Skip to main content

Advertisement

Log in

Bioremediation potential of biofilm forming multi-metal resistant marine bacterium Pseudomonas chengduensis PPSS-4 isolated from contaminated site of Paradip Port, Odisha

  • Published:
Journal of Earth System Science Aims and scope Submit manuscript

Abstract

Biofilm forming and heavy metal resistant marine bacterial strain Pseudomonas chengduensis PPSS-4 was isolated from the contaminated marine sediment of Paradip Port, Odisha, India. The strain showed biofilm formation up to 100 mg/L of multi-metal [Pb(II), Cr(VI), and Cd(II)] supplementation in the culture medium. Scanning electron microscopy (SEM) showed aggregation of rod-shaped cells in the extracellular polymeric substance (EPS) matrix of biofilm. Confocal laser scanning microscopy (CLSM) exhibited a higher nucleic acid to the α-polysaccharide ratio in the biofilm, and the observed thickness was ~21 µm. The metal uptake potential of biofilm culture was higher than planktonic culture both in single and multi-metal solutions. FESEM-EDS analysis revealed the sequestration of multi-metals by bacterial cells and biofilm-EPS. FTIR analysis of bacterial EPS further ensured the interaction of functional groups such as –OH, –NH, and P=O with the metal ions. The maximum removal of Pb, Cr, and Cd by the bacterial biomass was observed at 37°C within 4 h of contact time at pH 6, and 4% salinity for Pb and Cr, and 6% salinity for Cd. The present study revealed that the marine bacterium P. chengduensis PPSS-4 can remove multi-metals, and this bacterium could be efficiently utilized for the remediation of heavy metals in the contaminated environment.

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

Access this article

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

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8
Figure 9

Similar content being viewed by others

References

  • Andreasen R, Li Y, Rehman Y, Ahmed M, Meyer R L and Sabri A N 2018 Prospective role of indigenous Exiguobacterium profundum PT 2 in arsenic biotransformation and biosorption by planktonic cultures and biofilms; J. Appl. Microbiol. 124(2) 431–443.

    Article  Google Scholar 

  • Ara A and Usmani J A 2015 Lead toxicity: A review; Interdisc. Toxicol. 8(2) 55–64.

    Article  Google Scholar 

  • Babák L, Šupinova P, Zichova M, Burdychova R and Vítová E 2013 Biosorption of Cu, Zn and Pb by thermophilic bacteria – effect of biomass concentration on biosorption capacity; Acta Univ; Agric. et Silvic. Mendelianae Brun. 60(5) 9–18.

    Article  Google Scholar 

  • Bai H, Han Y, Kang Y and Sun J 2013 Removal of Cu (II) and Fe (III) from aqueous solutions by dead sulfate reducing bacteria; Front. Chem. Sci. Eng. 7(2) 177–184.

    Article  Google Scholar 

  • Barakat M A 2011 New trends in removing heavy metals from industrial wastewater; Arab. J. Chem. 4(4) 361–377.

    Article  Google Scholar 

  • Black R, Sartaj M, Mohammadian A and Qiblawey H A 2014 Biosorption of Pb and Cu using fixed and suspended bacteria; J. Environ. Chem. Eng. 2(3) 1663–1671.

    Article  Google Scholar 

  • Burnett P G G, Daughney C J and Peak D 2006 Cd adsorption onto Anoxybacillus flavithermus: Surface complexation modeling and spectroscopic investigations; Geochim. Cosmochim. Acta 70(21) 5253–5269.

    Article  Google Scholar 

  • Chakraborty J and Das S 2014 Characterization and cadmium-resistant gene expression of biofilm-forming marine bacterium Pseudomonas aeruginosa JP-11; Environ. Sci. Pollut. Res. 21(24) 14,188–14,201.

    Article  Google Scholar 

  • Chakravarty R and Banerjee P C 2008 Morphological changes in an acidophilic bacterium induced by heavy metals; Extremophiles 12(2) 279–284.

    Article  Google Scholar 

  • Chien C C, Lin B C and Wu C H 2013 Biofilm formation and heavy metal resistance by an environmental Pseudomonas sp; Biochem. Eng. J. 78 132–137.

    Article  Google Scholar 

  • Choińska-Pulit A, Sobolczyk-Bednarek J and Łaba W 2018 Optimization of copper, lead and cadmium biosorption onto newly isolated bacterium using a Box-Behnken design; Ecotoxicol. Environ. Saf. 149 275–283.

