Abstract
Quasielastic neutron scattering (QENS) is an ideal technique for studying water transport and relaxation dynamics at pico- to nanosecond timescales and at length scales relevant to cellular dimensions. Studies of high pressure dynamic effects in live organisms are needed to understand Earth’s deep biosphere and biotechnology applications. Here we applied QENS to study water transport in Shewanella oneidensis at ambient (0.1 MPa) and high (200 MPa) pressure using H/D isotopic contrast experiments for normal and perdeuterated bacteria and buffer solutions to distinguish intracellular and transmembrane processes. The results indicate that intracellular water dynamics are comparable with bulk diffusion rates in aqueous fluids at ambient conditions but a significant reduction occurs in high pressure mobility. We interpret this as due to enhanced interactions with macromolecules in the nanoconfined environment. Overall diffusion rates across the cell envelope also occur at similar rates but unexpected narrowing of the QENS signal appears between momentum transfer values Q = 0.7–1.1 Å−1 corresponding to real space dimensions of 6–9 Å. The relaxation time increase can be explained by correlated dynamics of molecules passing through Aquaporin water transport complexes located within the inner or outer membrane structures.
Highlights
Processes both in aqueous media and for biologically important macromolecules[10,11]
We tested our approach by examining water dynamics in the bulk aqueous buffer solutions (non isotopically substituted buffer Hydrogenated buffer (Hb); perdeuterated (98%) buffer Deuterated buffer (Db)) that served as the bacterial growth and suspension media for our experiments
Focusing on the main narrow component associated with translational relaxation, fitting the full width at half maximum (FWHM) Γ T(Q2) relations to a Singwi-Sjölander (SS) jump model[7] led to diffusion coefficients DT = 2.70±0.20 × 10−5 and 2.00±0.11 × 10−5 cm2s−1 for Hb and Db, respectively, at ambient conditions (Fig. 2A,B, Table 1)
Summary
Processes both in aqueous media and for biologically important macromolecules[10,11]. We extended the application of the QENS technique to investigate water dynamics in H/D substituted samples of live Shewanella oneidensis bacteria at ambient (0.1 MPa) and high (200 MPa) pressures relevant to subsurface biological processes. Observations of live bacteria at > 10 km below the ocean surface as well as samples recovered from continental and suboceanic drilling projects have revealed microbial lifeforms existing at up to at least P = 110 MPa12,13. Understanding the behavior of microorganisms exposed to HP conditions is necessary to optimize food preservation and other biotechnologies where pressures in the 200–700 MPa range are applied to eliminate harmful bacteria[14]. We selected S. oneidensis as a model for our study This prokaryotic organism exists under both aerobic and anaerobic conditions and its genus contains several piezophilic (“pressure-loving”) species[15,16,17]. S. oneidensis has been investigated to study its pressure adaptation and survival under conditions extending into the GigaPascal (P > 1 GPa) range[20,23]
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