Skip to main content
SpringerLink
Log in

Terahertz-infrared spectroscopy of Shewanella oneidensis MR-1 extracellular matrix

  • Original Paper
  • Published:
Journal of Biological Physics Aims and scope Submit manuscript

Abstract

Employing optical spectroscopy we have performed a comparative study of the dielectric response of extracellular matrix and filaments of electrogenic bacteria Shewanella oneidensis MR-1, cytochrome c, and bovine serum albumin. Combining infrared transmission measurements on thin layers with data of the terahertz spectra, we obtain the dielectric permittivity and AC conductivity spectra of the materials in a broad frequency band from a few cm−1 up to 7000 cm−1 in the temperature range from 5 to 300 K. Strong absorption bands are observed in the three materials that cover the range from 10 to 300 cm−1 and mainly determine the terahertz absorption. When cooled down to liquid helium temperatures, the bands in Shewanella oneidensis MR-1 and cytochrome c reveal a distinct fine structure. In all three materials, we identify the presence of liquid bound water in the form of librational and translational absorption bands at ≈ 200 and ≈ 600 cm−1, respectively. The sharp excitations seen above 1000 cm−1 are assigned to intramolecular vibrations.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Notes

  1. The formal amount of water in EMF is higher that the one in CytC and BSA. However, the water in our samples is in three different states: bulk, loosely bound and bound. We assume, that phenomena described here are related to the behavior of loosely bound water, the amount of which is lower in EMF. For more details, see [20]

References

  1. Veazey, J.P., Reguera, G., Tessmer, S.H.: Electronic properties of conductive pili of the metal-reducing bacterium Geobacter sulfurreducens probed by scanning tunneling microscopy. Phys. Rev. E 84, 1–4 (2011). https://doi.org/10.1103/PhysRevE.84.060901

  2. Leung, K.M., Wanger, G., El-Naggar, M.Y., Gorby, Y., Southam, G., Lau, W.M., Yang, J.: Shewanella oneidensis MR-1 bacterial nanowires exhibit p-type, tunable electronic behavior. Nano Lett. 13, 2407–2411 (2013). https://doi.org/10.1021/nl400237p

    Article  ADS  Google Scholar 

  3. El-Naggar, M.Y., Wanger, G., Leung, K.M., Yuzvinsky, T.D., Southam, G., Yang, J., Lau, W.M., Nealson, K.H., Gorby, Y.A.: Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1. Proc. Natl. Acad. Sci. U. S. A. 107, 18127–18131 (2010). https://doi.org/10.1073/pnas.1004880107

    Article  ADS  Google Scholar 

  4. Malvankar, N.S., Vargas, M., Nevin, K.P., Franks, A.E., Leang, C., Kim, B.-C., Inoue, K., Mester, T., Covalla, S.F., Johnson, J.P., Rotello, V.M., Tuominen, M.T., Lovley, D.R.: Tunable metallic-like conductivity in microbial nanowire networks. Nat. Nanotechnol. 6, 573–579 (2011). https://doi.org/10.1038/nnano.2011.119

    Article  ADS  Google Scholar 

  5. Malvankar, N.S., Yalcin, S.E., Tuominen, M.T., Lovley, D.R.: Visualization of charge propagation along individual pili proteins using ambient electrostatic force microscopy. Nat. Nanotechnol. 9, 1012–1017 (2014). https://doi.org/10.1038/nnano.2014.236

    Article  ADS  Google Scholar 

  6. Pirbadian, S., Barchinger, S.E., Leung, K.M., Byun, H.S., Jangir, Y., Bouhenni, R.A., Reed, S.B., Romine, M.F., Saffarini, D.A., Shi, L., Gorby, Y.A., Golbeck, J.H., El-Naggar, M.Y.: Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components. Proc. Natl. Acad. Sci. U. S. A. 111, 12883–12888 (2014). https://doi.org/10.1073/pnas.1410551111

