated from Bhitarkanika mangrove soil and characterization of reduced product. Chemosphere 84:231–1237
Morris J, Crane S (2013) Selenium toxicity from a misformulated dietary supplement, adverse health effects, and the temporal response in the nail biologic monitor. Nutrients 5:1024–1057
Moulick D, Ghosh D, Santra SC (2016) Evaluation of effectiveness of seed priming with selenium in rice during germination under arsenic stress. Plant Physiol Biochem 109:571–578
Mujawar SY, Shamim K, Vaigankar DC, Dubey SK (2019) Arsenite biotransformation and bioaccumulation by Klebsiella pneumoniae strain SSSW7 possessing arsenite oxidase (aioA) gene. Biometals 32:65–76
Naik MM, Dubey SK (2013) Lead resistant bacteria: lead resistance mechanisms, their applications in lead bioremediation and biomonitoring. Ecotoxicol Environ Saf 98:1–7
Naik MM, Dubey SK (2017) Marine pollution and microbial remediation. Springer, Singapore
Narasingarao P, Häggblom MM (2007) Identification of anaerobic selenate-respiring bacteria from aquatic sediments. Appl Environ Microbiol 73:3519–3527
Oremland RS, Herbel MJ, Blum JS, Langley S, Beveridge TJ, Ajayan PM, Sutto T, Ellis AV, Curran S (2004) Structural and spectral features of selenium nanospheres produced by Se-respiring bacteria. Appl Environ Microbiol 70:52–60
Ouédraogo O, Chételat J, Amyot M (2015) Bioaccumulation and trophic transfer of mercury and selenium in African sub-tropical fluvial reservoirs food webs (Burkina Faso). PLoS ONE 10(4):0123048
Ranjard L, Prigent-Combaret C, Nazaret S, Cournoyer B (2002) Methylation of inorganic and organic selenium by the bacterial thiopurine methyltransferase. J Bacteriol 184:3146–3149
Rathgeber C, Yurkova N, Stackebrandt E, Beatty JT, Yurkov V (2002) Isolation of tellurite-and selenite-resistant bacteria from hydrothermal vents of the juan de fuca ridge in the Pacific ocean. Appl Environ Microbiol 68:4613–4622
Rauschenbach I, Narasingarao P, Häggblom MM (2011) Desulfurispirillum indicum sp. nov, a selenate-and selenite-respiring bacterium isolated from an estuarine canal. Int J Syst Evol Microbiol 61:654–658
Samant S, Naik M, Parulekar K, Charya L, Vaigankar D (2018) Selenium reducing Citrobacter fruendii strain KP6 from Mandovi estuary and its potential application in selenium nanoparticle synthesis. Proc Natl Sci India Sect B: Bio Sci 88:747–754
Shakibaie M, Forootanfar H, Golkari Y, Mohammadi-Khorsand T, Shakibaie MR (2015) Anti-biofilm activity of biogenic selenium nanoparticles and selenium dioxide against clinical isolates of Staphylococcus aureus, Pseudomonas aeruginosa, and Proteus mirabilis. J Trace Elem Med Biol 29:235–241
Shirsat S, Kadam A, Naushad M, Mane RS (2015) Selenium nanostructures: microbial synthesis and applications. RSC Adv 5(112):92799–92811
Siddique T, Zhang Y, Okeke BC, Frankenberger WT Jr (2006) Characterization of sediment bacteria involved in selenium reduction. Bioresour Technol 97:1041–1049
Soda S, Takahashi H, Kagami T, Miyake M, Notaguchi E, Sei K, Iwasaki N, Ike M (2012) Biotreatment of selenium refinery wastewater using pilot-scale granular sludge and swim-bed bioreactors augmented with a selenium-reducing bacterium Pseudomonas stutzeri NT-I. J Water Treat Biol 48(2):63–71
Sowndarya P, Ramkumar G, Shivakumar MS (2017) Green synthesis of selenium nanoparticles conjugated Clausena dentata plant leaf extract and their insecticidal potential against mosquito vectors. Artif Cell Nanomed B 451:490–1495
Srivastava P, Kowshik M (2016) Anti-neoplastic selenium nanoparticles from Idiomarina sp. PR58-8. Enzyme Microb Technol 95:192–200
Srivastava N, Mukhopadhyay M (2013) Biosynthesis and structural characterization of selenium nanoparticles mediated by Zooglearamigera. Powder Technol 244:26–29
Srivastava P, Braganca JM, Kowshik M (2014) In vivo synthesis of selenium nanoparticles by Halococcus salifodinae BK18 and their anti-proliferative properties against HeLa cell line. Biotechnol Prog 30:1480–1487
