Abstract
Biological cells are fascinating systems of inconceivable complexity, which fulfil various functions. Among others, cells are able to execute motions, to produce heat, to breathe, to subsist, to grow wand proliferate and to die. Science aims at deciphering the different functionalities and activities of, and inside, the cells and how their different components participate to them. The methods employed are also versatile, as optical approaches by microscopies, modelling and simulations, spectroscopies, thermodynamic measurements and much more, each procuring some pieces of the puzzle. Although the different investigations are laborious and time consuming, research is the only way to disentangle the world at the microscopic level surrounding us. In the present study, we cite a few examples of studies on whole cells and cell components by different neutron scattering techniques to illustrate the modern possibilities. As neutrons are not charged, they have interactions directly with the atomic nuclei and give access to structural as well as dynamical information through coherent and incoherent neutron scattering. These techniques can be applied to the same samples and under identical experimental conditions so that we can gain knowledge on the correlations between structural and dynamical functions. Here, we present applications of neutron experiments to decipher the behaviour of complex biological samples, which study was not possible by other probes. The first example focuses on the molecular basis of the adaptation of cells living under extreme conditions, such as Archaea from the deep sea hydrothermal vents which experience both high temperature and high pressure stresses. Molecular dynamics seems to play a key role for adaptation as it is increased for the proteome of cells from such environment, in contrast to common expectation. In the second example, we exposed endogenous nanoparticles, low density lipoproteins, to high hydrostatic pressure, to shed light on the flexibility and stability of such particles under extreme conditions. Here we found that the native particle was surprisingly resistant to pressure application, concerning both dynamics and structure, while a modified form thereof was not.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Karr, J. R., Sanghvi, J. C., Macklin, D. N., Gutschow, M. V., Jacobs, J. M., Bolival, B., Jr., et al. (2012). A whole-cell computational model predicts phenotype from genotype. Cell, 150, 389–401. https://doi.org/10.1016/j.cell.2012.05.044.
Schulz, R., Lindner, B., Petridis, L., & Smith, J. C. (2009). Scaling of multimillion-atom biological molecular dynamics simulation on a petascale supercomputer. Journal of Chemical Theory and Computation, 5, 2798–2808. https://doi.org/10.1021/ct900292r.
Nam, D., Park, J., Gallagher-Jones, M., Kim, S., Kim, S., Kohmura, Y., et al. (2013). Imaging fully hydrated whole cells by coherent x-ray diffraction microscopy. Physical Review Letters, 110(9), 098103. https://doi.org/10.1103/PhysRevLett.110.098103.
Jiang, H., Song, C., Chen, C. C., Xu, R., Raines, K. S., Fahimian, B. P., et al. (2010). Quantitative 3D imaging of whole, unstained cells by using X-ray diffraction microscopy. Proc Natl Acad Sci U S A, 107(25), 11234–11239. https://doi.org/10.1073/pnas.1000156107.
Tehei, M., Franzetti, B., Madern, D., Ginzburg, M., Ginzburg, B. Z., Giudici-Orticoni, M. T., et al. (2004). Adaptation to extreme environments: macromolecular dynamics in bacteria compared in vivo by neutron scattering. EMBO Reports, 5(1), 66–70. https://doi.org/10.1038/sj.embor.7400049.
Jasnin, M. (2009). Atomic-scale dynamics inside living cells explored by neutron scattering. Journal of the Royal Society, Interface, 6(Suppl 5), S611–S617. https://doi.org/10.1098/rsif.2009.0144.focus.
Luef, B., Fakra, S. C., Csencsits, R., Wrighton, K. C., Williams, K. H., Wilkins, M. J., et al. (2013). Iron-reducing bacteria accumulate ferric oxyhydroxide nanoparticle aggregates that may support planktonic growth. ISME Journal, 7(2), 338–350. https://doi.org/10.1038/ismej.2012.103.
Hajj, B., Wisniewski, J., El Beheiry, M., Chen, J., Revyakin, A., Wu, C., et al. (2014). Whole-cell, multicolor superresolution imaging using volumetric multifocus microscopy. Proc Natl Acad Sci U S A, 111(49), 17480–17485. https://doi.org/10.1073/pnas.1412396111.
Gabel, F., Bicout, B. J., Lehnert, U., Tehei, M., Weik, M., & Zaccai, G. (2002). Proteins dynamics studied by neutron scattering. Quaterly reviews of biophysics, 35(4), 327–367.
