Skip to main content

Advertisement

SpringerLink
Log in

Rapid arsenite oxidation by Paenarthrobacter nicotinovorans strain SSBW5: unravelling the role of GlpF, aioAB and aioE genes

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

A novel arsenite resistant bacterial strain SSBW5 was isolated from the battery waste site of Corlim, Goa, India. This strain interestingly exhibited rapid arsenite oxidation with an accumulation of 5 mM arsenate within 24 h and a minimum inhibitory concentration (MIC) of 18 mM. The strain SSBW5 was identified as Paenarthrobacter nicotinovorans using 16S rDNA sequence analysis. Fourier-transformed infrared (FTIR) spectroscopy of arsenite-exposed cells revealed the interaction of arsenite with several important functional groups present on the cell surface, possibly involved in the resistance mechanism. Interestingly, the whole genome sequence analysis also clearly elucidated the presence of genes, such as GlpF, aioAB and aioE encoding transporter, arsenite oxidase and oxidoreductase enzyme, respectively, conferring their role in arsenite resistance. Furthermore, this strain also revealed the presence of several other genes conferring resistance to various metals, drugs, antibiotics and disinfectants. Further suggesting the probable direct or indirect involvement of these genes in the detoxification of arsenite thereby increasing its tolerance limit. In addition, clumping of bacterial cells was observed through microscopic analysis which could also be a strategy to reduce arsenite toxicity thus indicating the existence of multiple resistance mechanisms in strain SSBW5. In the present communication, we are reporting for the first time the potential of P. nicotinovorans strain SSBW5 to be used in the bioremediation of arsenite via arsenite oxidation along with other toxic metals and metalloids.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

The data sets generated during and/or analyzed during the current study are available in the GenBank repository (MN640912 and SZVS00000000). All the data sets generated or analyzed during this study are included in this published article and its supplementary information files.

References

  • Aguilar NC, Faria MC, Pedron T, Batista BL, Mesquita JP, Bomfeti CA, Rodrigues JL (2020) Isolation and characterization of bacteria from a brazilian gold mining area with a capacity of arsenic bioaccumulation. Chemosphere 240:124871

    Article  CAS  PubMed  Google Scholar 

  • Andres J, Bertin PN (2016) The microbial genomics of arsenic. FEMS Microbiol Rev 40(2):299–322

    Article  CAS  PubMed  Google Scholar 

  • Antenozio ML, Giannelli G, Marabottini R, Brunetti P, Allevato E, Marzi D, Capobianco G, Bonifazi G, Serranti S, Visioli G, Stazi SR (2021) Phytoextraction efficiency of Pteris vittata grown on a naturally As-rich soil and characterization of As-resistant rhizosphere bacteria. Sci Rep 11(1):6794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Banerjee S, Datta S, Chattyopadhyay D, Sarkar P (2011) Arsenic accumulating and transforming bacteria isolated from contaminated soil for potential use in bioremediation. J Environ Sci Health A 46(14):1736–1747

    Article  CAS  Google Scholar 

  • Banerjee A, Sarkar S, Gorai S, Kabiraj A, Bandopadhyay R (2021) High arsenic tolerance in Brevundimonas aurantiaca PFAB1 from an arsenic-rich Indian hot spring. Electron J Biotechnol 53:1–7

    Article  CAS  Google Scholar 

  • Ben Fekih I, Zhang C, Li YP, Zhao Y, Alwathnani HA, Saquib Q, Rensing C, Cervantes C (2018) Distribution of arsenic resistance genes in prokaryotes. Front Microbiol 9:2473

    Article  PubMed  PubMed Central  Google Scholar 

  • Cai X, Zhang Z, Yin N, Du H, Li Z, Cui Y (2016) Comparison of arsenate reduction and release by three As (V)-reducing bacteria isolated from arsenic-contaminated soil of Inner Mongolia, China. Chemosphere 161:200–207

    Article  CAS  PubMed  Google Scholar 

  • Ceballos-Escalera A, Pous N, Chiluiza-Ramos P, Korth B, Harnisch F, Bañeras L, Balaguer MD, Puig S (2021) Electro-bioremediation of nitrate and arsenite polluted groundwater. Water Res 190:116748

    Article  CAS  PubMed  Google Scholar 

  • Chang JS (2015) Biotransformation of arsenite and bacterial aox activity in drinking water produced from surface water of floating houses: arsenic contamination in Cambodia. Environ Pollut 206:315–323

