Abstract
Pseudomonas aeruginosa, an opportunistic human pathogen, is a major health concern as it grows as a biofilm and evades the host’s immune defenses. Formation of biofilms on catheter and endotracheal tubes demands the development of biofilm-preventive (anti-biofilm) approaches and evaluation of nanomaterials as alternatives to antibiotics. The present study reports the successful biosynthesis of tellurium nanorods using cell lysate of Haloferax alexandrinus GUSF-1 (KF796625). The black particulate matter had absorption bands at 0.5 and 3.6 keV suggestive of elemental tellurium; showed x-ray diffraction peaks at 2θ values 24.50°, 28.74°, 38.99°, 43.13°, 50.23° and displayed a crystallite size of 36.99 nm. The black nanorods of tellurium were an average size of 40 nm × 7 nm, as observed in transmission electron microscopy. To our knowledge, the use of cell lysate of Haloferax alexandrinus GUSF-1 (KF796625) as a green route for the biosynthesis of tellurium nanorods with a Pseudomonas aeruginosa biofilm inhibiting capacity is novel to haloarchaea. At 50 µg mL−1, these tellurium nanorods exhibited 75.03% in-vitro reduction of biofilms of Pseudomonas aeruginosa ATCC 9027, comparable to that of ciprofloxacin, which is used in treatment of Pseudomonas infections. Further, the observed ability of these nanoparticles to inhibit the formation of Pseudomonas biofilms is worthy of future research perusal.
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References
Alvares JJ, Furtado IJ (2018) Extremely halophilic Archaea and Eubacteria are responsible for free radical scavenging activity of solar salts of Goa—India. Global J Biosci Biotechnol 7(2):242–254
Alvares JJ, Furtado IJ (2021) Characterization of multicomponent antioxidants from Haloferax alexandrinus GUSF-1 (KF796625). 3 Biotech 11:58. https://doi.org/10.1007/s13205-020-02584-9
Baesman SM, Bullen TD, Dewald J, Zhang D, Curran S, Islam FS, Beveridge TJ, Oremland RS (2007) Formation of tellurium nanocrystals during anaerobic growth of bacteria that use Te oxyanions as respiratory electron acceptors. Appl Environ Microbiol 73(7):2135–2143. https://doi.org/10.1128/AEM.02558-06
Barabadi H, Honary S, Ebrahimi P, Mohammadi MA, Alizadeh A, Naghibi F (2014) Microbial mediated preparation, characterization and optimization of gold nanoparticles. Braz J Microbiol 45(4):1493–1501. https://doi.org/10.1590/s1517-83822014000400046
Barabadi H, Kobarfard F, Vahidi H (2018) Biosynthesis and characterization of biogenic tellurium nanoparticles by using Penicillium chrysogenum PTCC 5031: a novel approach in gold biotechnology. Iran J Pharm Res 17(Suppl2):87–97
Basnayake RST, Bius JH, Akpolat OM, Chasteen TG (2001) Production of dimethyl telluride and elemental tellurium by bacteria amended with tellurite or tellurate. Appl Organomet Chem 15(6):499–510
Borghese R, Borsetti F, Foladori P, Ziglio G, Zannoni D (2004) Effects of the metalloid oxyanion tellurite (TeO32−) on growth characteristics of the phototrophic bacterium Rhodobacter capsulatus. Appl Environ Microbiol 70(11):6595–6602. https://doi.org/10.1128/AEM.70.11.6595-6602.2004
Calderón IL, Arenas FA, Pérez JM, Fuentes DE, Araya MA, Saavedra CP, Tantaleán JC, Pichuantes SE, Youderian PA, Vásquez CC (2006) Catalases are NAD(P)H-dependent tellurite reductases. PLoS ONE 1(1):e70. https://doi.org/10.1371/journal.pone.0000070
