Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-20T15:31:09.752Z Has data issue: false hasContentIssue false
  • English
  • Français

Intracellular Biosynthesis of Fluorescent CdSe Quantum Dots in Bacillus subtilis: A Strategy to Construct Signaling Bacterial Probes for Visually Detecting Interaction Between Bacillus subtilis and Staphylococcus aureus

Published online by Cambridge University Press:  21 December 2015

Zheng-Yu Yan ,
Xiao-Xia Ai ,
Yi-Long Su ,
Xin-Ying Liu ,
Xiao-Hui Shan  and
Sheng-Mei Wu
Zheng-Yu Yan
Affiliation:
Department of Analytical Chemistry, China Pharmaceutical University, 24 Tongjia Lane, Gulou District, Nanjing 210009, China Key Laboratory of Drug Quality Control and Pharmacovigilance, Ministry of Education, 24 Tongjia Lane, Gulou District, Nanjing 210009, China
Xiao-Xia Ai
Affiliation:
Department of Analytical Chemistry, China Pharmaceutical University, 24 Tongjia Lane, Gulou District, Nanjing 210009, China Key Laboratory of Drug Quality Control and Pharmacovigilance, Ministry of Education, 24 Tongjia Lane, Gulou District, Nanjing 210009, China
Yi-Long Su
Affiliation:
Department of Analytical Chemistry, China Pharmaceutical University, 24 Tongjia Lane, Gulou District, Nanjing 210009, China Key Laboratory of Drug Quality Control and Pharmacovigilance, Ministry of Education, 24 Tongjia Lane, Gulou District, Nanjing 210009, China
Xin-Ying Liu
Affiliation:
Department of Analytical Chemistry, China Pharmaceutical University, 24 Tongjia Lane, Gulou District, Nanjing 210009, China Key Laboratory of Drug Quality Control and Pharmacovigilance, Ministry of Education, 24 Tongjia Lane, Gulou District, Nanjing 210009, China
Xiao-Hui Shan
Affiliation:
Laizhou Entry-Exit Inspection and Quarantine Bureau, Laizhou 261400, China
Sheng-Mei Wu*
Affiliation:
Department of Analytical Chemistry, China Pharmaceutical University, 24 Tongjia Lane, Gulou District, Nanjing 210009, China Key Laboratory of Drug Quality Control and Pharmacovigilance, Ministry of Education, 24 Tongjia Lane, Gulou District, Nanjing 210009, China
*
*Corresponding authors. wushengmei80@163.com; wsm310@126.com
Get access

Abstract

In this work, fluorescent Bacillus subtilis (B. subtilis) cells were developed as probes for imaging applications and to explore behaviorial interaction between B. subtilis and Staphylococcus aureus (S. aureus). A novel biological strategy of coupling intracellular biochemical reactions for controllable biosynthesis of CdSe quantum dots by living B. subtilis cells was demonstrated, through which highly luminant and photostable fluorescent B. subtilis cells were achieved with good uniformity. With the help of the obtained fluorescent B. subtilis cells probes, S. aureus cells responded to co-cultured B. subtilis and to aggregate. The degree of aggregation was calculated and nonlinearly fitted to a polynomial model. Systematic investigations of their interactions implied that B. subtilis cells inhibit the growth of neighboring S. aureus cells, and this inhibition was affected by both the growth stage and the amount of surrounding B. subtilis cells. Compared to traditional methods of studying bacterial interaction between two species, such as solid culture medium colony observation and imaging mass spectrometry detection, the procedures were more simple, vivid, and photostable due to the efficient fluorescence intralabeling with less influence on the cells’ surface, which might provide a new paradigm for future visualization of microbial behavior.

