快速脱水与复水过程中2种藓类植物的活性氧代谢与脂质过氧化特征

以来自不同水分生境的金发藓和湿地匐灯藓为材料,对二者在脱水与复水胁迫条件下的活性氧代谢、脂质过氧化损伤程度及其抗氧化系统应答的差异进行比较研究。结果显示:在脱水与复水过程中,(1)硅胶快速脱水更接近阳光直射条件下藓类植物的水分丧失。(2)随着含水量的变化,湿地匐灯藓虽然能够在复水后迅速修复细胞的完整性,但变化剧烈;金发藓则能够始终维持较低的膜透性。(3)2种藓类植物的丙二醛(MDA)含量变化均呈先升后降趋势,但金发藓的MDA含量明显低于湿地匐灯藓。(4)2种藓类植物的超氧阴离子自由基(O2.-)产生速率和过氧化氢含量(H2O2)的变化均与MDA含量变化相似,且金发藓活性氧水平明显高于湿地匐灯藓。(5)2种藓类植物的超氧化物歧化酶(SOD)、过氧化氢酶(CAT)和抗坏血酸过氧化物酶(APX)活性受活性氧诱导亦呈先升后降的趋势,但金发藓抗氧化酶对活性氧迸发的应答更快,活性更强。(6)2种藓类植物的抗坏血酸(AsA)含量呈先降后升态势,但金发藓的含量低于湿地匐灯藓。研究表明,来自不同生境的2种藓类植物对脱水胁迫所致的氧化胁迫均具有很强的适应能力,尤其是复水过程中的修复能力,但不同藓类可能通过不同途径和机制来适应脱水所致的氧化胁迫;来自易发生水分亏缺生境的金发藓可能因具有更强抗氧化能力,从而获得比来自水分充沛生境的湿地匐灯藓更高的脱水耐性。     

The discovery,scope, and puzzle of desiccation tolerance in plants

The modern scientific study of desiccation tolerance began in 1702 when Anthony von Leeuwenhoek discovered that rotifers could survive without water for months. By 1860, the controversy over whether organisms could dry up without dying had reached such a pitch that a special French commission was convened to adjudicate the dispute. In 2000, we know that a few groups of animals and a wide variety of plants can tolerate desiccation in the active, adult stages of their life cycles. Among plants, this includes many lichens and bryophytes, a few ferns, and a very few flowering plants, but no gymnosperms nor trees. Some desiccation-tolerant species can survive without water for over ten years, recover from desiccation to unmeasurably low water potentials, and, when plants are desiccated, endure temperature extremes from ?272 to 100 °C. Desiccation-tolerant plants occur on all continents but mainly in xeric habitats or microhabitats where the cover of desiccation-sensitive species is low. Two main puzzles arise from these patterns: What are the mechanisms by which plants tolerate desiccation? and Why are desiccation-tolerant plants not more ecologically widespread? Recent molecular and biochemical studies suggest that there are multiple mechanisms of tolerance, many of which involve protection from oxidants and from the loss of configuration of macromolecules during dehydration. Hypotheses to explain the restricted ecological range of desiccation-tolerance plants include inability to maintain a cumulative positive carbon balance during repeated cycles of wetting and drying and inherent trade offs between desiccation tolerance and growth rate.

     

Changes in chlorophyll a fluorescence, photosynthetic CO2 assimilation and xanthophyll cycle interconversions during dehydration in desiccation-tolerant and intolerant liverworts

