Biofilm Formation by the Hexavalent Chromium Removing Strain Streptococcus salivarius: in Vitro Approach on Abiotic Surfaces

Document Type : Original Research Paper

Authors

1 1. Applied Microbiology Laboratory, Faculty of Nature and Life Sciences, University A. Mira, Bejaia, Algeria 2. Department of Applied Microbiology and Food Science, University Mohamed Seddik Benyahia, Jijel, Algeria

2 Laboratory of Molecular Toxicology, University Mohamed Seddik Benyahia, Jijel, Algeria

3 Department of Applied Microbiology and Food Science, University Mohamed Seddik Benyahia, Jijel, Algeria Laboratory of Molecular Toxicology, University Mohamed Seddik Benyahia, Jijel, Algeria

4 Applied Microbiology Laboratory, Faculty of Nature and Life Sciences, University A. Mira, Bejaia, Algeria

5 Department of Applied Microbiology and Food Science, University Mohamed Seddik Benyahia, Jijel, Algeria Laboratory of Biotechnology, Environment and Health, University Mohamed Seddik Benyahia, Jijel, Algeria

Abstract

In this study, a strain of lactic acid bacteria Streptococcus salivarius was studied for its capacity to remove hexavalent chromium (Cr (VI)) from a liquid medium and to form biofilm. Both properties are useful for using the strain in bioremediation of metal-contaminated effluents. For biofilm formation capacity, three methods were used: the tube method (TM), the Congo red agar method (CRA) and adherence to polystyrene tissue culture plate method (TCP). S. salivarius, showed a positive-biofilm and a correlation between the three methods was noted. The bacterial surface hydrophobicity was studied using the microbial adhesion to solvents method (MATS). On AISI-316 L stainless steel, the strain with a hydrophobic surface showed a good adhesion on this support after 18 h incubation. The colonization of the supports and the biofilms formation by the bacterial cell was observed using scanning electron microscopy (SEM). The minimum inhibitory concentration (MIC) of Cr(VI) on S. salivarius was determined on MRS broth, it was relatively high and equal to 400mg/l. In addition, it displayed a remarkable capacity to reduce Cr(VI) concentration on the liquid medium containing initially 50 mg/l of Cr(VI) ; the percent removal rate was equal to approximately 42% after 72 h of incubation at 37 °C. In addition to its GRAS status, the obtained results suggested that S. salivarius could be successfully used in Cr(VI) bioremediation.

