Abstract
Silver sulfide nanoparticles stable in aqueous solutions were obtained in presence of the cells of the bacterium Shewanella oneidensis MR-1 in aqueous solution containing an equimolar mixture of AgNO3 and Na2S2O3. Proteins absorbed on the surface of Ag2S nanoparticles were identified for the first time by MALDITOF/TOF. Among these proteins, multiheme cytochromes MtrC and OmcA, as well as the MtrB membrane porin, which forms a complex on the outer cell membrane, were detected. It was shown that an insoluble precipitate consisting of agglomerated Ag2S nanoparticles with a wide size distribution was formed in the absence of the cells. The role of the detected proteins in the mechanism of the formation and stabilization of the Ag2S nanoparticles in the studied system is discussed.
Similar content being viewed by others
Abbreviations
- IR:
-
infrared
- TEM:
-
transmission electron microscopy
- LB medium:
-
Luria–Bertani medium
- EPS:
-
extracellular polymeric substances
- QD:
-
quantum dots
References
Zhang, Y., Zhang, Y.J., Hong, G.S., He, W., Zhou, K., Yang, K., Li, F., Chen, G.C., Liu, Z., Dai, H.J., and Wang, Q.B., Biodistribution, pharmacokinetics and toxicology of Ag2S near-infrared quantum dots in mice, Biomaterials, 2013, vol. 34, pp. 3639–3646.
Li, C., Zhang, Y., Wang, M., Zhang, Y., Chen, G., Li, L., Wu, D., and Wang, Q., In vivo real-time visualization of tissue blood flow and angiogenesis using Ag2S quantum dots in the NIR-II window, Biomaterials, 2014, vol. 35, pp. 393–400.
Trandafilovic, L.V., Djokovic, V., Bibic, N., and Georges, M.K., Confined growth of Ag2S semiconductor nanocrystals in the presence of PDMAEMA-co-AA polyampholyte copolymer, Mater. Lett., 2010, vol. 64, pp. 1123–1126.
Narayanan, K. and Sakthevel, N., Biological synthesis of metal nanoparticles by microbes, Adv. Colloid Interface Sci., 2010, vol. 156, pp. 1–13.
Bansal, V., Bharde, A., Ramanathan, R., and Bhargava, S., Inorganic materials using “unusual” microorganisms, Adv. Colloid Interface Sci., 2012, vol. 179-182, no. (1), pp. 150–168.
Suresh, A.K., Suresh, A.K., Pelleter, D.A., Wang, W., Broich, M.L., Ji-Won Moon, Gu, B., Allison, D.P., Joy, D.C., Phelps, T.J., and Doktycz, M.J., Biofabrication of discrete spherical gold nanoparticles using the metal-reducing bacterium Shewanella oneidensis, Acta Biomat., 2011, vol. 7, pp. 2148–2152.
Ng, C.K., Sivakumar, K., Liu, X., Madhaiyan, M., Ji, L., Yang, L., Tang, C., Song, H., Kjelleberg, S., and Cao, B., Influence of outer membrane c-type cytochromes on particle size and activity of extracellular nanoparticles produced by Shewanella oneidensis, Biotechnol. Bioeng., 2013, vol. 110, pp. 1831–1837.
Suresh, A.K., Doktycz, M.J., Wang, W., Moon, Ji-W., Gu, B., Meyer, H.M., Hensley, D.K., Allison, D.P., Phelps, T.J., and Pelletier, D.A., Monodispersed biocompatible silver sulfide nanoparticles: facile extracellular biosynthesis using gamma-proteobacterium Shewanella oneidensis, Acta Biomat., 2011, vol. 7, pp. 4253–4258.
Debabov, V.G., Voeikova, T.A., Shebanova, A.S., Shaitan, K.V., Emel’yanova, L.K., Novikova, L.M., and Kirpichnikov, M.P., Bacterial synthesis of silver sulfide nanoparticles, Ross. Nanotekhnol., 2013, vol. 8, nos. 3–4, pp. 269–276.
Ng, C.K., Tan, T.K.C., Song, H., and Cao, B., Reductive formation of palladium nanoparticles by Shewanella oneidensis: role of outer membrane cytochromes and hydrogenases, RSC Advances, 2013, vol. 3, pp. 22498–22503.
Burgos, W.D., Mcdonongh, J.T., Senko, J.M., Zhang, G., Dohnalkova, A.C., Kekky, S.D., Gorby, Y., and Kenner, K.M., Characterization of uraninite nanoparticles produced by Shewanella oneidensis MR-1, Geochim. Cosmochim. Acta, 2008, vol. 72, pp. 4901–4915.