    Article  CAS  PubMed  Google Scholar 

  • Crognale S, Amalfitano S, Casentini B, Fazi S, Petruccioli M, Rossetti S (2017) Arsenic-related microorganisms in groundwater: a review on distribution, metabolic activities and potential use in arsenic removal processes. Rev Environ Sci Biotechnol 16:647–665

    Article  CAS  Google Scholar 

  • Debiec-Andrzejewska K, Krucon T, Piatkowska K, Drewniak L (2020) Enhancing the plants growth and arsenic uptake from soil using arsenite-oxidizing bacteria. Environ Pollut 264:114692

    Article  CAS  PubMed  Google Scholar 

  • Haghi M, Diznabi SH, Karaboz I, Omeroglu EE (2023) Arsenic pollution and arsenic-resistant bacteria of drying Urmia Salt Lake. Front Environ Sci 11:1195643

    Article  Google Scholar 

  • Han YH, Jia MR, Liu X, Zhu Y, Cao Y, Chen DL, Chen Y, Ma LQ (2017) Bacteria from the rhizosphere and tissues of As-hyperaccumulator Pteris vittata and their role in arsenic transformation. Chemosphere 186:599–606

    Article  CAS  PubMed  Google Scholar 

  • Hartl FU (1996) Molecular chaperones in cellular protein folding. Nature 381(6583):571–580

    Article  CAS  PubMed  Google Scholar 

  • Imran M, Das KR, Naik MM (2019) Co-selection of multi-antibiotic resistance in bacterial pathogens in metal and microplastic contaminated environments: an emerging health threat. Chemosphere 215:846–857

    Article  CAS  PubMed  Google Scholar 

  • Jebelli MA, Maleki A, Amoozegar MA, Kalantar E, Gharibi F, Darvish N, Tashayoe H (2018) Isolation and identification of the native population bacteria for bioremediation of high levels of arsenic from water resources. J Environ Manag 212:39–45

    Article  CAS  Google Scholar 

  • Ji Y, Wang L, Jiang M, Lu J, Ferronato C, Chovelon JM (2017) The role of nitrite in sulfate radical-based degradation of phenolic compounds: an unexpected nitration process relevant to groundwater remediation by in-situ chemical oxidation (ISCO). Water Res 123:249–257

    Article  CAS  PubMed  Google Scholar 

  • Kabiraj A, Biswas R, Halder U, Bandopadhyay R (2022) Bacterial arsenic metabolism and its role in arsenic bioremediation. Curr Microbiol 79(5):1–5

    Article  Google Scholar 

  • Kashyap DR, Botero LM, Lehr C, Hassett DJ, McDermott TR (2006) A Na+: H+ antiporter and a molybdate transporter are essential for arsenite oxidation in Agrobacterium tumefaciens. J Bacteriol 188(4):1577–1584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khairul I, Wang QQ, Jiang YH, Wang C, Naranmandura H (2017) Metabolism, toxicity and anticancer activities of arsenic compounds. Oncotarget 8(14):23905

    Article  PubMed  PubMed Central  Google Scholar 

  • Khanna K, Kohli SK, Kumar P, Ohri P, Bhardwaj R, Alam P, Ahmad P (2022) Arsenic as hazardous pollutant: perspectives on engineering remediation tools. Sci Total Environ 838:155870

    Article  CAS  PubMed  Google Scholar 

  • Khoei AJ, Joogh NJ, Darvishi P, Rezaei K (2018) Application of physical and biological methods to remove heavy metal, arsenic and pesticides, malathion and diazinon from water. Turk J Fish Aquat Sci 19(1):21–28

    Google Scholar 

  • Koechler S, Cleiss-Arnold J, Proux C, Sismeiro O, Dillies MA, Goulhen-Chollet F, Hommais F, Lièvremont D, Arsène-Ploetze F, Coppée JY, Bertin PN (2010) Multiple controls affect arsenite oxidase gene expression in Herminiimonas arsenicoxydans. BMC Microbiol 10(1):53

    Article  PubMed  PubMed Central  Google Scholar 

  • Kognou AL, Chio C, Khatiwada JR, Shrestha S, Chen X, Zhu Y, Ngono Ngane RA, Agbor Agbor G, Jiang ZH, Xu CC, Qin W (2023) Characterization of potential virulence, resistance to antibiotics and heavy metals, and biofilm-forming capabilities of soil lignocellulolytic bacteria. Microb Physiol 33(1):36–48

    Article  Google Scholar 

  • Koutros S, Lenz P, Hewitt SM, Kida M, Jones M, Schned AR, Baris D, Pfeiffer R, Schwenn M, Johnson A, Karagas MR (2018) RE: Elevated bladder cancer in northern new England: the role of drinking water and arsenic. JNCI Nat Cancer Inst 110(11):1273–1274

    Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laha A, Bhattacharyya S, Sengupta S, Bhattacharyya K, GuhaRoy S (2021) Investigation of arsenic-resistant, arsenite-oxidizing bacteria for plant growth promoting traits isolated from arsenic contaminated soils. Arch Microbiol 7:4677–4692

    Article  Google Scholar 

  • Lemire JA, Harrison JJ, Turner RJ (2013) Antimicrobial activity of metals: mechanisms, molecular targets and applications. Nat Rev Microbiol 11(6):371–384

    Article  CAS  PubMed  Google Scholar 

  • Lescure T, Joulian C, Charles C, Saanda TB, Charron M, Breeze D, Bauda P, Battaglia-Brunet F (2020) Simple or complex organic substrates inhibit arsenite oxidation and aioA gene expression in two β-Proteobacteria strains. Res Microbiol 171(1):13–20

    Article  CAS  PubMed  Google Scholar 

  • Lett MC, Paknikar KM, Lievremont D (2001) A simple and rapid method for arsenite and arsenate speciation. Process Metall 11:541–546

    Google Scholar 

  • Li X, Gu AZ, Zhang Y, Xie B, Li D, Chen J (2019) Sub-lethal concentrations of heavy metals induce antibiotic resistance via mutagenesis. J Hazard Mater 369:9–16

    Article  CAS  PubMed  Google Scholar 

  • Liu S, Zhang F, Chen J, Sun G (2011) Arsenic removal from contaminated soil via biovolatilization by genetically engineered bacteria under laboratory conditions. J Environ Sci 23(9):1544–1550

    Article  CAS  Google Scholar 

  • Lloyd NA, Nazaret S, Barkay T (2018) Whole genome sequences to assess the link between antibiotic and metal resistance in three coastal marine bacteria isolated from the mummichog gastrointestinal tract. Mar Pollut Bull 135:514–520

    Article  CAS  PubMed  Google Scholar 

  • Lupo A, Coyne S, Berendonk TU (2012) Origin and evolution of antibiotic resistance: the common mechanisms of emergence and spread in water bodies. Front Microbiol 3:18

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma B, Song W, Zhang X, Chen M, Li J, Yang X, Zhang L (2023) Potential application of novel cadmium-tolerant bacteria in bioremediation of Cd-contaminated soil. Ecotoxicol Environ Saf 255:114766

    Article  CAS  PubMed  Google Scholar 

  • Mahtani S, Mavinkurve S (1979) Microbial purification of longifolene-a sesquiterpene. J Ferment Technol 57:529–533

    CAS  Google Scholar 

  • Mandal BK, Suzuki KT (2002) Arsenic round the world: a review. Talanta 58(1):201–235

    Article  CAS  PubMed  Google Scholar 

  • 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 19:9883–9900

    Article  Google Scholar 

  • Meng YL, Liu Z, Rosen BP (2004) As(III) and Sb(III) uptake by GlpF and efflux by ArsB in Escherichia coli. J Biol Chem 279(18):18334–18341

    Article  CAS  PubMed  Google Scholar 

  • Miranda-Carrazco A, Vigueras-Cortés JM, Villa-Tanaca L, Hernández-Rodríguez C (2018) Cyanotrophic and arsenic oxidizing activities of Pseudomonas mendocina P6115 isolated from mine tailings containing high cyanide concentration. Arch Microbiol 200(7):1037–1048

    Article  CAS  PubMed  Google Scholar 

  • 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(1):65–76

    Article  CAS  PubMed  Google Scholar 

  • Mujawar SY, Vaigankar DC, Dubey SK (2021) Biological characterization of Bacillus flexus strain SSAI1 transforming highly toxic arsenite to less toxic arsenate mediated by periplasmic arsenite oxidase enzyme encoded by aioAB genes. Biometals 34(4):895–907

    Article  CAS  PubMed  Google Scholar 

  • Mukhopadhyay R, Rosen BP, Phung LT, Silver S (2002) Microbial arsenic: from geocycles to genes and enzymes. FEMS Microbiol Rev 26(3):311–325

    Article  CAS  PubMed  Google Scholar 

  • Mukhopadhyay R, Bhattacharjee H, Rosen BP (2014) Aquaglyceroporins: generalized metalloid channels. Biochim Biophys Acta (BBA) 1840(5):1583–1591

    Article  CAS  PubMed  Google Scholar 

  • Naumann D, Helm D, Labischinski H, Giesbrecht P (1991) The characterization of microorganisms by Fourier-transform infrared spectroscopy. In: Nelson WH (ed) Modern techniques for rapid microbiological analysis. VCH, New York, pp 43–96