    Article  Google Scholar 

  • CLSI W 2006 Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; 7th edn, Clinical and Laboratory Standards Institute Approve Standard M7–A7; CLSI, PA, USA.

    Google Scholar 

  • Congeevaram S, Dhanarani S, Park J, Dexilin M and Thamaraiselvi K 2007 Biosorption of chromium and nickel by heavy metal resistant fungal and bacterial isolates; J. Hazard. Mater. 146(1–2) 270–277.

    Article  Google Scholar 

  • Das S and Dash H R 2014 Microbial bioremediation: A potential tool for restoration of contaminated areas; In: Microbial Biodegradation and Bioremediation (ed.) S Das, Elsevier. USA, pp. 1–21.

  • Das S, Dash H R and Chakraborty J 2016 Genetic basis and importance of metal resistant genes in bacteria for bioremediation of contaminated environments with toxic metal pollutants; Appl. Microbiol. Biotechnol. 100(7) 2967–2984.

    Article  Google Scholar 

  • Dash H R, Basu S and Das S 2017 Evidence of mercury trapping in biofilm-EPS and mer operon-based volatilization of inorganic mercury in a marine bacterium Bacillus cereus BW-201B; Arch. Microbiol. 199(3) 445–455.

  • Dash H R, Mangwani N, Chakraborty J, Kumari S and Das S 2013 Marine bacteria: Potential candidates for enhanced bioremediation; Appl. Microbiol. Biotechnol. 97(2) 561–571.

    Article  Google Scholar 

  • De J, Ramaiah N and Vardanyan L 2008 Detoxification of toxic heavy metals by marine bacteria highly resistant to mercury; Mar. Biotechnol. 10(4) 471–477.

    Article  Google Scholar 

  • Devika L, Rajaram R and Mathivanan K 2013 Multiple heavy metal and antibiotic tolerance bacteria isolated from equatorial Indian Ocean; Int. J. Microbiol. Res. 4(3) 212–218.

    Google Scholar 

  • Dharmendra S, Kumar M R, Chinmayee A, Ranjan S D and Ranjan P C 2020 Assessment of marine sediment contamination and detection of their potential sources at Paradip port, East Coast of India; Res. J. Chem. Environ. 24 1–6.

    Google Scholar 

  • Edgell K 1988 USEPA method study 37: SW-846 method 3050 acid digestion of sediments, sludges, and soils (EPA Contract No. 68-03-3254); Environmental Monitoring Systems Lab., Cincinnati, OH.

  • Green-Ruiz C, Rodriguez-Tirado V and Gomez-Gil B 2008 Cadmium and zinc removal from aqueous solutions by Bacillus jeotgali: pH, salinity and temperature effects; Bioresour. Technol. 99(9) 3864–3870.

    Article  Google Scholar 

  • Gupta P and Diwan B 2017 Bacterial exopolysaccharide mediated heavy metal removal: A review on biosynthesis, mechanism and remediation strategies; Biotechnol. Rep. 13 58–71.

    Article  Google Scholar 

  • Halttunen T, Salminen S and Tahvonen R 2007 Rapid removal of lead and cadmium from water by specific lactic acid bacteria; Int. J. Food Microbiol. 114(1) 30–35.

    Article  Google Scholar 

  • Hosono T, Su C C, Delinom R, Umezawa Y, Toyota T, Kaneko S and Taniguchi M 2011 Decline in heavy metal contamination in marine sediments in Jakarta Bay, Indonesia due to increasing environmental regulations; Estuar. Coast. Shelf. Sci. 92(2) 297–306.

    Article  Google Scholar 

  • Jordjevic D, Wiedmann M and McLandsborough L A 2002 Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation; Appl. Environ. Microbiol. 68 2950–2958.

    Article  Google Scholar 

  • Joseph P 2009 Mechanisms of cadmium carcinogenesis; Toxicol. Appl. Pharm. 238(3) 272–279.

    Article  Google Scholar 

  • Kellen E, Zeegers M P, Den Hond E and Buntinx F 2007 Blood cadmium may be associated with bladder carcinogenesis: The Belgian case-control study on bladder cancer; Cancer Detect. Prev. 31(1) 77–82.