Stoeva S, Klabunde KJ, Sorensen CM, Dragieva I (2002) Gram-Scale Synthesis of Monodisperse Gold Colloids by the Solvated Metal Atom Dispersion Method and Digestive Ripening and Their Organization into Two-and Three-Dimensional structures. J Am ChemSoc 124:2305–2311
Sunitha MSL, Prashanth S, Kishor PK (2015) Characterization of arsenic-resistant bacteria and their arsgenotype for metal bioremediation. Int J Sci Eng Res 6:304–309
Swain T, Hillis WE (1959) The phenolic constituents of Prunus domestica. I.—The quantitativeanalysis of phenolic constituents. J Sci Food Agric 10(1):63–68
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Tan Y, Yao R, Wang R, Wang D, Wang G, Zheng S (2016) Reduction of selenite to Se (0) nanoparticles by filamentous bacterium Streptomyces sp. ES2–5 isolated from a selenium mining soil. Microb Cell Fact 15:157
Vaigankar DC, Dubey SK, Mujawar SY, D’Costa A, Shyama SK (2018) Tellurite biotransformation and detoxification by Shewanella baltica with simultaneous synthesis of tellurium nanorods exhibiting photo-catalytic and anti-biofilm activity. Ecotox Environ Safe 165:516–526
Watkinson JH (1966) Fluorimetric determination of selenium in bio-logical material with 2, 3-diaminonaphtalene. Anal Chem 38:92–97
Xu XY, McGrath SP, Meharg AA, Zhao FJ (2008) Growing rice aerobically markedly decreases arsenic accumulation. Environ Sci Technol 42(15):5574–5579
Yang YC, Lee SG, Lee HK, Kim MK, Lee SH, Lee HS (2002) A piperidine amide extracted from Piper longum L. fruit shows activity against Aedes aegypti mosquito larvae. J Agric Food Chem 50:3765–3767
Zeng H, Combs G Jr (2008) Selenium as an anticancer nutrient: roles in cell proliferation and tumor cell invasion. J Nutr Biochem 19:1–7
Zhao FJ, Ma JF, Meharg AA, McGrath SP (2009) Arsenic uptake and metabolism in plants. New Phytol 181(4):777–794
Acknowledgements
The authors thank Mr Areef Sardar and Mr Girish Prabhu from CSIR-National Institute of Oceanography, Goa for EDAX and XRD analysis respectively. The authors also acknowledge AIIMS, New Delhi for TEM analysis.
Funding
This work was supported by University Grants Commission, New Delhi as a junior research fellow [Ref. no. F/2017–18(SA-III)].
Author information
Authors and Affiliations
Contributions
DCV has designed, performed and analyzed the experiments. She has also prepared the draft of the manuscript. SKD professor and mentor has contributed to experimental designs, verified the data, and critically corrected the manuscript to bring in the final form. SYM has assisted in experimental work and making draft manuscript. AKM has helped in designing and conducting mosquito larvicidal assays.
Corresponding author
Ethics declarations
Conflict of interest
DCV received the grants from University Grants Commission, New Delhi as a junior research fellow [Ref. no. F/2017–18(SA-III)].
SYM declares no conflict of interest. AKM declares no conflict of interest. SKD declares no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Consent to participate
All the authors have agreed with the content and have given explicit consent to submit and all have obtained permission from the responsible authorities at the institute/organization where the work has been carried out.
Consent for publication
All authors whose names appear on the submission have approved the version to be published, and have agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.
Additional information
Communicated by Erko Stackebrandt.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Vaigankar, D.C., Mujawar, S.Y., Mohanty, A.K. et al. Biogenesis of selenium nanospheres using Halomonas venusta strain GUSDM4 exhibiting potent environmental applications. Arch Microbiol 204, 372 (2022). https://doi.org/10.1007/s00203-022-02977-9
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-022-02977-9