The interactions among water content, chlorophyll a fluorescence emission, xanthophyll interconversions and net photosynthesis were analyzed during dehydration in desiccation-tolerant Frullania dilatata (L.) Dum. and desiccation-intolerant Pellia endiviifolia (Dicks) Dum. Water loss led to a progressive suppression of photosynthetic carbon assimilation in both species. Their chlorophyll fluorescence characteristics at low water content were: low photosynthetic quantum conversion efficiency, high excitation pressure on photosystem II and strong non-photochemical quenching. However, dissipation activity was lower in P. endiviifolia and was not accompanied by a rise in the concentration of de-epoxidised xanthophylls as F. dilatata. The photosynthetic apparatus of F. dilatata remained fully and speedily recuperable after desiccation in as indicated by the restoration of chlorophyll fluorescence parameters to pre-desiccation values upon rehydration. A lack of recovery upon remoistening of P. endiviifolia indicated permanent and irreversible damage to photosystem II. The results suggest that F. dilatata possesses a desiccation-induced zeaxanthin-mediated photoprotective mechanism which might aid photosynthesis recovery when favourable conditions are restored by alleviating photoinhibitory damage during desiccation. This avoidance mechanism might have evolved as an adaptative response to repeated cycles of desiccation and rehydration that represent a real threat to photosynthetic viability. Received: 12 January 1998 / Accepted: 14 July 1998     

Analysis of the decrease in photosynthesis on desiccation of mosses from xeric and hydric environments

Three moss species [ Tortula ruraliformis (Besch.) Grout. Bryum pseudotriquetrum (Hedw.) Schaegr and Dicranella palustris (Dicks.) Crund. ex. E. F. Warb. ( D. squarrosa (Starke) Schp.] collected from a range of habitats differing in water availability were desiccated in controlled conditions. All species became photosynthetically inactive when dried below a water content of 100–200% dry weight. Only Tortula ruraliformis , a moss from arid sand dunes. was able to recover fully to pre-desiccated rates of photosynthetic electron transport during subsequent rehydration. The rate of recovery was influenced by irradiance during desiccation. Mosses from hydric habitats showed some resumption of photosynthetic electron transport (following rehydration) if dried in the dark. but did not do so if dried even in low light. In these circumstances the mosses showed evidence of lasting photoinhibition of photosynthesis after rehydration. The desiccation-tolerant T. ruraliformis became significantly photoinhibited only when continually exposed to high irradiance (1200 μmol m⁻² s⁻¹) in the hydrated state. If allowed to desiccate whilst exposed to high irradiance this species showed less evidence of photoinhibition after rehydration, and was not at all affected by desiccation in low irradiance. Photon flux absorption in dry moss was 50–60% less than that in hydrated moss as a result of leaf curling. However, the reduction in absorption of photosynthetically active radiation cannot account for the total loss of photosynthetic oxygen evolution and variable chlorophyll fluorescence observed in the desiccated mosses.     

Changes in photosynthetic rate and stress volatile emissions through desiccation‐rehydration cycles in desiccation‐tolerant epiphytic filmy ferns (Hymenophyllaceae)

Exposure to recurrent desiccation cycles carries a risk of accumulation of reactive oxygen species that can impair leaf physiological activity upon rehydration, but changes in filmy fern stress status through desiccation and rewatering cycles have been poorly studied. We studied foliage photosynthetic rate and volatile marker compounds characterizing cell wall modifications (methanol) and stress development (lipoxygenase [LOX] pathway volatiles and methanol) through desiccation–rewatering cycles in lower‐canopy species Hymenoglossum cruentum and Hymenophyllum caudiculatum, lower‐ to upper‐canopy species Hymenophyllum plicatum and upper‐canopy species Hymenophyllum dentatum sampled from a common environment and hypothesized that lower canopy species respond more strongly to desiccation and rewatering. In all species, rates of photosynthesis and LOX volatile emission decreased with progression of desiccation, but LOX emission decreased with a slower rate than photosynthesis. Rewatering first led to an emission burst of LOX volatiles followed by methanol, indicating that the oxidative burst was elicited in the symplast and further propagated to cell walls. Changes in LOX emissions were more pronounced in the upper‐canopy species that had a greater photosynthetic activity and likely a greater rate of production of photooxidants. We conclude that rewatering induces the most severe stress in filmy ferns, especially in the upper canopy species.     