    Google Scholar 

  • Páez-Espino D, Tamames J, de Lorenzo V, Cánovas D (2009) Microbial responses to environmental arsenic. Biometals 22(1):117–130

    Article  PubMed  Google Scholar 

  • Pal C, Bengtsson-Palme J, Rensing C, Kristiansson E, Larsson DJ (2014) BacMet: antibacterial biocide and metal resistance genes database. Nucleic Acids Res 42(D1):D737–D743

    Article  CAS  PubMed  Google Scholar 

  • Palma-Lara I, Martínez-Castillo M, Quintana-Pérez JC, Arellano-Mendoza MG, Tamay-Cach F, Valenzuela-Limón OL, García-Montalvo EA, Hernández-Zavala A (2020) Arsenic exposure: a public health problem leading to several cancers. Regul Toxicol Pharmacol 110:104539

    Article  CAS  PubMed  Google Scholar 

  • Rahman S, Kim KH, Saha SK, Swaraz AM, Paul DK (2014) Review of remediation techniques for arsenic (As) contamination: a novel approach utilizing bio-organisms. J Environ Manag 134:175–185

    Article  CAS  Google Scholar 

  • Rathod J, Dhanani AS, Jean JS, Jiang WT (2019) The whole genome insight on condition-specific redox activity and arsenopyrite interaction promoting As-mobilization by strain Lysinibacillus sp. B2A1. J Hazard Mater 364:671–681

    Article  CAS  PubMed  Google Scholar 

  • Raturi G, Chaudhary A, Rana V, Mandlik R, Sharma Y, Barvkar V, Salvi P, Tripathi DK, Kaur J, Deshmukh R, Dhar H (2023) Microbial remediation and plant-microbe interaction under arsenic pollution. Sci Total Environ 864:160972

    Article  CAS  PubMed  Google Scholar 

  • Rosen BP (2002) Biochemistry of arsenic detoxification. FEBS Lett 529(1):86–92

    Article  CAS  PubMed  Google Scholar 

  • Satyapal GK, Mishra SK, Srivastava A, Ranjan RK, Prakash K, Haque R, Kumar N (2018) Possible bioremediation of arsenic toxicity by isolating indigenous bacteria from the middle Gangetic plain of Bihar, India. Biotechnol Rep 17:117–125

    Article  Google Scholar 

  • Sher S, Hussain SZ, Cheema MT, Hussain A, Rehman A (2022) Efficient removal potential of Microbacterium sp. strain 1S1 against arsenite isolated from polluted environment. J King Saud Univ Sci 34(5):102066

    Article  Google Scholar 

  • Shi K, Wang Q, Wang G (2020) Microbial oxidation of arsenite: regulation, chemotaxis, phosphate metabolism and energy generation. Front Microbiol 11:569282

    Article  PubMed  PubMed Central  Google Scholar 

  • Silver S, Phung LT (1996) Bacterial heavy metal resistance: new surprises. Ann Rev Microbiol 50(1):753–789

    Article  CAS  Google Scholar 

  • Silver S, Phung LT (2005) Genes and enzymes involved in bacterial oxidation and reduction of inorganic arsenic. Appl Environ Microbiol 71(2):599–608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh N, Gupta S, Marwa N, Pandey V, Verma PC, Rathaur S, Singh N (2016) Arsenic mediated modifications in Bacillus aryabhattai and their biotechnological applications for arsenic bioremediation. Chemosphere 164:524–534

    Article  CAS  PubMed  Google Scholar 

  • Sodhi KK, Kumar M, Agrawal PK, Singh DK (2019) Perspectives on arsenic toxicity, carcinogenicity and its systemic remediation strategies. Environ Technol Innov 16:100462

    Article  Google Scholar 

  • Studholme DJ, Jackson RA, Leak DJ (1999) Phylogenetic analysis of transformable strains of thermophilic Bacillus species. FEMS Microbiol Lett 172(1):85–90

    Article  CAS  PubMed  Google Scholar 

  • Suhadolnik ML, Salgado AP, Scholte LL, Bleicher L, Costa PS, Reis MP, Dias MF, Ávila MP, Barbosa FA, Chartone-Souza E, Nascimento A (2017) Novel arsenic-transforming bacteria and the diversity of their arsenic-related genes and enzymes arising from arsenic-polluted freshwater sediment. Sci Rep 7(1):1–17

