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Review
. 2021 Apr 19:9:631370.
doi: 10.3389/fchem.2021.631370. eCollection 2021.

Small-Angle X-Ray and Neutron Scattering on Photosynthetic Membranes

Dainius Jakubauskas  1 , Kell Mortensen  1 , Poul Erik Jensen  2 , Jacob J K Kirkensgaard  1   2
Affiliations
Review

Small-Angle X-Ray and Neutron Scattering on Photosynthetic Membranes

Dainius Jakubauskas et al. Front Chem. .

Abstract

Ultrastructural membrane arrangements in living cells and their dynamic remodeling in response to environmental changes remain an area of active research but are also subject to large uncertainty. The use of noninvasive methods such as X-ray and neutron scattering provides an attractive complimentary source of information to direct imaging because in vivo systems can be probed in near-natural conditions. However, without solid underlying structural modeling to properly interpret the indirect information extracted, scattering provides at best qualitative information and at worst direct misinterpretations. Here we review the current state of small-angle scattering applied to photosynthetic membrane systems with particular focus on data interpretation and modeling.

Keywords: SANS; SAXS; photosynthesis; small-angle scattering; structural modeling; thylakoids.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
TEM images of photosynthetic membrane systems, revealing complex structural characteristics. (A) Etiolated maize prolamellar body. (B) Concentric Synechocystis sp. PCC 6803 cyanobacterial thylakoids. (C) Higher plant grana stacks of Arabidopsis Col0, interconnected by stromal thylakoids.
FIGURE 2
FIGURE 2
(A) General experimental setup. Incident radiation is collimated and penetrates the sample (green box). Scattering arising in 2θ direction and the resulting scattering vector q are depicted in light blue. A beamstop (white) blocks the primary radiation. (B) Isotropic 2-dimensional scattering pattern from nonaligned system. (C) Nonisotropic 2-dimensional scattering pattern from a magnetically aligned system.
FIGURE 3
FIGURE 3
(A) Illustration of structural model for a photosynthetic membrane system with a stack of double layered thylakoids. Neutron (light blue) and X-ray (red) SLD profiles are schematically depicted. (B) Full q-range model fits to SANS data from three independent replicas of Synechococcus sp. PCC 7002 [from Jakubauskas et al. (2019)]. (C) Extracted structural numbers from fits in B.
FIGURE 4
FIGURE 4
(A) X-ray scattering length densities for various molecules. (B) Dependence of neutron scattering length densities of lipid and protein moieties on D2O amount in the sample. (C) Contrast variation technique, where a photosynthetic membrane is visualized in different D2O buffers. The signal from lipid (5–25% D2O) or protein components (40–45% D2O) is “masked out.” The total scattering signal is enhanced in 100% D2O, as indicated by more intense colors than in 0% D2O.
FIGURE 5
FIGURE 5
(A) X-ray scattering curves of cyanobacterial systems: Synechocystis sp. PCC 6803 (WT), CB, CK, PAL mutants. (B) Plot of the peak positions from Liberton et al., 2013b. Circles are data values as reported and diamonds are the q values calculated using the Bragg equation (Eq. 2) with the lowest q value as the first-order peak.
FIGURE 6
FIGURE 6
Comparison of repeat distances obtained by SANS and TEM for isolated thylakoids and plant leaves.
FIGURE 7
FIGURE 7
SAXS pattern changes after single freeze–thaw cycle of prolamellar bodies. (A) Prior to freezing (thin line) and immediately after melting (thick line). (B) Difference between curves from (A) indexed to a Fd3m lattice [figure from Selstam et al. (2007)].
See this image and copyright information in PMC

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