Disentangling the role of extracellular polysaccharides in desiccation tolerance in lichen‐forming microalgae. First evidence of sulfated polysaccharides and ancient sulfotransferase genes

• Published in: Environmental microbiology Vol. 22; no. 8; pp. 3096 - 3111
• Main Authors: González‐Hourcade, María, Campo, Eva M., Braga, Marcia R., Salgado, Antonio, Casano, Leonardo M.
• Format: Journal Article
• Language: English
• Published: Hoboken, USA John Wiley & Sons, Inc 01.08.2020; Wiley Subscription Services, Inc; Wiley-Blackwell
• Subjects: Algae; Analytical methods; Anion exchange; anion exchange chromatography; Anion exchanging; Anions; Biochemical composition; Carbohydrates; Cell Wall - physiology; Cell walls; chemical composition; Chlorophyta - genetics; Chlorophyta - physiology; Chromatography; Coccomyxa; Composition; Dehydration; Desiccation; drought tolerance; Electrophoresis; Environmental changes; Extracellular; Gas chromatography; Gel electrophoresis; Gels; Genes; Lichens; Mass spectrometry; Mass spectroscopy; Microalgae; Microalgae - physiology; microbiology; Molecular weight; Monosaccharides; NMR; Nuclear magnetic resonance; nuclear magnetic resonance spectroscopy; Phytoplankton; Polymers; Polysaccharides; Polysaccharides - metabolism; Rehydration; Saccharides; Stress, Physiological - physiology; Sugar; Sulfates - chemistry; Sulfotransferase; Sulfotransferases - genetics; Trebouxia; Ultrastructure; Uronic acid; Water availability
• ISSN: 1462-2912; 1462-2920; 1462-2920
• DOI: 10.1111/1462-2920.15043

Summary Trebouxia sp. TR9 and Coccomyxa simplex are desiccation‐tolerant microalgae with flexible cell walls, which undergo species‐specific remodelling during dehydration–rehydration (D/R) due to their distinct ultrastructure and biochemical composition. Here, we tested the hypothesis that extracellular polysaccharides excreted by each microalga could be quantitatively and/or qualitatively modified by D/R. Extracellular polysaccharides were analysed by size exclusion and anion exchange chromatography, specific stains after gel electrophoresis and gas chromatography/mass spectrometry of trimethylsilyl derivatives (to determine their monosaccharide composition). The structure of a TR9‐sulfated polymer was deduced from nuclear magnetic resonance (NMR) analyses. In addition, sugar‐sulfotransferase encoding genes were identified in both microalgae, and their expression was measured by RT‐qPCR. D/R did not alter the polydispersed profile of extracellular polysaccharides in either microalga but did induce quantitative changes in several peaks. Furthermore, medium‐low‐sized uronic acid‐containing polysaccharides were almost completely substituted by higher molecular mass carbohydrates after D/R. Sulfated polysaccharide(s) were detected, for the first time, in the extracellular polymeric substances of both microalgae, but only increased significantly in TR9 after cyclic D/R, which induced a sugar‐sulfotransferase gene and accumulated sulfated ß‐D‐galactofuranan(s). Biochemical remodelling of extracellular polysaccharides in aeroterrestrial desiccation‐tolerant microalgae is species‐specific and seems to play a role in the response to changes in environmental water availability.