    Article  ADS  Google Scholar 

  7. Subramanian, P., Pirbadian, S., El-Naggar, M.Y., Jensen, G.J.: The ultrastructure of Shewanella oneidensis MR-1 nanowires revealed by electron cryo-tomography. bioRxiv. (2017)

  8. Malvankar, N.S., Vargas, M., Nevin, K., Tremblay, P., Evans-Lutterodt, K., Nykypanchuk, D.: Structural basis for metallic-like conductivity in microbial nanowires. mBio 6(2), e00084 (2015). https://doi.org/10.1128/mBio.00084-15

  9. Xiao, K., Malvankar, N.S., Shu, C., Martz, E., Lovley, D.R., Sun, X.: Low-energy atomic models suggesting a pilus structure that could account for electrical conductivity of Geobacter sulfurreducens pili. Sci. Rep. 6, 23385 (2016). https://doi.org/10.1038/srep23385

    Article  ADS  Google Scholar 

  10. Malvankar, N.S., Lovley, D.R.: Microbial nanowires: a new paradigm for biological electron transfer and bioelectronics. ChemSusChem 5, 1039–1046 (2012). https://doi.org/10.1002/cssc.201100733

    Article  Google Scholar 

  11. Adhikari, R.Y., Malvankar, N.S., Tuominen, M.T., Lovley, D.R.: Conductivity of individual Geobacter pili. RSC Adv. 6, 8354–8357 (2016). https://doi.org/10.1039/C5RA28092C

    Article  Google Scholar 

  12. Vargas, M., Malvankar, N.S., Tremblay, P.-L., Leang, C., Smith, J.A., Patel, P., Snoeyenbos-West, O., Synoeyenbos-West, O., Nevin, K.P., Lovley, D.R.: Aromatic amino acids required for pili conductivity and long-range extracellular electron transport in Geobacter sulfurreducens. mBio 4, e00105 (2013). https://doi.org/10.1128/mBio.00105-13

  13. Smith, D.M.A., Rosso, K.M.: Possible dynamically gated conductance along heme wires in bacterial multiheme cytochromes. J. Phys. Chem. B 118, 8505–8512 (2014). https://doi.org/10.1021/jp502803y

    Article  Google Scholar 

  14. El-Naggar, M.Y., Gorby, Y.A., Xia, W., Nealson, K.H.: The molecular density of states in bacterial nanowires. Biophys. J. 95, L10–L12 (2008). https://doi.org/10.1529/biophysj.108.134411

    Article  Google Scholar 

  15. Breuer, M., Rosso, K.M., Blumberger, J., Butt, J.N.: Multi-haem cytochromes in Shewanella oneidensis MR-1: structures, functions and opportunities. J. R. Soc. Interface 12, 20141117 (2015). https://doi.org/10.1098/rsif.2014.1117

    Article  Google Scholar 

  16. Yan, H., Chuang, C., Zhugayevych, A., Tretiak, S., Dahlquist, F.W., Bazan, G.C.: Inter-aromatic distances in Geobacter sulfurreducens pili relevant to biofilm charge transport. Adv. Mater. 27, 1908–1911 (2015). https://doi.org/10.1002/adma.201404167

    Article  Google Scholar 

  17. Grebenko, A., Dremov, V., Barzilovich, P., Bubis, A., Sidoruk, K., Voeikova, T., Gagkaeva, Z., Chernov, T., Korostylev, E., Gorshunov, B., Motovilov, K.: Impedance spectroscopy of single bacterial nanofilament reveals water-mediated charge transfer. PLoS ONE 13, 1–17 (2018). https://doi.org/10.1371/journal.pone.0191289

  18. Zaytsev, K.I., Kudrin, K.G., Karasik, V.E., Reshetov, I. V., Yurchenko, S.O.: In vivo terahertz spectroscopy of pigmentary skin nevi: pilot study of non-invasive early diagnosis of dysplasia. Appl. Phys. Lett. 106, (2015). https://doi.org/10.1063/1.4907350