Keywords

bacteria intralabelingquantum dots biosynthesisvisual interactionBacillus subtilisStaphylococcus aureus
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 22 , Issue 1 , February 2016 , pp. 13 - 21
Copyright
© Microscopy Society of America 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Asmathunisha, N. & Kathiresan, K. (2013). A review on biosynthesis of nanoparticles by marine organisms. Colloids Surf B Biointerfaces 103, 283–287.CrossRefGoogle ScholarPubMed
Balcerzak, M. (2002). Sample digestion methods for the determination of traces of precious metals by spectrometric techniques. Anal Sci 18, 737–750.CrossRefGoogle ScholarPubMed
Ben-Jacob, E., Cohen, I. & Levine, H. (2000). Cooperative self-organization of microorganisms. Adv Phys 49(4), 395–554.CrossRefGoogle Scholar
Berti, L. & Burley, G.A. (2008). Nucleic acid and nucleotide-mediated synthesis of inorganic nanoparticles. Nat Nano 3(2), 81–87.CrossRefGoogle ScholarPubMed
Cannon, B. (2014). Microbiology: Resistance fighters. Nature 509(7498), S6–S8.CrossRefGoogle ScholarPubMed
Chan, W.C. & Nie, S. (1998). Quantum dot bioconjugates for ultrasensitive nonisotopic detection. Science 281(5385), 2016–2018.CrossRefGoogle ScholarPubMed
Cui, R., Liu, H.H., Xie, H.Y., Zhang, Z.L., Yang, Y.R., Pang, D.W., Xie, Z.X., Chen, B.B., Hu, B. & Shen, P. (2009). Living yeast cells as a controllable biosynthesizer for fluorescent quantum dots. Adv Funct Mater 19(15), 2359–2364.CrossRefGoogle Scholar
Delaney, J.R., Stöven, S., Uvell, H., Anderson, K.V., Engström, Y. & Mlodzik, M. (2006). Cooperative control of Drosophila immune responses by the JNK and NF-κB signaling pathways. EMBO J 25(13), 3068–3077.CrossRefGoogle ScholarPubMed
Foster, T.J., Geoghegan, J.A., Ganesh, V.K. & Höök, M. (2014). Adhesion, invasion and evasion: The many functions of the surface proteins of Staphylococcus aureus. Nat Rev Microbiol 12(1), 49–62.CrossRefGoogle ScholarPubMed
Fuchs, S.W., Jaskolla, T.W., Bochmann, S., Kötter, P., Wichelhaus, T., Karas, M., Stein, T. & Entian, K.-D. (2011). Entianin, a novel subtilin-like lantibiotic from Bacillus subtilis subsp. spizizenii DSM 15029T with high antimicrobial activity. App Environ Microbiol 77(5), 1698–1707.CrossRefGoogle ScholarPubMed
Gadd, G.M. (2010). Metals, minerals and microbes: Geomicrobiology and bioremediation. Microbiology 156(3), 609–643.CrossRefGoogle ScholarPubMed
Gonzalez, D.J., Haste, N.M., Hollands, A., Fleming, T.C., Hamby, M., Pogliano, K., Nizet, V. & Dorrestein, P.C. (2011). Microbial competition between Bacillus subtilis and Staphylococcus aureus monitored by imaging mass spectrometry. Microbiology 157(9), 2485–2492.CrossRefGoogle ScholarPubMed
Hao, J., Huang, L.-L., Zhang, R., Wang, H.-Z. & Xie, H.-Y. (2012). A mild and reliable method to label enveloped virus with quantum dots by copper-free click chemistry. Anal Chem 84(19), 8364–8370.CrossRefGoogle ScholarPubMed
Hibbing, M.E., Fuqua, C., Parsek, M.R. & Peterson, S.B. (2010). Bacterial competition: Surviving and thriving in the microbial jungle. Nat Rev Microbiol 8(1), 15–25.CrossRefGoogle ScholarPubMed
Hochbaum, A.I., Kolodkin-Gal, I., Foulston, L., Kolter, R., Aizenberg, J. & Losick, R. (2011). Inhibitory effects of D-amino acids on Staphylococcus aureus biofilm development. J Bacteriol 193(20), 5616–5622.CrossRefGoogle ScholarPubMed
Ikram, M. & Faisal, M. (2010). Comparative assessment of selenite (SeIV) detoxification to elemental selenium (Se0) by Bacillus sp. Biotechnol Lett 32(9), 1255–1259.CrossRefGoogle ScholarPubMed
Kaiser, D. & Losick, R. (1993). How and why bacteria talk to each other. Cell 73(5), 873–885.CrossRefGoogle ScholarPubMed
Kong, L., Doona, C.J., Setlow, P. & Li, Y.-q. (2014). Monitoring rates and heterogeneity of high-pressure germination of Bacillus spores by phase-contrast microscopy of individual spores. Appl Environ Microbiol 80(1), 345–353.CrossRefGoogle ScholarPubMed
Lampis, S., Zonaro, E., Bertolini, C., Bernardi, P., Butler, C.S. & Vallini, G. (2014). Delayed formation of zero-valent selenium nanoparticles by Bacillus mycoides SeITE01 as a consequence of selenite reduction under aerobic conditions. Microb Cell Fact 13(35), 3–35.CrossRefGoogle ScholarPubMed