    Article  Google Scholar 

  • Kumar R, Singh R, Kumar N, Bishnoi K and Bishnoi N R 2009 Response surface methodology approach for optimization of biosorption process for removal of Cr (VI), Ni (II) and Zn (II) ions by immobilized bacterial biomass sp. Bacillus brevisChem. Eng. J. 146(3) 401–407.

  • Kumari S, Mangwani N and Das S 2017 Interaction of Pb (II) and biofilm associated extracellular polymeric substances of a marine bacterium Pseudomonas pseudoalcaligenes NP103; Spectrochim; Acta A. 173 655–665.

    Article  Google Scholar 

  • Kurniawan A and Yamamoto T 2013 Biofilm polymer for biosorption of pollutant ions; Procedia Environ; Sci. 17 179–187.

    Google Scholar 

  • Luo S, Li X, Chen L, Chen J, Wan Y and Liu C 2014 Layer-by-layer strategy for adsorption capacity fattening of endophytic bacterial biomass for highly effective removal of heavy metals; Chem. Eng. J. 239 312–321.

    Article  Google Scholar 

  • Mangwani N, Kumari S and Das S 2016 Bacterial biofilms and quorum sensing: Fidelity in bioremediation technology; Biotechnol. Genet. Eng. 32(1–2) 43–73.

    Article  Google Scholar 

  • Mangwani N, Shukla S K, Kumari S, Rao T S and Das S 2014 Characterization of Stenotrophomonas acidaminiphila NCW-702 biofilm for implication in the degradation of polycyclic aromatic hydrocarbons; J. Appl. Microbiol. 117(4) 1012–1024.

    Article  Google Scholar 

  • Matyar F, Kaya A and Dinçer S 2008 Antibacterial agents and heavy metal resistance in Gram-negative bacteria isolated from seawater, shrimp and sediment in Iskenderun Bay, Turkey; Sci. Total Environ. 407(1) 279–285.

    Article  Google Scholar 

  • Meliani A and Bensoltane A 2016 Biofilm-mediated heavy metals bioremediation in PGPR Pseudomonas; J. Bioremediat. Biodegrad. 7(370) 2.

    Google Scholar 

  • Mohapatra R K, Parhi P K, Pandey S, Bindhani B K, Thatoi H and Panda C R 2019 Active and passive biosorption of Pb (II) using live and dead biomass of marine bacterium Bacillus xiamenensis PbRPSD202: Kinetics and isotherm studies; J. Environ. Manag. 247 121–134.

    Article  Google Scholar 

  • Mohapatra R K, Parhi P K, Thatoi H and Panda C R 2017 Bioreduction of hexavalent chromium by Exiguobacterium indicum strain MW1 isolated from marine water of Paradip Port, Odisha, India; Chem. Ecol. 33(2) 114–130.

    Article  Google Scholar 

  • Moselhy K M, Shaaban M T, Ibrahim H A and Abdel-Mongy A S 2013 Biosorption of cadmium by the multiple-metal resistant marine bacterium Alteromonas macleodii ASC1 isolated from Hurghada Harbour, Red Sea; Arch. Sci. 66(2) 259–272.

    Google Scholar 

  • Mubashar K and Faisal M 2012 Uptake of toxic Cr(VI) by biomass of exo-polysaccharides producing bacterial strains; Afr. J. Microbiol. Res. 6(13) 3329–3336.

    Google Scholar 

  • Muñoz A J, Ruiz E, Abriouel H, Gálvez A, Ezzouhri L, Lairini K and Espínola F 2012 Heavy metal tolerance of microorganisms isolated from wastewaters: Identification and evaluation of its potential for biosorption; Chem. Eng. J. 210 325–332.

    Article  Google Scholar 

  • Naik M M, Pandey A and Dubey S K 2012 Biological characterization of lead-enhanced exopolysaccharide produced by a lead resistant Enterobacter cloacae strain P2B; Biodegradation 23(5) 775–783.

    Article  Google Scholar 

  • Nithya C, Gnanalakshmi B and Pandian S K 2011 Assessment and characterization of heavy metal resistance in Palk Bay sediment bacteria; Mar. Environ. Res. 71(4) 283–294.

    Article  Google Scholar 

  • Odokuma L O and Akponah E 2010 Effect of concentration and contact time on heavy metal uptake by three bacterial isolates; J. Environ. Chem. Ecotoxicol. 2(6) 84–97.