Keywords


Arena, M.P., Capozzi, V., Spano, G. and Fiocco, D. (2017) The potential of lactic acid bacteria to colonize biotic and abiotic surfaces and the investigation of their interactions and mechanisms.
Pollution, 6(2): 295-304, Spring 2020
303
Appl. Microbiol. Biotechnol., 101; 2641–2657. https://doi.org/10.1007/s00253-017-8182-z
Bellon-Fontaine, M. N. and Cerf, O. (1990). Experimental determination of spreading pressure in solid and liquid vapor systems. J. Adhes. Sci. Technol., 4; 475–480.
Bellon-Fontaine, M. N., Rault, J. and Van Oss, C. J. (1996). Microbial adhesion to solvents: a novel method to determine the electron donor/electron acceptor or Lewis acid-base properties of microbial cells. Colloids Surfaces B, 7; 47–53.
Bhakta, J. N., Ohnishi, K., Munekage, Y. and Iwasaki, K. (2012). Characterization of lactic acid bacteria‐based probiotics as potential heavy metal sorbents. J. Appl. Microbiol., 112(6); 1193-1206. https://doi.org/10.1111/j.1365-2672.2012.05284.x
Bhattacharya, A. and Gupta, A. (2013). Evaluation of Acinetobacter sp B9 for Cr (VI) resistance and detoxification with potential application in bioremediation of heavy-metals-rich industrial wastewater. Environ. Sci. Pollut. Res., 20(9); 6628–6637.
Bilgiç, A., and Çimen, A. (2019). Removal of chromium (VI) from polluted wastewater by chemical modification of silica gel with 4-acetyl-3-hydroxyaniline. RSC Advances, 9(64); 37403-37414.
Briandet, R., Meylheuc, T., Maher, C. and Bellon-Fontaine, M.N. (1999). Listeria monocytogenes Scott A: cell surface charge, hydrophobicity and electron donor and acceptor characteristics under different environmental growth conditions. J. Appl. Environ. Microbiol., 65; 5328-5333.
Burgain, J., Scher, J., Francius, G. and Borges, F. (2014). Lactic acid bacteria in dairy food: Surface characterization and interactions with food matrix components. Adv. Colloid Interface Sci., 213; 21–35. https://doi.org/10.1016/j.cis.2014.09.005
Caggianiello, G., Kleerebezem, M. and Spano, G. (2016). Exopolysaccharides produced by lactic acid bacteria: from health-promoting benefits to stress tolerance mechanisms. Appl. Microbiol. Biotechnol., 100; 3877–3886. https://doi.org/10.1007/s00253-016-7471-2
Chavant, P., Martinie, B., Meylheuc, T., and Bellon-Fontaine, M.N. (2001). Listeria monocytogenes LO28: Surface physicochemical properties and ability to form biofilms at different temperatures and growth phases. Appl. Environ. Microbiol., 68; 728–737.
Christensen, G. D., Simpson, W. A., Bisno, A. L. and Beachey, E. H. (1982). Adherence of slime–producing strains of Staphylococcus epidermidis to smooth surfaces. Infect. Immun., 37; 318–26.
Etesami, H. (2018). Bacterial mediated alleviation of heavy metal stress and decreased accumulation of metals in plant tissues: mechanisms and future prospects. Ecotoxicol. Environ. Saf., 147; 175-191. https://doi.org/10.1016/j.ecoenv.2017.08.032
Fleming, H. C. and Wingender, J. (2001). Relevance of microbial extracellular polymeric substances (EPSs) – Part I: Structural and ecological aspects. Water Sci. Technol., 43; 1-8. https://doi.org/10.2166/wst.2001.0326
Fosso-Kankeu, E., Mulaba-Bafubiandi, A. F. (2014). Implication of plants and microbial metalloproteins in the bioremediation of polluted waters: a review. Phys. Chem. Earth, 67; 242-252.
Guo, H., Luo, S., Chen, L. and Xiao, X. (2010). Bioremediation of heavy metals by growing hyperaccumulator endophytic bacterium Bacillus spL14. Bioresour. Technol., 101; 8599–8605. https://doi.org/10.1016/j.biortech.2010.06.085
Hassen, A., Saidi, N., Cherif, M. and Boudabous, A. (1998). Resistance of environmental bacteria to heavy metals. Bioresour. Technol., 64; 7-15.
Kinoshita, H., Sohma, Y., Ohtake, F. and Ishida, M. (2013). Biosorption of heavy metals by lactic acid bacteria and identification of mercury binding protein. Res. Microbiol., 164(7); 701-709. https://doi.org/10.1016/j.resmic.2013.04.004
Leriche, V. and Carpentier, B. (2000). Limitation of adhesion and growth of Listeria monocytogenes on stainless steel surfaces by Staphylococcus sciuri biofilms. J. Appl. Microbiol., 88; 594–605. https://doi.org/10.1046/j.1365-2672.2000.01000.x
Lewis, S. J., Gilmour, A., Fraser, T. W. and Mccall, R. D. (1987). Scanning electron microscopy of soiled stainless steel inoculated with single bacterial cells. Int. J. Food Microbiol., 4; 279–284. https://doi.org/10.1016/0168-1605(87)90002-X