  19. Dressel, M., Gruner, G.: Electrodynamics of Solids. Cambridge University Press, Cambridge (2002)

    Book  Google Scholar 

  20. Motovilov, K.A., Savinov, M., Zhukova, E.S., Pronin, A.A., Gagkaeva, Z. V., Grinenko, V., Sidoruk, K. V., Voeikova, T.A., Barzilovich, P.Y., Grebenko, A.K., Lisovskii, S. V., Torgashev, V.I., Bednyakov, P., Pokorný, J., Dressel, M., Gorshunov, B.P.: Observation of dielectric universalities in albumin, cytochrome c and Shewanella oneidensis MR-1 extracellular matrix. Sci. Rep. 7, 15731 (2017). https://doi.org/10.1038/s41598-017-15693-y

  21. Logan, B.E., Hamelers, B., Rozendal, R., Schröder, U., Keller, J., Freguia, S., Aelterman, P., Verstraete, W., Rabaey, K.: Microbial fuel cells: methodology and technology. Environ. Sci. Technol. 40, 5181–5192 (2006)

    Article  ADS  Google Scholar 

  22. Richardson, D.J., Butt, J.N., Fredrickson, J.K., Zachara, J.M., Shi, L., Edwards, M.J., White, G., Baiden, N., Gates, A.J., Marritt, S.J., Clarke, T.A.: The “porin-cytochrome” model for microbe-to-mineral electron transfer. Mol. Microbiol. 85, 201–212 (2012). https://doi.org/10.1111/j.1365-2958.2012.08088.x

    Article  Google Scholar 

  23. Gorshunov, B., Volkov, A., Spektor, I., Prokhorov, A., Mukhin, A., Dressel, M., Uchida, S., Loidl, A.: Terahertz BWO-spectrosopy. Int. J. Infrared Millimeter Waves 26, 1217–1240 (2005). https://doi.org/10.1007/s10762-005-7600-y

    Article  ADS  Google Scholar 

  24. Born, M., Wolf, E.: Principles of Optics. Pergamon, Oxford (1980)

    Google Scholar 

  25. Downing, H.D., Williams, D.: Optical constants of water in the infrared. J. Geophys. Res. 80, 1656–1661 (1975). https://doi.org/10.1029/JC080i012p01656

    Article  ADS  Google Scholar 

  26. Zelsmann, H.R.: Temperature dependence of the optical constants for liquid H2O and D2O in the far IR region. J. Mol. Struct. 350, 95–114 (1995). https://doi.org/10.1016/0022-2860(94)08471-S

    Article  ADS  Google Scholar 

  27. Liebe, H.J., Hufford, G.A., Manabe, T.: A model for the complex permittivity of water at frequencies below 1 THz. Int. J. Infrared Millimeter Waves 12, 659–675 (1991). https://doi.org/10.1007/BF01008897

  28. Grdadolnik, J., Marechal, Y.: Bovine serum albumin observed by infrared spectrometry. II. Hydration mechanisms and interaction configurations of embedded H2O molecules. Biopolymers 62, 54–67 (2001). https://doi.org/10.1002/1097-0282(2001)62:1<54::AID-BIP70>3.0.CO;2-4

  29. Grdadolnik, J., Marechal, Y.: Bovine serum albumin observed by infrared spectrometry. I. Methodology, structural investigation, and water uptake. Biopolymers 62, 40–53 (2001). https://doi.org/10.1002/1097-0282(2001)62:1<40::AID-BIP60>3.0.CO;2-C

    Article  Google Scholar 

  30. Thielges, M.C., Zimmermann, J., Dawson, P.E., Romesberg, F.E.: The determinants of stability and folding in evolutionarily diverged cytochromes c. J. Mol. Biol. 388, 159–167 (2009). https://doi.org/10.1016/j.jmb.2009.02.059

    Article  Google Scholar 

  31. Heimburg, T., Marsh, D.: Investigation of secondary and tertiary structural changes of cytochrome c in complexes with anionic lipids using amide hydrogen exchange measurements: an FTIR study. Biophys. J. 65, 2408–2417 (1993). https://doi.org/10.1016/S0006-3495(93)81299-2

