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Nitrogen limitation and slow drying induce desiccation tolerance in conjugating green algae (Zygnematophyceae, Streptophyta) from polar habitats.

Pichrtová M, Kulichová J, Holzinger A - PLoS ONE (2014)

Bottom Line: Nitrogen-free cultures (liquid as well as solidified) consisted of well-developed pre-akinetes after this period.Desiccation experiments were performed at three different drying rates (rapid: 10% relative humidity, slow: 86% rh and very slow); viability, effective quantum yield of PS II, visual and ultrastructural changes were monitored.Pre-akinetes, modified vegetative cells, rather than specialized stages of the life cycle, can be hardened by mild desiccation stress to survive rapid drying.

View Article: PubMed Central - PubMed

Affiliation: Charles University in Prague, Faculty of Science, Department of Botany, Prague, Czech Republic; Academy of Sciences of the Czech Republic, Institute of Botany, Třeboň, Czech Republic.

ABSTRACT

Background: Filamentous Zygnematophyceae are typical components of algal mats in the polar hydro-terrestrial environment. Under field conditions, they form senescent vegetative cells, designated as pre-akinetes, which are tolerant to desiccation and osmotic stress.

Key findings: Pre-akinete formation and desiccation tolerance was investigated experimentally under monitored laboratory conditions in four strains of Arctic and Antarctic isolates with vegetative Zygnema sp. morphology. Phylogenetic analyses of rbcL sequences revealed one Arctic strain as genus Zygnemopsis, phylogenetically distant from the closely related Zygnema strains. Algae were cultivated in liquid or on solidified medium (9 weeks), supplemented with or lacking nitrogen. Nitrogen-free cultures (liquid as well as solidified) consisted of well-developed pre-akinetes after this period. Desiccation experiments were performed at three different drying rates (rapid: 10% relative humidity, slow: 86% rh and very slow); viability, effective quantum yield of PS II, visual and ultrastructural changes were monitored. Recovery and viability of pre-akinetes were clearly dependent on the drying rate: slower desiccation led to higher levels of survival. Pre-akinetes survived rapid drying after acclimation by very slow desiccation.

Conclusions: The formation of pre-akinetes in polar Zygnema spp. and Zygnemopsis sp. is induced by nitrogen limitation. Pre-akinetes, modified vegetative cells, rather than specialized stages of the life cycle, can be hardened by mild desiccation stress to survive rapid drying. Naturally hardened pre-akinetes play a key role in stress tolerance and dispersal under the extreme conditions of polar regions, where sexual reproduction and production of dormant stages is largely suppressed.

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Effective quantum yield (ΦPSII) under different desiccation scenarios.A–D: rapid desiccation, approximately 10% relative humidity (rh); E–H: slow desiccation, 86% rh; I–L: very slow desiccation, 86% rh plus additional moistening of samples with 10 µl BBM. All strains shown were pre-cultivated on regular agar medium (A BBM) or on medium without nitrate (A BBM-N). Results are means ± standard deviations of four independent experimental replicates.
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pone-0113137-g004: Effective quantum yield (ΦPSII) under different desiccation scenarios.A–D: rapid desiccation, approximately 10% relative humidity (rh); E–H: slow desiccation, 86% rh; I–L: very slow desiccation, 86% rh plus additional moistening of samples with 10 µl BBM. All strains shown were pre-cultivated on regular agar medium (A BBM) or on medium without nitrate (A BBM-N). Results are means ± standard deviations of four independent experimental replicates.

Mentions: The initial values of ΦPSII differed between the A BBM and A BBM-N cultures for each strain and were always lower in the starved culture (GLM ANOVA, Tukey's post-hoc tests, n = 12, p<0.001; Fig. 4). Following the transfer into the desiccation chambers, ΦPSII started to decrease and the rate of the decline differed according to the desiccation scenario. Over silica gel (rh around 10%), the samples began to desiccate almost immediately and ΦPSII dropped to zero within 10–20 minutes, indicating the complete cessation of physiological activity (Fig. 4A–D). By contrast, it took up to 50 minutes for the ΦPSII to reach its lowest value in samples desiccated at 86% rh (Fig. 4E–H). When the samples were moistened with 10 µl L BBM medium prior to desiccation at 86% rh, the ΦPSII remained unchanged for several hours before the values began to drop, with the lowest values being reached as late as 8–9 hours after the beginning of the experiment (Fig. 4I–L). Markedly, in some strains, cultures pre-grown on A BBM lost their physiological activity much faster than those pre-cultivated on A BBM-N (Fig. 4A, E, F, G and K). Zygnemopsis sp. L cultivated on A BBM-N showed very small ΦPSII values (around 0.1), even prior to any experimental manipulation, indicating the very low performance of this strain under starvation conditions. These initial values did not change, regardless of the desiccation regimes applied (Fig. 4D, H and L).