    Article  CAS  Google Scholar 

  • Sultana M, Vogler S, Zargar K, Schmidt AC, Saltikov C, Seifert J, Schlömann M (2012) New clusters of arsenite oxidase and unusual bacterial groups in enrichments from arsenic-contaminated soil. Arch Microbiol 194(7):623–635

    Article  CAS  PubMed  Google Scholar 

  • Sun LN, Guo B, Lyu WG, Tang XJ (2020) Genomic and physiological characterization of an antimony and arsenite-oxidizing bacterium Roseomonas rhizosphaerae. Environ Res 191:110136

    Article  CAS  PubMed  Google Scholar 

  • Teixeira P, Tacão M, Alves A, Henriques I (2016) Antibiotic and metal resistance in a ST395 Pseudomonas aeruginosa environmental isolate: a genomics approach. Mar Pollut Bull 110(1):75–81

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Han Y, Shi K, Fan X, Wang L, Li M, Wang G (2017) An oxidoreductase AioE is responsible for bacterial arsenite oxidation and resistance. Sci Rep 7(1):1–10

    PubMed  PubMed Central  Google Scholar 

  • WHO (2017) Guidelines for drinking-water quality: fourth edition incorporating the first addendum, 4th edn. World Health Organization, Geneva

    Google Scholar 

  • Wu Y, Feng S, Li B, Mi X (2010) The characteristics of Escherichia coli adsorption of arsenic(III) from aqueous solution. World J Microbiol Biotechnol 26(2):249–256

    Article  CAS  Google Scholar 

  • Yang Z, Wu Z, Liao Y, Liao Q, Yang W, Chai L (2017) Combination of microbial oxidation and biogenic schwertmannite immobilization: a potential remediation for highly arsenic-contaminated soil. Chemosphere 181:1–8

    Article  CAS  PubMed  Google Scholar 

  • Yuan C, Li P, Qing C, Kou Z, Wang H (2022) Different regulatory strategies of arsenite oxidation by two isolated Thermus tengchongensis strains from hot springs. Front Microbiol 13:817891

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao M, Zheng G, Kang X, Zhang X, Guo J, Zhang M, Zhang J, Chen Y, Xue L (2023) Arsenic pollution remediation mechanism and preliminary application of arsenic-oxidizing bacteria isolated from industrial wastewater. Environ Pollut 324:121384

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Mujawar SY is grateful to University Grants Commission, New Delhi, for financial support as Senior Research Fellow (SRF). The authors are also thankful to Dr. B. R. Srinivasan and Mr. Rahul Kerkar from Department of Chemistry, Goa University for FTIR analysis.

Funding

This work was supported by University Grants Commission, New Delhi as Senior Research Fellow (SRF) [Award Letter No. F1-17.1/2015-16/MANF-2015-17-Goa-50641].

Author information

Author notes

  1. Santosh Kumar Dubey

    Present address: Center of Advanced Study in Botany, Banaras Hindu University, Varanasi, U.P., 221005, India

Authors and Affiliations

  1. Laboratory of Bacterial Genetics and Environmental Biotechnology, Department of Microbiology, Goa University, Taleigao Plateau, Goa, 403206, India

    Sajiya Yusuf Mujawar, Kashif Shamim, Diviya Chandrakant Vaigankar, Milind Mohan Naik & Santosh Kumar Dubey

  2. National Centre for Natural Product Research, University of Mississippi, Oxford, MS, USA

    Kashif Shamim

  3. Marine Microbiology, School of Earth, Ocean and Atmospheric Sciences, Goa University, Taleigao Plateau, Goa, 403206, India

    Diviya Chandrakant Vaigankar

Authors
  1. Sajiya Yusuf Mujawar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kashif Shamim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Diviya Chandrakant Vaigankar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Milind Mohan Naik
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Santosh Kumar Dubey
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Experimental design, data collection and analysis was performed by SYM. The first draft of the manuscript was written by SYM and all the authors provided their comments and suggestions on the previous versions of the manuscript. SKD mentored the experiments, corrected and thoroughly edited the manuscript. All the authors have read and approved the final manuscript.

Corresponding author

Correspondence to Santosh Kumar Dubey.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Communicated by Yusuf Akhter.

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.

Supplementary file1 (DOCX 841 KB)

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mujawar, S.Y., Shamim, K., Vaigankar, D.C. et al. Rapid arsenite oxidation by Paenarthrobacter nicotinovorans strain SSBW5: unravelling the role of GlpF, aioAB and aioE genes. Arch Microbiol 205, 333 (2023). https://doi.org/10.1007/s00203-023-03673-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00203-023-03673-y

Keywords

Search

Navigation