Photosynthesis and dark respiration in Antarctic mosses—an initial comparative study

Rates of dark respiration (DR), gross photosynthesis (GPS) and net photosynthesis (NPS) were investigated for 14 species of moss from a maritime Antarctic locality. The rates found were similar to those reported in studies of temperate, alpine and Arctic species, indicating no physiological specialisation to the Antarctic environment. There was no relationship between the habitat occupied by a species (hydric, mesic, xeric) and physiological measures. There was, however, a loose correlation between NPS and a species' ecology or reproductive behaviour in the maritime Antarctic — species with high NPS being either colonists or those that show high and regular investment in sporophyte production.     

哀牢山湿性常绿阔叶林树干4种附生苔藓植物的水分变化对光合、荧光参数的影响

以云南哀牢山湿性常绿阔叶林中的附生苔藓植物为对象,研究林内4种树干附生苔藓植物阿萨羽苔(Plagiochila assamica Steph.)、西南树平藓(Homaliodendron montagneanum(Müll.Hal.)M.Fleisch.)、刀叶树平藓(H.scalpellifolium(Mitt.)M.Fleisch.)、大羽藓(Thuidium cymbifolium(Dozy et Molk.)Dozy et Molk.)的吸水力、失水特征和脱水耐性,稳定碳同位素(δ~(13)C)值,以及水分变化对苔藓净光合速率和荧光参数的影响。结果显示:(1)4种附生苔藓植物均具有较强的吸水能力和较低持水力,脱水耐性较强,脱水后均可迅速复水;(2)4种附生苔藓植物的δ~(13)C值较低,其水分利用效率小于其他维管束植物;除大羽藓外,其余3种附生苔藓雨季的δ~(13)C值与水分利用效率均高于干季;(3)4种附生苔藓植物的净光合速率(Pn)随着含水量的降低而降低,在含水量小于60%~80%时,其最大光化学效率(Fv/Fm)急剧下降,反映出这些附生苔藓植物的光合、荧光特性对水分变化非常敏感。     

Differential proteomics of dehydration and rehydration in bryophytes: evidence towards a common desiccation tolerance mechanism

All bryophytes evolved desiccation tolerance (DT) mechanisms during the invasion of terrestrial habitats by early land plants. Are these DT mechanisms still present in bryophytes that colonize aquatic habitats? The aquatic bryophyte Fontinalis antipyretica Hedw. was subjected to two drying regimes and alterations in protein profiles and sucrose accumulation during dehydration and rehydration were investigated. Results show that during fast dehydration, there is very little variation in protein profiles, and upon rehydration proteins are leaked. On the other hand, slow dehydration induces changes in both dehydration and rehydration protein profiles, being similar to the protein profiles displayed by the terrestrial bryophytes Physcomitrella patens (Hedw.) Bruch and Schimp. and, to what is comparable with Syntrichia ruralis (Hedw.) F. Weber and D. Mohr. During dehydration there was a reduction in proteins associated with photosynthesis and the cytoskeleton, and an associated accumulation of proteins involved in sugar metabolism and plant defence mechanisms. Upon rehydration, protein accumulation patterns return to control values for both photosynthesis and cytoskeleton whereas proteins associated with sugar metabolism and defence proteins remain high. The current results suggest that bryophytes from different ecological adaptations may share common DT mechanisms.     

A field portable method for the semi‐quantitative estimation of dehydration tolerance of photosynthetic tissues across distantly related land plants

