Desiccation stress and tolerance in green algae: consequences for ultrastructure, physiological and molecular mechanisms

Abstract

Although most green algae typically occur in aquatic ecosystems, many species also live partly or permanently under aeroterrestrial conditions, where the cells are exposed to the atmosphere and hence regularly experience dehydration. The ability of algal cells to survive in an air-dried state is termed desiccation tolerance. The mechanisms involved in desiccation tolerance of green algae are still poorly understood, and hence the aim of this review is to summarize recent findings on the effects of desiccation and osmotic water loss. Starting from structural changes, physiological, and biochemical consequences of desiccation will be addressed in different green-algal lineages. The available data clearly indicate a range of strategies, which are rather different in streptophycean and non-streptophycean green algae. While members of the Trebouxiophyceae exhibit effective water loss-prevention mechanisms based on the biosynthesis and accumulation of particular organic osmolytes such as polyols, these compounds are so far not reported in representatives of the Streptophyta. In members of the Streptophyta such as Klebsormidium, the most striking observation is the appearance of cross-walls in desiccated samples, which are strongly undulating, suggesting a high degree of mechanical flexibility. This aids in maintaining structural integrity in the dried state and allows the cell to maintain turgor pressure for a prolonged period of time during the dehydration process. Physiological strategies in aeroterrestrial green algae generally include a rapid reduction of photosynthesis during desiccation, but also a rather quick recovery after rewetting, whereas aquatic species are sensitive to drying. The underlying mechanisms such as the affected molecular components of the photosynthetic machinery are poorly understood in green algae. Therefore, modern approaches based on transcriptomics, proteomics, and/or metabolomics are urgently needed to better understand the molecular mechanisms involved in desiccation-stress physiology of these organisms. The very limited existing information is described in the present review.

Keywords: aeroterrestrial algae; cell wall; dehydration; desiccation tolerance; osmolyte; phylogeny of green algae; soluble carbohydrates; turgor pressure.

FIGURE 1

Schematic representation of desiccation-induced phenomena in green algae from different habitats.

FIGURE 2

Different habitats of desiccation-tolerant green algae, on anthropogenic (A,B) or natural (C–G) surfaces. (A) Aeroterrestrial biofilm dominated by Apatococcus sp., growing on roof tiles in Rostock, Germany, (B) detail from the same roof, note the biofilm only on the rain-exposed tiles, (C) Apatococcus sp. on bark of tree, Innsbruck, Tyrol, (D) Trentepohlia sp. on rock surface, Innsbruck, Tyrol, (E) Biological soil crust dominated by Klebsormidium sp. and Stichococcus sp., pine forest near Innsbruck, (F) Epilithic green algae on shaded rock surface, Tulfes, Tyrol, (G) Zygnema sp. mat near Ny Alesund, Svalbard (G reprinted from Holzinger et al., 2009 with permission from Elsevier).

FIGURE 3

The effect of desiccation and rehydration on the optimum quantum yield (Fv/Fm) in Klebsormidium crenulatum and Klebsormidium dissectum isolated from an alpine biological soil crust, and in Zygogonium ericetorum collected from an adjacent intermittent streamlet (data adapted from Karsten et al., 2010; Karsten and Holzinger, 2012; Aigner et al., 2013).

FIGURE 4

Comparisons of hydrated and experimentally desiccated cells of the streptophytic green alga Klebsormidium crenulatum observed by light- (A,B) and confocal laser scanning microscopy (C–F). (A) cells form liquid culture, (B) cells desiccated for 1 day at ~5% RH and observed in immersion oil, note the loss of diameter (arrows), (C) mitochondrial staining in hydrated cells, (D) mitochondrial staining in 1-day desiccated (~5% RH) cells, (E) F-actin staining in hydrated cells, (F) severely damaged F-actin in 1-day desiccated (~5% RH) cells. Bars 10 μm (reprinted from Holzinger et al., 2011 with permission from the Phycological Society of America).

FIGURE 5

Comparisons of the ultrastructure of hydrated and experimentally desiccated cells of the streptophytic green alga Klebsormidium. (A) hydrated cells from liquid culture, observed by scanning electron microscopy, (B) 7-day desiccated (~5% RH) cells, with severely damaged cell walls (arrow), (C) transmission electron micrograph of high-pressure frozen freeze-substituted cells from liquid culture, (D) desiccated cells (1 day, ~5% RH), cytoplasm appears electron-dense with nucleus and chloroplast still visible, cell walls are irregularly shaped and the cross-walls show an undulating structure (arrows). Bars (A,B) 10 μm, (C,D) 1 μm. Chl, chloroplast; CW, cell wall; N, nucleus (A,B reprinted from Holzinger et al., 2011 with permission of the Phycological Society of America; C,D reprinted from Karsten and Holzinger, 2012 with permission from Springer Science and Business Media).