Kurr, M., Huber, R., Konig, H., Jannasch, H. W., Fricke, H., Trincone, A., et al. (1991). Methanopyrus kandleri, gen. and sp. nov. represents a novel group of hyperthermophilic methanogens, growing at 110 °C. Archives of Microbiology, 156, 239–247.
Takai, K., Nakamura, K., Toki, T., Tsunogai, U., Miyazaki, M., Miyazaki, J., et al. (2008). Cell proliferation at 122 °C and isotopically heavy CH4 production by a hyperthermophilic methanogen under high-pressure cultivation. Proceedings of the National Academy of Sciences of the United States of America, 105, 10949–10954.
Vauclare, P., Marty, V., Fabiani, E., Martinez, N., Jasnin, M., Gabel, F., et al. (2015). Molecular adaptation and salt stress response of Halobacterium salinarum cells revealed by neutron spectroscopy. Extremophiles, 19(6), 1099–1107. https://doi.org/10.1007/s00792-015-0782-x.
Lund, P., Tramonti, A., & De Biase, D. (2014). Coping with low pH: Molecular strategies in neutralophilic bacteria. FEMS Microbiology Reviews, 38(6), 1091–1125. https://doi.org/10.1111/1574-6976.12076.
Bée, M. (1988). Quasielastic neutron scattering: Principles and applications in solid state chemistry. Adam Hilger, Philadelphia: Biology and Materials Science.
Sears, V. F. (1992). Neutron scattering lengths and cross sections. Neutron News, 3, 26–37.
Natali, F., Peters, J., Russo, D., Barbieri, S., Chiapponi, C., Cupane, A., et al. (2008). IN13 backscattering spectrometer at ILL: Looking for motions in biological macromolecules and organisms. Neutron News, 19(4), 14–18. https://doi.org/10.1080/10448630802474083.
Strunz, P., Mortensen, K., & Janssen, S. (2004). SANS-II at SINQ: Installation of the former Riso-SANS facility. Phys B - Cond Matt, 350, E783–E786.
Bée, M. (2003). Localized and long-range diffusion in condensed matter: State of the art of QENS studies and future prospects. Chemical Physics, 292(2–3), 121–141.
Doster, W. (2006). Dynamical structural distributions in proteins. Physica B, 385–386, 831–834.
Peters, J., Trapp, M., Hughes, D., Rowe, S., Demé, B., Laborier, J.-L., et al. (2011). High hydrostatic pressure equipment for neutron scattering studies of samples in solutions. High Pressure Research, 32(1), 97–102.
Lelièvre-Berna, E., Demé, B., Gonthier, J., Gonzales, J. P., Maurice, J., Memphis, Y., et al. (2017). 700 MPa sample stick for studying liquid samples or solid-gas reactions down to 1.8 K and up to 550 K. Journal of Neutron Research, 19, 77–84.
Sidorov, V. A., & Sadykov, R. A. (2005). Hydrostatic limits of Fluorinert liquids used for neutron and transport studies at high pressure. Journal of Physics: Condensed Matter, 17, 3005–3008.
Woese, C. R., Kandler, O., & Wheelis, M. L. (1990). Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proceedings of the National Academy of Sciences U S A, 87(12), 4576–4579.
Rampelotto, P. H. (2013). Extremophiles and extreme environments. Life (Basel), 3(3), 482–485. https://doi.org/10.3390/life3030482.
Albers, S. V., & Meyer, B. H. (2011). The archaeal cell envelope. Nature Reviews Microbiology, 9(6), 414–426. https://doi.org/10.1038/nrmicro2576.
Jebbar, M., Franzetti, B., Girard, E., & Oger, P. (2015). Microbial diversity and adaptation to high hydrostatic pressure in deep-sea hydrothermal vents prokaryotes. Extremophiles, 19(4), 721–740. https://doi.org/10.1007/s00792-015-0760-3.
Atomi, H., Fukui, T., Kanai, T., Morikawa, M., & Imanaka, T. (2004). Description of Thermococcus kodakaraensis sp. nov., a well studied hyperthermophilic archaeon previously reported as Pyrococcus sp. KOD1. Archaea, 1, 263–267.