Desiccation tolerant (DT) plants withstand complete cellular dehydration, reaching relative water contents (RWC) below 30% in their photosynthetic tissues. Desiccation sensitive (DS) plants exhibit different degrees of dehydration tolerance (DHT), never surviving water loss >70%. To date, no procedure for the quantitative evaluation of DHT extent exists that is able to discriminate DS species with differing degrees of DHT from truly DT plants. We developed a simple, feasible and portable protocol to differentiate between DT and different degrees of DHT in the photosynthetic tissues of seed plants and between fast desiccation (< 24 h) tolerant (FDT) and sensitive (FDS) bryophytes. The protocol is based on (1) controlled desiccation inside Falcon tubes equilibrated at three different relative humidities that, consequently, induce three different speeds and extents of dehydration and (2) an evaluation of the average percentage of maximal photochemical efficiency of PSII (F_v/fm) recovery after rehydration. Applying the method to 10 bryophytes and 28 tracheophytes from various locations, we found that (1) imbibition of absorbent material with concentrated salt‐solutions inside the tubes provides stable relative humidity and avoids direct contact with samples; (2) for 50 ml capacity tubes, the optimal plant amount is 50–200 mg fresh weight; (3) the method is useful in remote locations due to minimal instrumental requirements; and (4) a threshold of 30% recovery of the initial F_v/fm upon reaching RWC ≤ 30% correctly categorises DT species, with three exceptions: two poikilochlorophyllous species and one gymnosperm. The protocol provides a semi‐quantitative expression of DHT that facilitates comparisons of species with different morpho‐physiological traits and/or ecological attributes.     

Desiccation Tolerance and Global Change: Implications for Tropical Bryophytes in Lowland Forests

Global change puts an increasing pressure on tropical forests and their inherent diversity by the risk of longer droughts and drier microclimatic conditions within the forest. How organisms will respond is uncertain, especially for organisms highly depending on their microclimatic environment such as bryophytes. An adequate tolerance to desiccation is important to face these changes, however, little is known for tropical bryophytes. We investigated for the first time the desiccation tolerance of epiphytic bryophytes from contrasting microsites at the tropical lowland forest in French Guiana. Using chlorophyll‐fluorescence (F_v/F_m) as an indicator of recovery, we tested: (1) desiccation tolerance for short (3 d) and long (9 d) desiccation events; (2) different desiccation intensities; and (3) recovery by rehydration with water vapor. Species from the canopy were well adapted to desiccation events. Thirteen of 18 species maintained more than 75 percent of their photosynthetic capacity after recovery at the strongest desiccation treatment of 9 d at 43 percent relative humidity (RH). In contrast, species from the understory were sensitive and withstood desiccation only at humid conditions of 75 percent RH and higher. The photosystem of the studied bryophytes was reactivated efficiently in equilibration with water vapor only—a yet neglected phenomenon in bryology. A novel introduced desiccation tolerance index allows global comparison of desiccation tolerances and highlights the sensitivity of understory species. Our results suggest that decreasing humidity caused by climate change and forest degradation could be a concerning threat for understory species.     

Desiccation resistance and water balance in southern African keratin beetles (Coleoptera, Trogidae): the influence of body size and habitat

Desiccation resistance and water balance were examined in the adults of seven trogid species, which differed both in body size and in the habitats from which they were collected. Body water contents (51–58% fresh mass) and desiccation rates at 27 °C (0.00026–0.00093 g h⁻¹) in these species were very similar to those of unrelated, similar-sized beetles from arid habitats. The keratin beetles differed markedly from many other adult Coleoptera by virtue of their very high haemolymph osmolality and inability to regulate haemolymph osmolality, and to catabolise lipids for water production, during desiccation. Like most other insects, the xeric trogid species had lower rates of water loss and longer survival times than trogids from mesic areas. This was due both to lower rates of water loss and to the larger body size of species from the more arid areas. Because absolute body water content was higher in large beetles than in small ones, larger body size conferred higher desiccation resistance on the very large Kalahari desert species. This suggests that there may be strong selection for large body size in such insects from arid areas. Most ecological and ecophysiological investigations of geographical variation in body size, and the species-body size distribution, have focused on temperature and metabolic rate as explanatory variables. This study suggests that attention should also be given to desiccation resistance. Accepted: 29 September 1997     

Geographic variation in adult and embryonic desiccation tolerance in a terrestrial-breeding frog