    Google Scholar 

  • Okeke B C 2008 Bioremoval of hexavalent chromium from water by a salt tolerant bacterium, Exiguobacterium sp. GS1; J. Ind. Microbiol. Biot. 35(12) 1571–1579.

    Article  Google Scholar 

  • Oves M, Khan M S and Zaidi A 2013 Biosorption of heavy metals by Bacillus thuringiensis strain OSM29 originating from industrial effluent contaminated north Indian soil; Saudi J. Biol. Sci. 20(2) 121–129.

    Article  Google Scholar 

  • Ozdemir G, Ceyhan N, Ozturk T, Akirmak F and Cosar T 2004 Biosorption of chromium (VI), cadmium (II) and copper (II) by Pantoea sp. TEM18; Chem. Eng. J. 102(3) 249–253.

    Article  Google Scholar 

  • Pan X, Liu Z, Chen Z, Cheng Y, Pan D, Shao J and Guan X 2014 Investigation of Cr (VI) reduction and Cr (III) immobilization mechanism by planktonic cells and biofilms of Bacillus subtilis ATCC-6633; Water Res. 55 21–29.

  • Pun R, Raut P and Pant B R 2013 Removal of chromium (VI) from leachate using bacterial biomass; Sci. World. 11(11) 63–65.

    Article  Google Scholar 

  • Puranik P R and Paknikar K M 1999 Biosorption of lead, cadmium, and zinc by Citrobacter strain MCM B-181: Characterization Studies; Biotechnol. Prog. 15(2) 228–237.

    Article  Google Scholar 

  • Rahimzadeh M R, Rahimzadeh M R, Kazemi S and Moghadamnia A A 2017 Cadmium toxicity and treatment: An update; Caspian J. Intern. Med. 8(3) 135.

    Google Scholar 

  • Rani A, Kumar A, Lal A and Pant M 2014 Cellular mechanisms of cadmium-induced toxicity: A review; Int. J. Environ. Health Res. 24(4) 378–399.

    Article  Google Scholar 

  • Rodríguez-Tirado V, Green-Ruiz C and Gómez-Gil B 2012 Cu and Pb biosorption on Bacillus thioparans strain U3 in aqueous solution: Kinetic and equilibrium studies; Chem. Eng. J. 181 352–359.

    Article  Google Scholar 

  • Sahmoune M N 2018 Performance of Streptomyces rimosus biomass in biosorption of heavy metals from aqueous solutions; Microchem. J. 141 87–95.

    Article  Google Scholar 

  • Salta M, Wharton J A, Blache Y, Stokes K R and Briand J F 2013 Marine biofilms on artificial surfaces: Structure and dynamics; Environ. Microbiol. 15(11) 2879–2893.

    Google Scholar 

  • Saranya K, Sundaramanickam A, Shekhar S, Meena M, Sathishkumar R S and Balasubramanian T 2018 Biosorption of multi-heavy metals by coral associated phosphate solubilising bacteria Cronobacter muytjensii KSCAS2; J. Environ. Manage. 222 396–401.

    Article  Google Scholar 

  • Sati M, Verma M and Rai J P N 2014 Biosorption of heavy metals from single and multimetal solutions by free and immobilized cells of Bacillus megaterium [J]; Int. J. Adv. Manuf. Tech. 2(6) 923–934.

    Google Scholar 

  • Selatnia A, Boukazoula A, Kechid N, Bakhti M Z, Chergui A and Kerchich Y 2004 Biosorption of lead (II) from aqueous solution by a bacterial dead Streptomyces rimosus biomass; Biochem. Eng. J. 19(2) 127–135.

    Article  Google Scholar 

  • Sethuraman P and Balasubramanian N 2010 Removal of Cr (VI) from aqueous solution using Bacillus subtilis, Pseudomonas aeruginosa and Enterobacter cloacae; Int. J. Eng. Sci. Technol. 2(6) 1811–1825.

    Google Scholar 

  • Stepanović S, Vuković D, Hola V, Bonaventura G D, Djukić S, Ćirković I and Ruzicka F 2007 Quantification of biofilm in microtiter plates: Overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci; Apmis. 115(8) 891–899.

    Article  Google Scholar 

  • Tchounwou P B, Yedjou C G, Patlolla A K and Sutton D J 2012 Heavy metal toxicity and the environment; In: Molecular, Clinical and Environmental Toxicology (ed.) Andreas L, Springer, pp. 133–164.