Marteinsson, V. T., Birrien, J. L., Reysenbach, A. L., Vernet, M., Marie, D., Gambacorta, A., et al. (1999). Thermococcus barophilus sp. nov., a new barophilic and hyperthermophilic archaeon isolated under high hydrostatic pressure from a deep-sea hydrothermal vent. International Journal of Systematic and Evolutionary Microbiology, 49(2), 351–359. https://doi.org/10.1099/00207713-49-2-351.
Peters, J., Martinez, N., Michoud, G., Cario, A., Franzetti, B., Oger, P., et al. (2014). Deep sea microbes probed by incoherent neutron scattering under high hydrostatic pressure. Zeitschrift für Physikalische Chemie, 228, 1121–1133.
Martinez, N., Michoud, G., Cario, A., Ollivier, J., Franzetti, B., Jebbar, M., et al. (2016). High protein flexibility and reduced hydration water dynamics are key pressure adaptive strategies in prokaryotes. Scientific Reports, 6, 32816. https://doi.org/10.1038/srep32816.
Bratbak, G. (1985). Bacterial biovolume and biomass estimations. Applied and Environment Microbiology, 49, 1488–1493.
Dellerue, S., & Bellissent-Funel, M. C. (2000). Relaxational dynamics of water molecules at protein surface. Chemical Physics, 258, 315–325.
Schiro, G., Fichou, Y., Gallat, F. X., Wood, K., Gabel, F., Moulin, M., et al. (2015). Translational diffusion of hydration water correlates with functional motions in folded and intrinsically disordered proteins. Nature Communications, 6, 6490. https://doi.org/10.1038/ncomms7490.
Perticaroli, S., Ehlers, G., Stanley, C. B., Mamontov, E., O’Neill, H., Zhang, Q., et al. (2017). Description of hydration water in protein (green fluorescent protein) solution. Journal of the American Chemical Society, 139(3), 1098–1105. https://doi.org/10.1021/jacs.6b08845.
Peters, J., Martinez, N., Trovaslet, M., Scannapieco, K., Koza, M. M., Masson, P., et al. (2016). Dynamics of human acetylcholinesterase bound to non-covalent and covalent inhibitors shedding light on changes to the water network structure. Physical Chemistry Chemical Physics: PCCP, 18(18), 12992–13001. https://doi.org/10.1039/c6cp00280c.
Van Hove, L. (1954). Correlations in space and time and born approximation scattering in systems of interacting particles. Physical Review, 95(1), 249–262.
Natali, F., Dolce, C., Peters, J., Gerelli, Y., Stelletta, C., & Leduc, G. (2013). Water dynamics in neural tissue. Journal of the Physical Society of Japan, 82(Suppl. A), SA017.
Volino, F., & Dianoux, A. J. (1980). Neutron incoherent-scattering law for diffusion in a potential of spherical-symmetry: General formalism and application to diffusion inside a sphere. Molecular Physics, 41(2), 271–279. https://doi.org/10.1080/00268978000102761.
Martinko, M. T. M. J. M., & Parker, J. (2006). Brock’s biology of microorganism 11th. New Jersey: Prentice Hall.
Martinez, N., Natali, F., & Peters, J. (2015). mQfit, a new program for analyzing quasi-elastic neutron scattering data. EPJ Web of Conferences, 83(3010), 3011–3014.
Stadler, A. M., Embs, J. P., Digel, I., Artmann, G. M., Unruh, T., Buldt, G., et al. (2008). Cytoplasmic water and hydration layer dynamics in human red blood cells. Journal of the American Chemical Society, 130(50), 16852–16853. https://doi.org/10.1021/ja807691j.
Jasnin, M., Stadler, A. M., Tehei, M., & Zaccai, G. (2010). Specific cellular water dynamics observed in vivo by neutron scattering and NMR. Physical Chemistry Chemical Physics: PCCP, 12, 10154–10160.
Laggner, P., & Müller, K. (1978). The structure of serum lipoproteins as analysed by X-ray small-angle scattering. Quarterly Reviews of Biophysics, 11, 371–425.
Krieger, M. (1998). The “best” of cholesterols, the “worst” of cholesterols: a tale of two receptors. Proceedings of the National Academy of Sciences of the United States of America, 95, 4077–4080.
Muller, K., Laggner, P., Glatter, O., & Kostner, G. (1978). The structure of human-plasma low-density lipoprotein B. An X-ray small-angle scattering study. European Journal of Biochemistry, 82, 73–90.