Mathur, T., Singhal, S., Khan, S. and Upadhyay, D.J. (2006). Detection of biofilm formation among the clinical isolates of Staphylococci: an evaluation of three different screening methods. Indian J. Medical Microbiol., 24; 25-9. http://dx.doi.org/10.4103/0255-0857.19890
Monsan, P., Bozonn, E. T., Albenn, E. C. and Joucla, G. (2001). Homopolysaccharides from lactic acid bacteria. Int. Dairy J., 11; 675. https://doi.org/10.1016/S0958-6946(01)00113-3
Mozes, N., Léonard, A. J. and Rouxhet, P. G. (1988). On the relations between the elemental surface composition of yeasts and bacteria and their
Ait-Meddour A., et al.
Pollution is licensed under a "Creative Commons Attribution 4.0 International (CC-BY 4.0)"
304
charge and hydrophobicity. Biochim. Biophys. Acta Biomembr., 945; 324-334. https://doi.org/10.1016/0005-2736(88)90495-6
Ncibi, M. C., Mahjoub, B. and Seffen, M. (2008). Study of the biosorption of chromium (VI) by a Mediterranean biomass: Posidonia oceanica (L) delile (Paper in French). Rev. Sci. Eau, 21(4); 441-449. https://doi.org/10.7202/019166ar
Neu, T.R., Swernhone, G.D.W. and Lawrence, J.R. (2001). Assessment of lectin binding analysis for in situ detection of glycoconjugates in biofilms systems. Microbiol., 147; 299–313. http://dx.doi.org/10.1099/00221287-147-2-299
O’toole, G. and Kolter, R. (1998). Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol., 30; 295-304.
Ozturk, S. and Aslim, B. (2008). Relationship between chromium (VI) resistance and extracellular polymeric substances (EPS) concentration by some cyanobacterial isolates. Environ. Sci. Pollut. Res., 15(6); 478-480. https://doi.org/10.1007/s11356-008-0027-y
Ozturk, S., Kaya, T., Aslim, B. and Tan, S. (2012). Removal and reduction of chromium by Pseudomonas spp. and their correlation to rhamnolipid production. J. Hazard. Mater., 231; 64–69. https://doi.org/10.1016/j.jhazmat.2012.06.038
Pieniz, S., de Moura, T. M., Vaz Cassenego, A. P. and Andreazza, R. (2015). Evaluation of resistance genes and virulence factors in a food isolated Enterococcus durans with potential probiotic effect. Food Control, 51; 49-54. https://doi.org/10.1016/j.foodcont.2014.11.012
Priya, K., Roja, K., Priya, A. S. and Arvind, S. (2013). Detoxification and bioremediation of chromium (VI) from the tannery effluents. Int. J. ChemTech Res., 5; 2177-2185.
Rafaat, M. Elsanhoty, I.A. Al-Turki, and Ramadan, M.F. (2016). Application of lactic acid bacteria in removing heavy metals and aflatoxin B1 from contaminated water. Water Sci. Technol., 74 (3); 625–638. https://doi.org/10.2166/wst.2016.255
Rizzi, V., D'agostino, F., Fini, P. and Semeraro, P. (2017). An interesting environmental friendly cleanup: The excellent potential of olive pomace for disperse blue adsorption/desorption from wastewater. Dyes Pigments, 140; 480-490.
Schut, S., Zauner, S., Hampel, G., Kӧnig, H. and Claus, H. (2011). Biosorption of copper by wine relevant lactobacilli. Int. J. Food Microbiol., 145; 126-131.
Sedláček, I., Švec, P. and Kukletová, M. (2010). Slime production and adhesion properties among Lactobacilli isolated from dental caries. In Proceedings of the 12th – International Conference on Culture Collections (ICCC12).
Shakoori, A. R., Makhdoom, M. and Haq, R. U. (2000). Hexavalent chromium reduction by a dichromate resistant Gram-positive bacterium isolated from effluents of tanneries. Appl. Microbiol. Biotechnol., 53(3); 348–351. https://doi.org/10.1007/s002530050033
Srinath, T., Verma, T., Ramteke, P.W. and Garg, S.K. (2002). Chromium (VI) biosorption and bioaccumulation by chromate resistant bacteria. Chemosphere, 48; 427–435.
Staudt, C., Horn, H., Hempel, D. C. and Neu, T. R. (2004). Volumetric measurements of bacterial cells and extracellular polymeric substance glycoconjugates in biofilms. Biotechnol. Bioeng., 88; 585–592. https://doi.org/10.1002/bit.20241
Stepanovic, S., Vukovic, D., Dakic, I. and Savic, B. (2000). A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J. Microbiol. Methods, 40; 175–179.
Sutherland, I. W. (2001). Microbial polysaccharides from Gram-negative bacteria. Int. Dairy J., 11; 663-674. https://doi.org/10.1016/S0958-6946(01)00112-1.
Whitfield, C. and Roberts, I. S. (1999). Structure, assembly and regulation of expression of capsules in Escherichia coli. Mol. Microbiol., 31; 1307-1319.
Zhou, Y. F. and Haynes, R. J. (2010). Sorption of heavy metals by inorganic and organic components of solid wastes: significance to use of wastes as low-cost adsorbents and immobilizing agents. Crit. Rev. Environ. Sci. Technol., 40(11); 909-977.