    Article  Google Scholar 

  32. Ye, M., Zhang, Q.-L., Li, H., Weng, Y.-X., Wang, W.-C., Qiu, X.-G.: Infrared spectroscopic discrimination between the loop and α-helices and determination of the loop diffusion kinetics by temperature-jump time-resolved infrared spectroscopy for cytochrome c. Biophys. J. 93, 2756–2766 (2007). https://doi.org/10.1529/biophysj.107.106799

    Article  ADS  Google Scholar 

  33. von Hippel, A.R.: The dielectric relaxation spectra of water, ice, and aqueous solutions, and their interpretation. I. Critical survey of the status-quo for water. IEEE Trans. Electr. Insul. 23, 801–816 (1988). https://doi.org/10.1109/14.8745

    Article  Google Scholar 

  34. Eisenberg, D., Kautzmann, W.: The Structure and Properties of Water. Oxford University Press, New York (1969)

    Google Scholar 

  35. Yamamoto, N., Ohta, K., Tamura, A., Tominaga, K.: Broadband dielectric spectroscopy on lysozyme in the sub-gigahertz to terahertz frequency regions: effects of hydration and thermal excitation. J. Phys. Chem. B 120, 4743–4755 (2016). https://doi.org/10.1021/acs.jpcb.6b01491

    Article  Google Scholar 

  36. Urabe, H., Sugawara, Y., Ataka, M., Rupprecht, A.: Low-frequency Raman spectra of lysozyme crystals and oriented DNA films: dynamics of crystal water. Biophys. J. 74, 1533–1540 (1998). https://doi.org/10.1016/S0006-3495(98)77865-8

    Article  ADS  Google Scholar 

  37. Nakanishi, M., Sokolov, A.P.: Protein dynamics in a broad frequency range: dielectric spectroscopy studies. J. Non-Cryst. Solids 407, 478–485 (2015). https://doi.org/10.1016/j.jnoncrysol.2014.08.057

    Article  ADS  Google Scholar 

  38. Khodadadi, S., Pawlus, S., Sokolov, A.P.: Influence of hydration on protein dynamics: combining dielectric and neutron scattering spectroscopy data. J. Phys. Chem. B 112, 14273–14280 (2008). https://doi.org/10.1021/jp8059807

    Article  Google Scholar 

  39. Bertie, J.E., Labbé, H.J., Whalley, E.: Absorptivity of ice I in the range 4000–30 cm−1. J. Chem. Phys. 50, 4501–4520 (1969). https://doi.org/10.1063/1.1670922

    Article  ADS  Google Scholar 

  40. Buckingham, A.D.: The hydrogen bond, and the structure and properties of H20 and (H20)2. J. Mol. Struct. 250, 111–118 (1991). https://doi.org/10.1016/0022-2860(91)85023-V

    Article  ADS  Google Scholar 

  41. Bagchi, B.: Water dynamics in the hydration layer around proteins and micelles. (2005). https://doi.org/10.1021/CR020661+

  42. Qvist, J., Persson, E., Mattea, C., Halle, B.: Time scales of water dynamics at biological interfaces: peptides, proteins and cells. Faraday Discuss. 141, 131–144. discussion 175-207 (2009)

    Article  ADS  Google Scholar 

  43. Sasisanker, P., Weingärtner, H.: Hydration dynamics of water near an amphiphilic model peptide at low hydration levels: a dielectric relaxation study. ChemPhysChem 9, 2802–2808 (2008). https://doi.org/10.1002/cphc.200800508

    Article  Google Scholar 

  44. Khodadadi, S., Sokolov, A.P.: Protein dynamics: from rattling in a cage to structural relaxation. Soft Matter 11, 4984–4998 (2015). https://doi.org/10.1039/C5SM00636H

