The Under-explored Extracellular Proteome of Aero-Terrestrial Microalgae Provides Clues on Different Mechanisms of Desic

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PHYSIOLOGY AND BIOTECHNOLOGY

The Under-explored Extracellular Proteome of Aero-Terrestrial Microalgae Provides Clues on Different Mechanisms of Desiccation Tolerance in Non-Model Organisms María González-Hourcade 1

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Eva M. del Campo 1

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Leonardo M. Casano 1

Received: 18 July 2020 / Accepted: 16 September 2020 # Springer Science+Business Media, LLC, part of Springer Nature 2020

Abstract Trebouxia sp. (TR9) and Coccomyxa simplex (Csol) are desiccation-tolerant lichen microalgae with different adaptive strategies in accordance with the prevailing conditions of their habitats. The remodelling of cell wall and extracellular polysaccharides depending on water availability are key elements in the tolerance to desiccation of both microalgae. Currently, there is no information about the extracellular proteins of these algae and other aero-terrestrial microalgae in response to limited water availability. To our knowledge, this is the first report on the proteins associated with the extracellular polymeric substances (EPS) of aero-terrestrial microalgae subjected to cyclic desiccation/rehydration. LC-MS/MS and bioinformatic analyses of the EPSassociated proteins in the two lichen microalgae submitted to four desiccation/rehydration cycles allowed the compilation of 111 and 121 identified proteins for TR9 and Csol, respectively. Both sets of EPS-associated proteins shared a variety of predicted biological functions but showed a constitutive expression in Csol and partially inducible in TR9. In both algae, the EPSassociated proteins included a number of proteins of unknown functions, some of which could be considered as small intrinsically disordered proteins related with desiccation-tolerant organisms. Differences in the composition and the expression pattern between the studied EPS-associated proteins would be oriented to preserve the biochemical and biophysical properties of the extracellular structures under the different conditions of water availability in which each alga thrives. Keywords Exoproteome . Extracellular . Desiccation . Rehydration . Secretome . Microalgae . Coccomyxa simplex . Trebouxia sp.

Introduction Extracellular polymeric substances (EPS) are highly hydrated polymers produced by a wide range of microorganisms. Microbial EPS facilitate water retention, cell adhesion, signalling and protection from abiotic and biotic environmental stresses. This mucous mass surrounding cells or group of cells is mainly composed by complex polysaccharides and proteins [1]. In spite of the high diversity of substances secreted beyond the plasma Electronic supplementary material The online version of this article (https://doi.org/10.1007/s00248-020-01604-8) contains supplementary material, which is available to authorized users. * Eva M. del Campo [email protected] 1

Department of Life Sciences, University of Alcalá, 28805, Alcalá de Henares, Madrid, Spain

membrane, secretomics is usually considered within the frame of proteomics as a compilation of proteins exported into the extracellular space [2]. In plants, the