Plastid thylakoid architecture optimizes photosynthesis in diatoms

Abstract

Photosynthesis is a unique process that allows independent colonization of the land by plants and of the oceans by phytoplankton. Although the photosynthesis process is well understood in plants, we are still unlocking the mechanisms evolved by phytoplankton to achieve extremely efficient photosynthesis. Here, we combine biochemical, structural and in vivo physiological studies to unravel the structure of the plastid in diatoms, prominent marine eukaryotes. Biochemical and immunolocalization analyses reveal segregation of photosynthetic complexes in the loosely stacked thylakoid membranes typical of diatoms. Separation of photosystems within subdomains minimizes their physical contacts, as required for improved light utilization. Chloroplast 3D reconstruction and in vivo spectroscopy show that these subdomains are interconnected, ensuring fast equilibration of electron carriers for efficient optimum photosynthesis. Thus, diatoms and plants have converged towards a similar functional distribution of the photosystems although via different thylakoid architectures, which likely evolved independently in the land and the ocean.

ppGpp influences protein protection, growth and photosynthesis inPhaeodactylum tricornutum

“…The diatom chloroplast differs in a number of aspects from the chloroplast of plants and green algae. At the level of membrane architecture, the diatom chloroplast is surrounded by four membranes, and the thylakoids are loosely stacked with three interconnected membranes (Flori et al , 2017). Moreover, the light-harvesting complex (LHC) of diatoms is known as the Fucoxanthin Chlorophyll Protein complex (FCP), and is composed of tetramers containing chlorophyll c and the carotenoid fucoxanthin (Lepetit et al , 2012; Roding et al , 2018; Nagao et al , 2019; Pi et al , 2019).…”

In-cell quantitative structural imaging of phytoplankton using 3D electron microscopy

“…However, optical microscopy studies have insufficient resolution to reveal microstructural features, emphasising the need to develop complementary imaging approaches to study the cellular and subcellular bases of phytoplankton physiology and cell biology. Recently, a few studies (Decelle et al, 2019;Engel et al, 2015;Flori et al, 2017) have highlighted the potential of 3D electron microscopy (EM) imaging to explore these fundamental aspects of phytoplankton. This is a critical aspect, since previous work has suggested, for instance, that the physiology and metabolism of diatoms are determined by their peculiar cell organisations and more particularly by the morphology and arrangement of key energy-producing machineries, such as the plastids and mitochondria (Bailleul et al, 2015;Flori et al, 2017).…”

“…Here, we present a complete imaging workflow to access the cellular and subcellular features of phytoplankton at the nanometric scale based on Focused Ion Beam -Scanning Electron Microscopy (FIB-SEM) (Hawes and Hummel, 2015;Narayan and Subramaniam, 2015;Titze and Genoud, 2016). This technique has already been applied successfully to provide 3D models of eukaryotic cells (Decelle et al, 2019;Flori et al, 2017;Gavelis et al, 2019). Although the spatial resolution of FIB-SEM (4-8 nm) is lower than the resolution of transmission electron microscopy (Engel et al, 2015;Wietrzynski et al, 2020), it has the advantage of providing contextual 3D images of whole cells at a specific time.…”

The singular properties of photosynthetic cytochrome c550 from the diatom Phaeodactylum tricornutum suggest new alternative functions

“…In order to optimize photosynthetic efficiency, the chloroplasts of diatoms display a refined thylakoid architecture (Flori et al ), which includes the presence of the pyrenoid, an electron‐dense semicrystalline protein aggregate present in the chloroplast of most unicellular eukaryotic algae. It is considered that CO 2 fixation occurs in the pyrenoid, where the enzyme ribulose‐1,5‐bisphosphate carboxylase/oxygenase (RubisCO) is preferentially localized, accounting for over 90% of the pyrenoid's protein content (reviewed in Badger et al , Meyer et al ).…”