    Article  ADS  Google Scholar 

  45. He, Y., Chen, J.-Y., Knab, J.R., Zheng, W., Markelz, A.G.: Evidence of protein collective motions on the picosecond timescale. Biophys. J. 100, 1058–1065 (2011). https://doi.org/10.1016/j.bpj.2010.12.3731

    Article  ADS  Google Scholar 

  46. Markelz, A.G., Knab, J.R., Chen, J.Y., He, Y.: Protein dynamical transition in terahertz dielectric response. Chem. Phys. Lett. 442, 413–417 (2007). https://doi.org/10.1016/j.cplett.2007.05.080

    Article  ADS  Google Scholar 

  47. Chen, J.-Y., Knab, J.R., Cerne, J., Markelz, A.G.: Large oxidation dependence observed in terahertz dielectric response for cytochrome c. Phys. Rev. E 72, 40901 (2005). https://doi.org/10.1103/PhysRevE.72.040901

    Article  ADS  Google Scholar 

  48. Yamamoto, K., Tominaga, K., Sasakawa, H., Tamura, A., Murakami, H., Ohtake, H., Sarukura, N.: Far-infrared absorption measurements of polypeptides and cytochrome c by THz radiation. Bull. Chem. Soc. Jpn. 75, 1083–1092 (2002). https://doi.org/10.1246/bcsj.75.1083

    Article  Google Scholar 

  49. Markelz, A., Roitberg, A., Heilweil, E.: Pulsed terahertz spectroscopy of DNA, bovine serum albumin and collagen between 0.1 and 2.0 THz. Chem. Phys. Lett. 320, 42–48 (2000). https://doi.org/10.1016/S0009-2614(00)00227-X

    Article  ADS  Google Scholar 

  50. Mernea, M., Calborean, O., Grigore, O., Dascalu, T., Mihailescu, D.F.: Validation of protein structural models using THz spectroscopy: a promising approach to solve three-dimensional structures. Opt. Quant. Electron. 46, 505–514 (2014). https://doi.org/10.1007/s11082-013-9872-0

    Article  Google Scholar 

  51. Acbas, G., Niessen, K.A., Snell, E.H., Markelz, A.G.: Optical measurements of long-range protein vibrations. Nat. Commun. 6, 3076 (2014). https://doi.org/10.1038/ncomms4076

    Article  Google Scholar 

  52. Balu, R., Zhang, H., Zukowski, E., Chen, J.-Y., Markelz, A.G., Gregurick, S.K.: Terahertz spectroscopy of bacteriorhodopsin and rhodopsin: similarities and differences. Biophys. J. 94, 3217–3226 (2008). https://doi.org/10.1529/biophysj.107.105163

    Article  ADS  Google Scholar 

  53. Xu, J., Plaxco, K.W., Allen, S.J.: Probing the collective vibrational dynamics of a protein in liquid water by terahertz absorption spectroscopy. Protein Sci. 15, 1175–1181 (2006). https://doi.org/10.1110/ps.062073506

    Article  Google Scholar 

  54. Markelz, A., Whitmire, S., Hillebrecht, J., Birge, R.: THz time domain spectroscopy of biomolecular conformational modes. Phys. Med. Biol. 47, 3797–3805 (2002). https://doi.org/10.1088/0031-9155/47/21/318

    Article  Google Scholar 

  55. Balog, E., Becker, T., Oettl, M., Lechner, R., Daniel, R., Finney, J., Smith, J.C.: Direct determination of vibrational density of states change on ligand binding to a protein. Phys. Rev. Lett. 93, 28103 (2004). https://doi.org/10.1103/PhysRevLett.93.028103

    Article  ADS  Google Scholar 

  56. MacKerell, A.D., Bashford, D., Bellott, M., Dunbrack, R.L., Evanseck, J.D., Field, M.J., Fischer, S., Gao, J., Guo, H., Ha, S., Joseph-McCarthy, D., Kuchnir, L., Kuczera, K., Lau, F.T., Mattos, C., Michnick, S., Ngo, T., Nguyen, D.T., Prodhom, B., Reiher, W.E., Roux, B., Schlenkrich, M., Smith, J.C., Stote, R., Straub, J., Watanabe, M., Wiórkiewicz-Kuczera, J., Yin, D., Karplus, M.: All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102, 3586–3616 (1998). https://doi.org/10.1021/jp973084f