Li, Y., Cui, R., Zhang, P., Chen, B.-B., Tian, Z.-Q., Li, L., Hu, B., Pang, D.-W. & Xie, Z.-X. (2013). Mechanism-oriented controllability of intracellular quantum dots formation: The role of glutathione metabolic pathway. ACS Nano 7(3), 2240–2248.CrossRefGoogle ScholarPubMed
Liu, W.-T., Yang, Y.-L., Xu, Y., Lamsa, A., Haste, N.M., Yang, J.Y., Ng, J., Gonzalez, D., Ellermeier, C.D. & Straight, P.D. (2010). Imaging mass spectrometry of intraspecies metabolic exchange revealed the cannibalistic factors of Bacillus subtilis. Proc Nat Acad Sci U S A 107(37), 16286–16290.CrossRefGoogle ScholarPubMed
Lloyd, J.R., Byrne, J.M. & Coker, V.S. (2011). Biotechnological synthesis of functional nanomaterials. Curr Opin Biotechnol 22(4), 509–515.CrossRefGoogle ScholarPubMed
Løvdal, I.S., Granum, P.E., Rosnes, J.T. & Løvdal, T. (2013). Activation of Bacillus spores at moderately elevated temperatures (30–33°C). Antonie van Leeuwenhoek 103(3), 693–700.CrossRefGoogle Scholar
Mi, C., Wang, Y., Zhang, J., Huang, H., Xu, L., Wang, S., Fang, X., Fang, J., Mao, C. & Xu, S. (2011). Biosynthesis and characterization of CdS quantum dots in genetically engineered Escherichia coli. J Biotechnol 153(3), 125–132.CrossRefGoogle ScholarPubMed
Saikaly, P.E. & Oerther, D.B. (2004). Bacterial competition in activated sludge: Theoretical analysis of varying solids retention times on diversity. Microb Ecol 48(2), 274–284.CrossRefGoogle ScholarPubMed
Setlow, P. (2014). Germination of spores of Bacillus species: What we know and do not know. J Bacteriol 196(7), 1297–1305.CrossRefGoogle Scholar
Shank, E.A. & Kolter, R. (2011). Extracellular signaling and multicellularity in Bacillus subtilis. Curr Opin Microbiol 14(6), 741–747.CrossRefGoogle ScholarPubMed
Shin, H., Jang, D., Hwang, J., Jang, Y., Cho, M. & Park, K. (2014). Structural characterization of CdSe/ZnS core–shell quantum dots (QDs) using TEM/STEM observation. J Mater Sci Mater Electron 25(5), 2047–2052.CrossRefGoogle Scholar
Siddique, T., Zhang, Y., Okeke, B.C. & Frankenberger, W.T. (2006). Characterization of sediment bacteria involved in selenium reduction. Bioresour Technol 97(8), 1041–1049.CrossRefGoogle ScholarPubMed
Silver, L.L. (2014). Antibacterials for any target. Nat Biotech 32(11), 1102–1104.CrossRefGoogle ScholarPubMed
Stover, A.G. & Driks, A. (1999). Secretion, localization, and antibacterial activity of TasA, a Bacillus subtilis spore-associated protein. Journal of Bacteriology 181(5), 1664–1672.CrossRefGoogle Scholar
Suresh, A.K. (2014). Extracellular bio-production and characterization of small monodispersed CdSe quantum dot nanocrystallites. Spectrochim Acta A Mol Biomol Spectrosc 130, 344–349.CrossRefGoogle ScholarPubMed
Valizadeh, A., Mikaeili, H., Samiei, M., Farkhani, S.M., Zarghami, N., Akbarzadeh, A. & Davaran, S. (2012). Quantum dots: Synthesis, bioapplications, and toxicity. Nanoscale Res Lett 7(1), 1–14.CrossRefGoogle ScholarPubMed
Vinopal, S., Ruml, T. & Kotrba, P. (2007). Biosorption of Cd 2+ and Zn 2+ by cell surface-engineered Saccharomyces cerevisiae. Int Biodeterior Biodegradation 60(2), 96–102.CrossRefGoogle Scholar
Xiong, L.-H., Cui, R., Zhang, Z.-L., Yu, X., Xie, Z., Shi, Y.-B. & Pang, D.-W. (2014). Uniform fluorescent nanobioprobes for pathogen detection. ACS Nano 8(5), 5116–5124.CrossRefGoogle ScholarPubMed
Yan, G. & Viraraghavan, T. (2000). Effect of pretreatment on the bioadsorption of heavy metals on Mucor rouxii. Water SA-Pretoria 26(1), 119–124.Google Scholar
Yan, Z., Qian, J., Gu, Y., Su, Y., Ai, X. & Wu, S. (2014). Green biosynthesis of biocompatible CdSe quantum dots in living Escherichia coli cells. Mater Res Exp 1(1), 015401.CrossRefGoogle Scholar
Zhang, M., Bai, L., Shang, W., Xie, W., Ma, H., Fu, Y., Fang, D., Sun, H., Fan, L., Han, M., Liu, C. & Yang, S. (2012). Facile synthesis of water-soluble, highly fluorescent graphene quantum dots as a robust biological label for stem cells. J Mater Chem 22(15), 7461–7467.CrossRefGoogle Scholar
Zhao, Y., Selvaraj, J.N., Xing, F., Zhou, L., Wang, Y., Song, H., Tan, X., Sun, L., Sangare, L., Folly, Y.M.E. & Liu, Y. (2014). Antagonistic action of Bacillus subtilis strain SG6 on Fusarium graminearum. PLoS One 9(3), e92486.CrossRefGoogle Scholar
Supplementary material: File

Yan supplementary material S1

Yan supplementary material

Download Yan supplementary material S1(File)
File 10.6 MB