Versatility of the green microalga cell vacuole function as revealed by analytical transmission electron microscopy

Abstract

Vacuole is a multifunctional compartment central to a large number of functions (storage, catabolism, maintenance of the cell homeostasis) in oxygenic phototrophs including microalgae. Still, microalgal cell vacuole is much less studied than that of higher plants although knowledge of the vacuolar structure and function is essential for understanding physiology of nutrition and stress tolerance of microalgae. Here, we combined the advanced analytical and conventional transmission electron microscopy methods to obtain semi-quantitative, spatially resolved at the subcellular level information on elemental composition of the cell vacuoles in several free-living and symbiotic chlorophytes. We obtained a detailed record of the changes in cell and vacuolar ultrastructure in response to environmental stimuli under diverse conditions. We suggested that the vacuolar inclusions could be divided into responsible for storage of phosphorus (mainly in form of polyphosphate) and those accommodating non-protein nitrogen (presumably polyamine) reserves, respectively.The ultrastructural findings, together with the data on elemental composition of different cell compartments, allowed us to speculate on the role of the vacuolar membrane in the biosynthesis and sequestration of polyphosphate. We also describe the ultrastructural evidence of possible involvement of the tonoplast in the membrane lipid turnover and exchange of energy and metabolites between chloroplasts and mitochondria. These processes might play a significant role in acclimation in different stresses including nitrogen starvation and extremely high level of CO and might also be of importance for microalgal biotechnology. Advantages and limitations of application of analytical electron microscopy to biosamples such as microalgal cells are discussed.

Phosphorus Feast and Famine in Cyanobacteria: Is Luxury Uptake of the Nutrient Just a Consequence of Acclimation to Its Shortage?

“…The microalgal samples for transmission electron microscopy (TEM), including nanoscale elemental analysis in TEM using energy-dispersive X-ray (EDX) spectroscopy and energy-filtered (EF)TEM cell section mapping, were prepared and processed as described previously [ 39 ]. All quantitative morphometric analyses were done as described previously [ 40 ].…”

“…Since the analysis of the residual P i is simpler, it was routinely employed in this work. The intracellular PolyP content was assayed by 4′,6-diamidino-2-phenylindole (DAPI) staining ([ 39 ]; for more detail, please refer to online Supplementary Materials ).…”

Perspectives for Glyco-Engineering of Recombinant Biopharmaceuticals from Microalgae

“…Moreover, the microalga P. tricornutum naturally expresses paucimannosidic fucosylated N-glycans [109]. Although the function of microalgal vacuole is still under-characterized compared to higher plants [150], subcellular localization engineering might result in successful production of paucimannosidic biopharmaceuticals in microalgae. Interestingly, microalgal vacuole signal peptides for P. tricornutum have been identified [151].…”

Ultrastructural patterns of photoacclimation and photodamage to photosynthetic algae cell under environmental stress

“…Chl) during its stress‐induced reduction is accomplished by the vacuoles, although participation of plastoglobuli in Chl degradation was also suggested in A. thaliana (Lundquist et al ). The latter are organelles with multi‐faceted function central to the development of the microalgal cell and its responses to stress (Shebanova et al ). Vacuoles in microalgal cell, as in higher plant cell, fulfill the function of lytic compartments, serve as a depot of ions and metabolites important for cell homeostasis, and play a pivotal role in the detoxication of potentially harmful compounds.…”

“…Relatively mild stresses like phosphorus shortage and moderate irradiance exposure as well as recovery from them might be manifested, in particular, as peculiar epichloroplastic membranous structures (EMS) termed as ‘twirls’ ending up in a lytic vacuole (Baulina et al , Shebanova et al ). A hypothetic mechanism of their formation involves putative imbalance in the generation of the chloroplast envelope membranes.…”