    Article  Google Scholar 

  57. Smith, J.C.: Protein dynamics: comparison of simulations with inelastic neutron scattering experiments. Q. Rev. Biophys. 24, 227–291 (1991)

    Article  Google Scholar 

  58. Hayward, S., Kitao, A., Hirata, F., Gō, N.: Effect of solvent on collective motions in globular protein. J. Mol. Biol. 234, 1207–1217 (1993). https://doi.org/10.1006/jmbi.1993.1671

    Article  Google Scholar 

  59. Go, N., Noguti, T., Nishikawa, T.: Dynamics of a small globular protein in terms of low-frequency vibrational modes. Proc. Natl. Acad. Sci. U. S. A. 80, 3696–3700 (1983)

    Article  ADS  Google Scholar 

  60. Rasmussen, B.F., Stock, A.M., Ringe, D., Petsko, G.A.: Crystalline ribonuclease a loses function below the dynamical transition at 220 K. Nature 357, 423–424 (1992). https://doi.org/10.1038/357423a0

    Article  ADS  Google Scholar 

  61. Sokolov, A.P., Roh, J.H., Mamontov, E., García Sakai, V.: Role of hydration water in dynamics of biological macromolecules. Chem. Phys. 345, 212–218 (2008). https://doi.org/10.1016/j.chemphys.2007.07.013

    Article  Google Scholar 

  62. He, Y., Ku, P., Knab, J., Chen, J., Markelz, A.: Protein dynamical transition does not require protein structure. Phys. Rev. Lett. 101, 178103 (2008). https://doi.org/10.1103/PhysRevLett.101.178103

    Article  ADS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Ministry of Education and Science of the Russian Federation (Projects N3.9896.2017/BY, 5-100) and by MIPT visiting professors grant. The authors acknowledge K.A. Motovilov for fruitful discussions. We acknowledge discussions with V.I. Borshchevskiy, V.I. Gordelii, Yu. Feldman, V.V. Lebedev, S. Tretiak, G.A. Tsirlina, A. Zhugayevych.

Author information

Authors and Affiliations

  1. Moscow Institute of Physics and Technology, Dolgoprudny, Moscow Region, Russia

    Z. V. Gagkaeva, E. S. Zhukova, A. K. Grebenko, M. Dressel & B. P. Gorshunov

  2. Institute for Metallic Materials, IFW Dresden, Dresden, Germany

    V. Grinenko

  3. Scientific Center of Russian Federation Research Institute for Genetics and Selection of Industrial Microorganisms, Moscow, Russia

    K. V. Sidoruk & T. A. Voeikova

  4. Physikalisches Institut, Universität Stuttgart, Stuttgart, Germany

    M. Dressel

Authors
  1. Z. V. Gagkaeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. S. Zhukova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. V. Grinenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. K. Grebenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. K. V. Sidoruk
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. T. A. Voeikova
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. Dressel
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. B. P. Gorshunov
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

T.A.V. and B.P.G. designed the research; K.V.S. and T.A.V. performed cultivation of Shewanella oneidensis MR-1, A.K.G. prepared EMF, Z.V.G., E.S.Z, V.G., K.V.S. and A.K.G. performed research; Z.V.G., E.S.Z. and V.G. analyzed data; B.P.G and M.D. wrote the paper.

Corresponding author

Correspondence to B. P. Gorshunov.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gagkaeva, Z.V., Zhukova, E.S., Grinenko, V. et al. Terahertz-infrared spectroscopy of Shewanella oneidensis MR-1 extracellular matrix. J Biol Phys 44, 401–417 (2018). https://doi.org/10.1007/s10867-018-9497-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10867-018-9497-4

Keywords

Search

Navigation