Coates J (2000) Interpretation of infrared spectra, a practical approach. In: Meyers RA (ed) Encyclopedia of analytical chemistry. Wiley, New York, pp 10815–10837
Gómez-Gómez B, Arregui L, Serrano S, Santos A, Pérez-Corona T, Madrid Y (2019) Selenium and tellurium-based nanoparticles as interfering factors in quorum sensing-regulated processes: violacein production and bacterial biofilm formation. Metallomics 11(6):1104–1114. https://doi.org/10.1039/c9mt00044e
Honary S, Ghajar K, Khazaeli P, Shalchian P (2011) Preparation, characterization and antibacterial properties of silver-chitosan nanocomposites using different molecular weight grades of chitosan. Trop J Pharm Res 10:69–74
Johnson LR (2008) Micro colony and biofilm formation as a survival strategy for bacteria. J Theor Biol 251:24–34. https://doi.org/10.1016/j.jtbi.2007.10.039
Klonowska A, Heulin T, Vermeglio A (2005) Selenite and tellurite reduction by Shewanella oneidensis. Appl Environ Microbiol 71:5607–5609. https://doi.org/10.1128/AEM.71.9.5607-5609.2005
Lemire JA, Harrison JJ, Turner RJ (2013) Antimicrobial activity of metals: mechanisms, molecular targets and applications. Nat Rev Microbiol 11(6):371–384. https://doi.org/10.1038/nrmicro3028
Lin ZH, Lee CH, Chang HY, Chang HT (2012) Antibacterial activities of tellurium nanomaterials. Chem Asian J 7(5):930–934. https://doi.org/10.1002/asia.201101006
Lloyd-Jones G, Osborne M, Ritchie DA, Strike P, Hobman JL, Brown NL, Rouch DA (1994) Accumulation and intracellular fate of tellurite-resistant Escherichia coli: a model for mechanism of resistance. FEMS Microbiol Lett 118:113–120
Naik S, Furtado I (2019) Formation of Rhodochrosite by Haloferax alexandrinus GUSF-1. J Clust Sci 30:1435–1441. https://doi.org/10.1007/s10876-019-01586-9
Nakanishi K, Solomon PA (1977) Infrared absorption spectroscopy, 2nd edn. Holden-Day, San Francisco
O’Toole GA (2011) Microtiter dish biofilm formation assay. J vis Exp 47:2437. https://doi.org/10.3791/2437
Ottosson LG, Logg K, Ibstedt S, Sunnerhagen P, Käll M, Blomberg A, Warringer J (2010) Sulfate assimilation mediates tellurite reduction and toxicity in Saccharomyces cerevisiae. Eukaryot Cell 9(10):1635–1647. https://doi.org/10.1128/EC.00078-10
Patil S, Fernandes J, Tangsali RB, Furtado I (2014) Exploitation of Haloferax alexandrinus for biogenic synthesis of silver nanoparticles antagonistic to human and lower mammalian pathogens. J Clust Sci 25:423–433. https://doi.org/10.1007/s10876-013-0621-0
Radzig MA, Nadtochenko VA, Koksharova OA, Kiwi J, Lipasova VA, Khmel IA (2013) Antibacterial effects of silver nanoparticels on gram-negative bacteria: influence on the growth and biofilm formation, mechanisms of action. Colloids Surf B 102:300–306. https://doi.org/10.1016/j.colsurfb.2012.07.039
Raghavan TM, Furtado I (2004) Occurrence of extremely halophilic archaea in sediments from the continental shelf of west coast of India. Curr Sci India 86:1065–1067
Raghavan TM, Furtado I (2005) Expression of carotenoid pigments of haloarchaeal cultures exposed to aniline. Environ Toxicol 20(2):165–169. https://doi.org/10.1002/tox.20091
Rasamiravaka T, Labtani Q, Duez P, El Jaziri M (2015) The formation of biofilms by pseudomonas aeruginosa: a review of the natural and synthetic compounds interfering with control mechanisms. BioMed Res Int 2015:759348. https://doi.org/10.1155/2015/759348