Ross, D.E., Flynn, J.M., Baron, D.B., Gralnick, J.A., and Bond, D.R., Towards electrosynthesis in Shewanella: energetics of reversing the Mtr pathway for reductive metabolism, Plos One, 2011, vol. 6, no. 2, pp. 1–9.
Burns, J.L. and Dichristina, T.J., Anaerobic respiration of elemental sulfur and thiosulfate by Shewanella oneidensis MR-1 requires psrA, a homolog of the phsA gene of Salmonella enterica serovar typhimurium LT2, Appl. Environ. Microbiol., 2009, vol. 75, no. 16, pp. 5209–5217.
Xiao, X., Ma, X.B., Yuan, H., Liu, P.C., Lei, Y.B., Xu, H., Du, D.L., Sun, J.F., and Feng, Y.J., Photocatalytic properties of zinc sulfide nanocrystals biofabricated by metal-reducing bacterium Shewanella oneidensis MR-1, J. Hazardous Mat., 2015, vol. 288, pp. 134–139.
Ivanov, Y.D., Pleshakova, T.O., Krohin, N.V., Kaysheva, A.L., Usanov, S.A., and Archakov, A.I., Registration of the protein with compact disc, Biosens. Bioelectron., 2013, vol. 43, pp. 384–390.
Ivanov, Y.D., Bukharina, N.S., Pleshakova, T.O., Frantsuzov, P.A., Andreeva, E.Y., Kaysheva, A.L., Zgoda, V.G., Izotov, A.A., Pavlova, T.I., and Ziborov, V.S., Atomic force microscopy fishing and mass spectrometry identification of gp120 on immobilized aptamers, Int. J. Nanomed., 2014, vol. 9, pp. 4659–4670.
Ripan, R. and Chetyanu, I., Neorganicheskaya khimiya. Khimiya metallov (Inorganic Chemistry. Chemistry of Metals), Moscow: Mir, 1972, vol. 2.
Shebanova, A.C., Voeikova, T.A., Egopov, A.V., Novikova, L.M., Kpect’yanova, I.N., Emel’yanova, L.K., Debabov, V.G., Kippichnikov, M.P., and Shaitan, K.V., Biophysics (Moscow), 2014, vol. 59, no. 3, pp. 408–414.
Shi, L., Chen, B., Wang, Z., Elias, D.A., Mayer, M.U., Gorby, Y.A., Ni, S., Lower, B.H., Kennedy, D.W., and Wunschel, D.S, Isolation of a high-affinity functional protein complex between OmcA and MtrC: two outer membrane decahemec-type cytochromes of Shewanella oneidensis MR-1, J. Bacteriol., 2006, vol. 188, no. 13, pp. 4705–4714.
Xiong, Y.B., Fredrickson, J.K., Romine, M.F., Marshall, M.J., Lipton, M.S., and Beyenal, H., HRCR-1 biofilms: characterization by infrared spectroscopy and proteomics, Environ. Microbiol., 2011, vol. 13, no. 4, pp. 1018–1031.
Mukherjee, P., Ahmad, A., Mandal, D., Senapati, S., Sainkar, S.R., Khan, M.I., Parischa, R., Ajayakumar, P.V., Alam, M., Kumar, R., and Sastry, M., Fungus-mediated synthesis of silver nanoparticles and their immobilization in the mycelial matrix: a novel biological approach to nanoparticle synthesis, Nano Lett., 2001, vol. 1, pp. 515–519.
Mukherjee, P., Senapati, S., Mandal, D., Ahmad, A., Khan, M.I., Kumar, R., and Sastry, M., Extracellular synthesis of gold nanoparticles by the fungus Fusarium oxysporum, Chembiochem., 2002, vol. 3, no. 5, pp. 461–463.
León-Velázquez, M.S., Irizarry, R., and Castro-Rosario, M.E., Nucleation and growth of silver sulfide nanoparticles, J. Phys. Chem. C, 2010, vol. 114, no. 13, pp. 5839–5849.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © T.A. Voeikova, A.S. Shebanova, Yu.D. Ivanov, A.L. Kaysheva, L.M. Novikova, O.A. Zhuravliova, V.V. Shumyantseva, K.V. Shaitan, M.P. Kirpichnikov, V.G. Debabov, 2015, published in Biotekhnologiya, 2015, No. 5, pp. 41–48.
Rights and permissions
About this article
Cite this article
Voeikova, T.A., Shebanova, A.S., Ivanov, Y.D. et al. The role of proteins of the outer membrane of Shewanella oneidensis MR-1 in the formation and stabilization of silver sulfide nanoparticles. Appl Biochem Microbiol 52, 769–775 (2016). https://doi.org/10.1134/S0003683816080081
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0003683816080081