Declarations
Funding. This study was supported by the Austrian Science Fund
(FWF) grant I 1951-B16 to AH. The research stay of AH 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).
Conflicts of interest/Competing interests. The authors declare
no conflicts of interest.
Availability of data and material . New DNA sequence
data are accessed in NCBI GenBank. Raw physiological data and scripts
for data analysis were deposited to DRYAD repository and
GitHub/eterlova/TetradesmusPhysiology.
Figure legends
Fig. 1 Phylogenetic tree of desert and aquaticTetradesmus species based on BI of tuf A, rbc L, and
ITS 2 rDNA. Numbers associated with the nodes indicate support values
for BI and ML analysis, respectively. Strains used in the desiccation
experiments indicated with a dot (a black dot for the strains from the
original experiment, gray dots indicate strains desiccated in a second
experiment, see the supplementary materials). Habitats of origin
(aquatic, temperate soils, or desert soil crusts) are indicated by the
color of a bar (blue, brown, and orange, respectively).
Fig. 2 Example trace of the desiccation/rehydration cycle. In
black (left y-axis): representative example of raw measurements of PSII
effective yield of a desert alga (T. adustus , strain LG2-VF29)
taken every 10 min during desiccation to 65% RH, and rehydration. Data
points correspond to the mean of four ΦPSIImeasurements, error bars indicate one standard deviation. In gray (right
y-axis) is RH recorded during desiccation and rehydration. A rapid
decrease in humidity coinciding with the shift from desiccation to
rehydration was by the opening of the desiccation chamber to replace the
desiccant with water for algae rehydration.
Fig. 3 Examples of typical responses to desiccation and
rehydration (a) by aquatic and desert Tetradesmus and (b) to
different desiccation modes by a desert species. Each data point
represents mean ΦPSII (n=4), measurements were taken
every 10 min. (a) Behavior of T. obliquus (aquatic species),T. deserticola , and T. bajacalifornicus (desert taxa) when
desiccated at 65% RH. (b) Response of T. deserticola to
desiccation under three conditions (RH 5%, 65% and 80%). We used
cluster analysis to differentiate among cell physiological states
(hydrated, desiccating, or rehydrated).
Fig. 4 Hierarchical cluster analyses of recovery indices (ratio
of a rehydrated value to the initial hydrated photosynthetic yield) ofTetradesmus across desiccation treatments demonstrate that the
habitat of the species (aquatic or terrestrial) as well as the
desiccation mode influence their ability to recover from desiccation.
(a) After 10 min of rehydration all desert algae are able to re-initiate
their photosynthetic activity rapidly upon rehydration, and aquatic
algae do not, although there is variation among strains of most
species). (b) After 12 h of rehydration the difference in recovery from
different desiccation modes became apparent. Within-species variation in
the aquatic taxon is clear under the gentlest desiccation at 80% RH.
Cluster number on the x-axis represents distinct groups (identified in
cluster analysis of Euclidean distances, verified with gap statistic).
Symbol shape indicated the native habitat of each species (circles for
aquatic and triangles for terrestrial), color indicates the individual
species. Multiple symbols of the same color correspond to different
strains of each species.
Fig. 5 TEM photographs of an aquatic and terrestrialTetradesmus in hydrated, desiccated, and rehydrated states. (a)
Ultrastructure of the aquatic species Tetradesmus obliquus (UTEX
393). (b) Ultrastructure of the desert species T. deserticola(EM2-VF30). Arrows point at plastoglobuli. GA - Golgi body, Chl -
chloroplast, M - mitochondrion, N - nucleus, P – pyrenoid.
Fig. 6 Fluorescence photomicrographs of an aquatic and
terrestrial Tetradesmus in hydrated state, under osmotic stress,
and rehydrated. Effect of osmotic stress by 4M sorbitol on the cells ofT. obliquus UTEX 72 (a-c), T. dissociatus SAG 5/95 (d-f),
and T. deserticola SNI-2 (h-i) visualized by CLSM and
lipid-soluble fluorescent dye FM 1-43. (a) T. obliquus fully
hydrated control cells, only plasma membrane was exposed to the dye. (b)T. obliquus cells under osmotic stress, arrow points to the
fracture in the cell membrane. (c) T. obliquus rehydrated cells
with the dye binding to the intracellular material, indicating the
damage to the plasma membrane by desiccation. (d)T. dissociatus hydrated
cells. (e) T. dissociatus under osmotic stress, no indication of
membrane damage. (f) T. dissociatus rehydrated cells the membrane
preserved its integrity. (g) T. deserticola hydrated control
cells. (h) T. deserticola under osmotic stress, no indication of
membrane fracturing. (i) T. deserticola rehydrated, the membrane
integrity was preserved. Chl — chloroplast, P — pyrenoid.
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