Sequeira F (1992) Microbiological study of salt pans of Goa. Master of Science dissertation. Goa University, India
Shakibaie M, Adeli-Sardou M, Mohammadi-Khorsand T, Zeydabadi-Nejad M, Amirafzali E, Amirpour-Rostami S, Ameri A, Forootanfar H (2017) Antimicrobial and antioxidant activity of the biologically synthesized tellurium nanorods; a preliminary in vitro study. Iran J Biotechnol 15(4):268–276. https://doi.org/10.15171/ijb.1580
Srey S, Jahid IK, Ha S-D (2013) Biofilm formation in food industries: a food safety concern. Food Control 31(2):572–585. https://doi.org/10.1016/j.foodcont.2012.12.001
Subramanian R, Subbramaniyan P, Raj V (2013) Antioxidant activity of the stem bark of Shorea roxburghii and its silver reducing power. Springerplus 2:28. https://doi.org/10.1186/2193-1801-2-28
Srivastava P, Nikhil EVR, Braganca JM, Kowshik M (2015) Anti-bacterial TeNPs biosynthesized by haloarcheaon Halococcus salifodinae BK3. Extremophiles 19:875–884. https://doi.org/10.1007/s00792-015-0767-9
Summers AO, Jacoby GA (1977) Plasmid-determined resistance to tellurium compounds. J Bacteriol 129:276–281
Taylor DE (1999) Bacterial tellurite resistance. Trends Microbiol 7:111–115
Tremaroli V, Fedi S, Zannoni D (2007) Evidence for a tellurite-dependent generation of reactive oxygen species and absence of a tellurite-mediated adaptive response to oxidative stress in cells of Pseudomonas pseudoalcaligenes KF707. Arch Microbiol 187(2):127–135. https://doi.org/10.1007/s00203-006-0179-4
Wagner VE, Iglewski BH (2008) P. aeruginosa biofilms in CF infection. Clin Rev Allergy Immunol 35:124–134. https://doi.org/10.1007/s12016-008-8079-9
Wu M, Li X (2015) Klebsiella pneumoniae and Pseudomonas aeruginosa. In: Tang Y-W, Sussman M, Liu D, Poxton I, Schwartzman J (eds) Molecular medical microbiology, vol 87, 2nd edn. Academic Press, New York, pp 1547–1564
Yurkov V, Jappe J, Vermeglio A (1996) Tellurite resistance and reduction by obligately aerobic photosynthetic bacteria. Appl Environ Microbiol 62(11):4195–4198
Zare B, Faramarzi MA, Sepehrizadeh Z, Shakibaie M, Rezaie S, Shahverdi AR (2012) Biosynthesis and recovery of rod-shaped tellurium nanoparticles and their bactericidal activities. Mater Res Bull 47(11):3719–3725. https://doi.org/10.1016/J.Materresbull.2012.06.034
Zonaro E, Lampis S, Turner RJ, Qazi SJS, Vallini G (2015) Biogenic selenium and tellurium nanoparticles synthesized by environmental microbial isolates efficaciously inhibit bacterial planktonic cultures and biofilms. Front Microbiol 6(584). https://doi.org/10.3389/fmicb.2015.00584
Acknowledgements
The authors wish to thank IIT-Bombay, for the TEM facility, National Institute of Oceanography, Goa, for the XRD profiling, University Science Instrumentation Centre (USIC), Goa University, for SEM-EDX and Department of Chemistry, Goa University, for FT-IR analysis.
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Authors dedicate the paper to Prof. Suneela Mavinkurve, former Head, Microbiology and Dean, Faculty of Life Sciences and Environment, Goa University-India.
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Alvares, J.J., Furtado, I.J. Anti-Pseudomonas aeruginosa biofilm activity of tellurium nanorods biosynthesized by cell lysate of Haloferax alexandrinus GUSF-1(KF796625). Biometals 34, 1007–1016 (2021). https://doi.org/10.1007/s10534-021-00323-y
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DOI: https://doi.org/10.1007/s10534-021-00323-y