  • UNCTAD 2015 Review of Maritime Transport; In: UNCTAD/RMT/2015 Report, New York and Geneva.

  • Uslu G and Tanyol M 2006 Equilibrium and thermodynamic parameters of single and binary mixture biosorption of lead (II) and copper (II) ions onto Pseudomonas putida: Effect of temperature; J. Hazard. Mater. 135(1–3) 87–93.

    Article  Google Scholar 

  • Vijayaraghavan K and Yun Y S 2008 Bacterial biosorbents and biosorption; Biotechnol. Adv. 26(3) 266–291.

    Article  Google Scholar 

  • Vimalnath S and Subramanian S 2018 Studies on the biosorption of Pb (II) ions from aqueous solution using extracellular polymeric substances (EPS) of Pseudomonas aeruginosa; Colloid. Surface. B. 172 60–67.

    Article  Google Scholar 

  • Vimercati L, Gatti M F, Gagliardi T, Cuccaro F, Maria L D, Caputi A and Baldassarre A 2017 Environmental exposure to arsenic and chromium in an industrial area; Environ. Sci. Pollut. Res. 24 11,528–11,535.

    Article  Google Scholar 

  • Völkel S, Fröls S and Pfeifer F 2018 Heavy metal ion stress on Halobacterium salinarum R1 planktonic cells and biofilms; Front. Microbiol. 9 3157.

    Article  Google Scholar 

  • Vullo D L, Ceretti H M, Daniel M A, Ramírez S A and Zalts A 2008 Cadmium, zinc and copper biosorption mediated by Pseudomonas veronii 2E; Bioresour. Technol. 99(13) 5574–5581.

    Article  Google Scholar 

  • Wang T and Sun H 2013 Biosorption of heavy metals from aqueous solution by UV-mutant Bacillus subtilis; Environ. Sci. Pollut. Res. 20(10) 7450–7463.

    Article  Google Scholar 

  • Wierzba S and Latała A 2010 Biosorption lead (II) and nikel (II) from an aqueous solution by bacterial biomass; Pol. J. Chem. Technol. 12(3) 72–78.

    Article  Google Scholar 

  • Yue Z B, Li Q, Li C C, Chen T H and Wang J 2015 Component analysis and heavy metal adsorption ability of extracellular polymeric substances (EPS) from sulfate reducing bacteria; Bioresour. Technol. 194 399–402.

    Article  Google Scholar 

  • Zampieri B D B, Pinto A B, Schultz L, de Oliveira M A and de Oliveira A J F C 2016 Diversity and distribution of heavy metal-resistant bacteria in polluted sediments of the Araça Bay, São Sebastião (SP), and the relationship between heavy metals and organic matter concentrations; Microb. Ecol. 72(3) 582–594.

    Article  Google Scholar 

  • Zhou W, Ma Y, Zhou J and Zhang Y 2013 Bio-removal of cadmium by growing deep-sea bacterium Pseudoalteromonas sp. SCSE709-6; Extremophiles 17(5) 723–731.

    Article  Google Scholar 

  • Zouboulis A I, Loukidou M X and Matis K A 2004 Biosorption of toxic metals from aqueous solutions by bacteria strains isolated from metal-polluted soils; Process Biochem. 39(8) 909–916.

    Article  Google Scholar 

Download references

Acknowledgements

The authors acknowledge NIT Rourkela, Odisha, for providing the research facility. MP acknowledge the Department of Science & Technology, Govt. of India, for the INSPIRE Award (No. DST/INSPIRE Fellowship/2017/IF170195) for the doctoral study.

Author information

Authors and Affiliations

Authors

Contributions

MP executed the experiments and drafted the manuscript. SD conducted the field visit for sampling, designed the research, secured internal funding, supervised the experiments and finalized the manuscript.

Corresponding author

Correspondence to Surajit Das.

Additional information

Communicated by Maripi Dileep

This article is part of the topical collection: Advances in Coastal Research.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Priyadarshanee, M., Das, S. Bioremediation potential of biofilm forming multi-metal resistant marine bacterium Pseudomonas chengduensis PPSS-4 isolated from contaminated site of Paradip Port, Odisha. J Earth Syst Sci 130, 125 (2021). https://doi.org/10.1007/s12040-021-01627-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12040-021-01627-w

Keywords

Navigation