Nitrogen limitation and slow drying induce desiccation tolerance in conjugating green algae (Zygnematophyceae, Streptophyta) from polar habitats.

Pichrtová M, Kulichová J, Holzinger A - PLoS ONE (2014)

Effective quantum yield (ΦPSII) under different desiccation scenarios.A–D: rapid desiccation, approximately 10% relative humidity (rh); E–H: slow desiccation, 86% rh; I–L: very slow desiccation, 86% rh plus additional moistening of samples with 10 µl BBM. All strains shown were pre-cultivated on regular agar medium (A BBM) or on medium without nitrate (A BBM-N). Results are means ± standard deviations of four independent experimental replicates.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4232603&req=5

pone-0113137-g004: Effective quantum yield (ΦPSII) under different desiccation scenarios.A–D: rapid desiccation, approximately 10% relative humidity (rh); E–H: slow desiccation, 86% rh; I–L: very slow desiccation, 86% rh plus additional moistening of samples with 10 µl BBM. All strains shown were pre-cultivated on regular agar medium (A BBM) or on medium without nitrate (A BBM-N). Results are means ± standard deviations of four independent experimental replicates.
Mentions: The initial values of ΦPSII differed between the A BBM and A BBM-N cultures for each strain and were always lower in the starved culture (GLM ANOVA, Tukey's post-hoc tests, n = 12, p<0.001; Fig. 4). Following the transfer into the desiccation chambers, ΦPSII started to decrease and the rate of the decline differed according to the desiccation scenario. Over silica gel (rh around 10%), the samples began to desiccate almost immediately and ΦPSII dropped to zero within 10–20 minutes, indicating the complete cessation of physiological activity (Fig. 4A–D). By contrast, it took up to 50 minutes for the ΦPSII to reach its lowest value in samples desiccated at 86% rh (Fig. 4E–H). When the samples were moistened with 10 µl L BBM medium prior to desiccation at 86% rh, the ΦPSII remained unchanged for several hours before the values began to drop, with the lowest values being reached as late as 8–9 hours after the beginning of the experiment (Fig. 4I–L). Markedly, in some strains, cultures pre-grown on A BBM lost their physiological activity much faster than those pre-cultivated on A BBM-N (Fig. 4A, E, F, G and K). Zygnemopsis sp. L cultivated on A BBM-N showed very small ΦPSII values (around 0.1), even prior to any experimental manipulation, indicating the very low performance of this strain under starvation conditions. These initial values did not change, regardless of the desiccation regimes applied (Fig. 4D, H and L).

Bottom Line: Nitrogen-free cultures (liquid as well as solidified) consisted of well-developed pre-akinetes after this period.Desiccation experiments were performed at three different drying rates (rapid: 10% relative humidity, slow: 86% rh and very slow); viability, effective quantum yield of PS II, visual and ultrastructural changes were monitored.Pre-akinetes, modified vegetative cells, rather than specialized stages of the life cycle, can be hardened by mild desiccation stress to survive rapid drying.

View Article: PubMed Central - PubMed

Affiliation: Charles University in Prague, Faculty of Science, Department of Botany, Prague, Czech Republic; Academy of Sciences of the Czech Republic, Institute of Botany, Třeboň, Czech Republic.

ABSTRACT

Background: Filamentous Zygnematophyceae are typical components of algal mats in the polar hydro-terrestrial environment. Under field conditions, they form senescent vegetative cells, designated as pre-akinetes, which are tolerant to desiccation and osmotic stress.

Key findings: Pre-akinete formation and desiccation tolerance was investigated experimentally under monitored laboratory conditions in four strains of Arctic and Antarctic isolates with vegetative Zygnema sp. morphology. Phylogenetic analyses of rbcL sequences revealed one Arctic strain as genus Zygnemopsis, phylogenetically distant from the closely related Zygnema strains. Algae were cultivated in liquid or on solidified medium (9 weeks), supplemented with or lacking nitrogen. Nitrogen-free cultures (liquid as well as solidified) consisted of well-developed pre-akinetes after this period. Desiccation experiments were performed at three different drying rates (rapid: 10% relative humidity, slow: 86% rh and very slow); viability, effective quantum yield of PS II, visual and ultrastructural changes were monitored. Recovery and viability of pre-akinetes were clearly dependent on the drying rate: slower desiccation led to higher levels of survival. Pre-akinetes survived rapid drying after acclimation by very slow desiccation.

Conclusions: The formation of pre-akinetes in polar Zygnema spp. and Zygnemopsis sp. is induced by nitrogen limitation. Pre-akinetes, modified vegetative cells, rather than specialized stages of the life cycle, can be hardened by mild desiccation stress to survive rapid drying. Naturally hardened pre-akinetes play a key role in stress tolerance and dispersal under the extreme conditions of polar regions, where sexual reproduction and production of dormant stages is largely suppressed.

Show MeSH
Related in: MedlinePlus