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Terrestrial Green Algae Show Higher Tolerance to Dehydration than Do Their Aquatic Sister-Species

Abstract

Diverse algae possess the ability to recover from extreme desiccation without forming specialized resting structures. Green algal genera such as Tetradesmus (Sphaeropleales, Chlorophyceae) contain temperate terrestrial, desert, and aquatic species, providing an opportunity to compare physiological traits associated with the transition to land in closely related taxa. We subjected six species from distinct habitats to three dehydration treatments varying in relative humidity (RH 5%, 65%, 80%) followed by short- and long-term rehydration. We tested the capacity of the algae to recover from dehydration using the effective quantum yield of photosystem II as a proxy for physiological activity. The degree of recovery was dependent both on the habitat of origin and the dehydration scenario, with terrestrial, but not aquatic, species recovering from dehydration. Distinct strains of each species responded similarly to dehydration and rehydration, with the exception of one aquatic strain that recovered from the mildest dehydration treatment. Cell ultrastructure was uniformly maintained in both aquatic and desert species during dehydration and rehydration, but staining with an amphiphilic styryl dye indicated damage to the plasma membrane from osmotically induced water loss in the aquatic species. These analyses demonstrate that terrestrial Tetradesmus possess a vegetative desiccation tolerance phenotype, making these species ideal for comparative omics studies.

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Data Availability

New DNA sequence data are available in NCBI GenBank. Raw physiological data and scripts for data analysis were deposited to DRYAD (doi:10.5061/dryad.sqv9s4n1t).

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Acknowledgments

The authors thank Dr. X. Sun and Dr. M. Abril from the Bioscience Electron Microscopy Laboratory at University of Connecticut for their help in sample preparation and assistance with TEM, and C. O’Connell from the Advanced Light Microscopy Facility at UConn for assistance with fluorescence microscopy. We thank Dr. P. Lewis for advice about the ancestral states analyses, and Drs. B. Goffinet, N. Patel, J. Seemann, Y. Yuan, J. Wegrzyn, and two anonymous reviewers for their helpful comments.

Funding

This study was supported by the Austrian Science Fund (FWF) grant I 1951-B16 to A.H. The research stay of A.H. at the University of Connecticut was generously supported by a Fulbright Scholarship. TEM and CLSM imaging of cells was supported by 2017 UConn EEB Research Award (The Betty Foster Feingold Endowment for Ecology and Evolutionary Biology to the Department of Ecology and Evolutionary Biology).

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Correspondence to Elizaveta F. Terlova.

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Terlova, E.F., Holzinger, A. & Lewis, L.A. Terrestrial Green Algae Show Higher Tolerance to Dehydration than Do Their Aquatic Sister-Species. Microb Ecol 82, 770–782 (2021). https://doi.org/10.1007/s00248-020-01679-3

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Keywords

  • Desert algae
  • Vegetative desiccation tolerance
  • Dehydration
  • PSII fluorescence
  • Cell ultrastructure