Maric, S., Lind, T. K., Lyngso, J., Cardenas, M., & Pedersen, J. S. (2017). Modeling small-angle X-ray scattering data for low-density lipoproteins: Insights into the fatty core packing and phase transition. ACS Nano, 11, 1080–1090.
Orlova, E. V., Sherman, M. B., Chiu, W., Mowri, H., Smith, L. C., & Gotto, A. M. (1999). Three-dimensional structure of low density lipoproteins by electron cryomicroscopy. Proceedings of the National Academy of Sciences, 96, 8420–8425.
Liu, Y., & Atkinson, D. (2011). Enhancing the contrast of ApoB to locate the surface components in the 3D density map of human LDL. Journal of Molecular Biology, 405, 274–283.
Liu, Y. H., & Atkinson, D. (2011). Immuno-electron cryo-microscopy imaging reveals a looped topology of apoB at the surface of human LDL. Journal of Lipid Research, 52, 1111–1116.
Vea, Kumar. (2011). Three-dimensional cryoEM reconstruction of native LDL particles to 16 angstrom resolution at physiological body temperature. PLoS ONE, 6, e18841.
Prassl, R., & Laggner, P. (2009). Molecular structure of low density lipoprotein: Current status and future challenges. European Biophysics Journal, 38(2), 145–158. https://doi.org/10.1007/s00249-008-0368-y.
Benjamin, E. J., et al. (2017). Heart disease and stroke statistics—2017 update: A report from the American Heart Association. Circulation, 135, e146–e603.
Deckelbaum, R. J., Shipley, G. G., Small, D. M., Lees, R. S., & George, P. K. (1975). Thermal transitions in human plasma low density lipoproteins. Science, 190, 392–394.
Wanderlingh, U., D’Angelo, G., Branca, C., Nibali, V. C., Trimarchi, A., Rifici, S., et al. (2014). Multi-component modeling of quasielastic neutron scattering from phospholipid membranes. J Chem Phys, 140(17), 174901. https://doi.org/10.1063/1.4872167.
Golub, M., Lehofer, B., Martinez, N., Ollivier, J., Kohlbrecher, J., Prassl, R., et al. (2017). High hydrostatic pressure specifically affects molecular dynamics and shape of low-density lipoprotein particles. Scientific Reports, 7, 46034. https://doi.org/10.1038/srep46034.
Peters, J., Golub, M., Demé, B., Gonthier, J., Payre, C., Maurice, J., Sadykov, R., Lelièvre-Berna, E. (2018) A new high pressure cell going up to 100 °C. Rev Sc Instr., To be submitted.
Acknowledgements
This work has been supported by the Austrian Science Fund (FWF Project No. I 1109-N28 to R. P.) and by two projects financed by the Agence Nationale de la Recherche (ANR; project number ANR 2010 BLAN 1725 01 Living deep and project number ANR-12-ISV5-0002-01 LDLPRESS to J.P.). We thank the ILL for allocation of beamtime and the SANE group of ILL for their support to develop the HHP equipment and C. Payre and J. Maurice for their help to perform the experiments. The work is partially based on experiments performed at the Swiss spallation neutron source SINQ, Paul Scherrer Institute, Villigen, Switzerland. The work benefitted from SasView software, originally developed by the DANSE project under NSF award DMR-0520547. We are gratefully acknowledging the help of the local contacts on the various instruments, in particular B. Frick, M. M. Koza, J. Ollivier, J. Kohlbrecher and G. Nagy. We wish to thank our many co-workers for their help and fruitful discussions, in particular N. Martinez, G. Michoud, A. Cario, B. Franzetti, M. Jebbar, B. Lehofer and M. Golub.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
Peters, J., Prassl, R., Oger, P. (2018). Probing the Structure and Dynamics of Cells, Cell Components and Endogenous Nanoparticles Under Extreme Conditions with Neutrons. In: Artmann, G., Artmann, A., Zhubanova, A., Digel, I. (eds) Biological, Physical and Technical Basics of Cell Engineering. Springer, Singapore. https://doi.org/10.1007/978-981-10-7904-7_18
Download citation
DOI: https://doi.org/10.1007/978-981-10-7904-7_18
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-10-7903-0
Online ISBN: 978-981-10-7904-7
eBook Packages: EngineeringEngineering (R0)