Intraspecific variation in the ability of individuals to tolerate environmental perturbations is often neglected when considering the impacts of climate change. Yet this information is potentially crucial for mitigating deleterious effects of climate change on threatened species. Here we assessed patterns of intraspecific variation in desiccation tolerance in the frog Pseudophryne guentheri, a terrestrial-breeding species experiencing a drying climate. Adult frogs were collected from six populations across a rainfall gradient and their dehydration and rehydration rates were assessed. We also compared desiccation tolerance of embryos and hatchlings originating from within-population parental crosses from four of the populations. Embryos were reared on soil at three soil–water potentials and their desiccation tolerance was assessed across a range of traits. We found significant and strong patterns of intraspecific variation in almost all traits, both in adults and first-generation offspring. Adult frogs exhibited clinal variation in their water balance responses, with populations from drier sites both dehydrating and rehydrating more slowly compared to frogs from more mesic sites. Similarly, desiccation tolerance of first-generation offspring was significantly greater in populations from xeric sites. Our findings suggest that populations within this species will respond differently to the regional reduction in rainfall predicted by climate change models.     

Energetic consequences of repeated and prolonged dehydration in the Antarctic midge, Belgica antarctica

Larvae of the Antarctic midge, Belgica antarctica, routinely face periods of limited water availability in their natural environments on the Antarctic Peninsula. As a result, B. antarctica is one of the most dehydration-tolerant insects studied, surviving up to 70% loss of its body water. While previous studies have characterized the physiological effects of a single bout of dehydration, in nature larvae are likely to experience multiple bouts of dehydration throughout their lifetime. Thus, we examined the physiological consequences of repeated dehydration and compared results to larvae exposed to a single, prolonged period of dehydration. For the repeated dehydration experiment, larvae were exposed to 1-5 cycles of 24 h dehydration at 75% RH followed by 24 h rehydration. Each bout of dehydration resulted in 30-40% loss of body water, with a concomitant 2- to 3-fold increase in body fluid osmolality. While nearly 100% of larvae survived a single bout of dehydration, <65% of larvae survived five such cycles. Larvae subjected to multiple bouts of dehydration also experienced severe depletion of carbohydrate energy reserves; glycogen and trehalose content decreased with each successive cycle, with larvae losing 89% and 48% of their glycogen and trehalose, respectively, after five cycles of dehydration/rehydration. Larvae exposed to prolonged dehydration (99% RH for 10d) had 26% less water, 43% less glycogen, and 27% less lipid content than controls, but did not experience any mortality. Thus, both repeated and prolonged dehydration results in substantial energetic costs that are likely to negatively impact fitness.     

Photosynthetic activity of homoiochlorophyllous desiccation tolerant plant <Emphasis Type="Italic">Haberlea rhodopensis</Emphasis> during dehydration and rehydration

The functional state of the photosynthetic apparatus of flowering homoiochlorophyllous desiccation tolerant plant Haberlea rhodopensis during dehydration and subsequent rehydration was investigated in order to characterize some of the mechanisms by which resurrection plants survive drought stress. The changes in the CO₂ assimilation rate, chlorophyll fluorescence parameters, thermoluminescence, fluorescence imaging and electrophoretic characteristics of the chloroplast proteins were measured in control, moderately dehydrated (50% water content), desiccated (5% water content) and rehydrated plants. During the first phase of desiccation the net CO₂ assimilation decline was influenced by stomatal closure. Further lowering of net CO₂ assimilation was caused by both the decrease in stomatal conductance and in the photochemical activity of photosystem II. Severe dehydration caused inhibition of quantum yield of PSII electron transport, disappearance of thermoluminescence B band and mainly charge recombination related to S₂Q_A⁻ takes place. The blue and green fluorescence emission in desiccated leaves strongly increased. It could be suggested that unchanged chlorophyll content and amounts of chlorophyll–proteins, reversible modifications in PSII electron transport and enhanced probability for non-radiative energy dissipation as well as increased polyphenolic synthesis during desiccation of Haberlea contribute to drought resistance and fast recovery after rehydration.     

Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats?

Bryophytes are a non-monophyletic group of three major lineages (liverworts, hornworts, and mosses) that descend from the earliest branching events in the phylogeny of land plants. We postulate that desiccation tolerance is a primitive trait, thus mechanisms by which the first land plants achieved tolerance may be reflected in how extant desiccation-tolerant bryophytes survive drying. Evidence is consistent with extant bryophytes employing a tolerance strategy of constitutive cellular protection coupled with induction of a recovery/repair mechanism upon rehydration. Cellular structures appear intact in the desiccated state but are disrupted by rapid uptake of water upon rehydration, but cellular integrity is rapidly regained. The photosynthetic machinery appears to be protected such that photosynthetic activity recovers quickly. Gene expression responds following rehydration and not during drying. Gene expression is translationally controlled and results in the synthesis of a number of proteins, collectively called rehydrins. Some prominent rehydrins are similar to Late Embryogenesis Abundant (LEA) proteins, classically ascribed a protection function during desiccation. The role of LEA proteins in a rehydrating system is unknown but data indicates a function in stabilization and reconstitution of membranes. Phylogenetic studies using a Tortula ruralis LEA-like rehydrin led to a re-examination of the evolution of desiccation tolerance. A new phylogenetic analysis suggests that: (i) the basic mechanisms of tolerance seen in modern day bryophytes have changed little from the earliest manifestations of desiccation tolerance in land plants, and (ii) vegetative desiccation tolerance in the early land plants may have evolved from a mechanism present first in spores.     

Effects of dehydration rate on physiological responses and survival after rehydration in larvae of the anhydrobiotic chironomid

Strategies to combat desiccation are critical for organisms living in arid and semi-arid areas. Larvae of the Australian chironomid Paraborniella tonnoiri resist desiccation by reducing water loss. In contrast, larvae of the African species Polypedilum vanderplanki can withstand almost complete dehydration, referred to as anhydrobiosis. For successful anhydrobiosis, the dehydration rate of P. vanderplanki larvae has to be controlled. Here, we desiccated larvae by exposing them to different drying regimes, each progressing from high to low relative humidity, and examined survival after rehydration. In larvae of P. vanderplanki, reactions following desiccation can be categorized as follows: (I) no recovery at all (direct death), (II) dying by unrepairable damages after rehydration (delayed death), and (III) full recovery (successful anhydrobiosis). Initial conditions of desiccation severely affected survival following rehydration, i.e. P. vanderplanki preferred 100% relative humidity where body water content decreased slightly. In subsequent conditions, unfavorable dehydration rate, such as more than 0.7 mg water lost per day, resulted in markedly decreased survival rate of rehydrated larvae. Slow dehydration may be required for the synthesis and distribution of essential molecules for anhydrobiosis. Larvae desiccated at or above maximum tolerable rates sometimes showed temporary recovery but died soon after.     

Ultrastructural responses of the desiccation tolerant plants Xerophyta viscosa and X. retinervis to dehydration and rehydration

This paper compares the changes in water content, chlorophyll a fluorescence and leaf ultrastructure during dehydration and rehydration in two desiccation tolerant plants Xerophyta viscosa and X. retinervis. Both species showed decreasing quantum efficiency of photosystem 2 (F_v/F_m) with decreasing water content. Extreme water loss observed after 25 d of dehydration resulted in considerable damage of leaf tissue ultrastructure. After rehydration, both species need several days to reconstitute their photosynthetic machinery.     

Tests of the contribution of acclimation to geographic variation in water loss rates of the West Indian lizard <Emphasis Type="Italic">Anolis cristatellus</Emphasis>

Phenotypic plasticity can contribute to the process of adaptive radiation by facilitating population persistence in novel environments. West Indian Anolis lizards provide a classic example of an adaptive radiation, in which divergence has occurred along two primary ecological axes: structural microhabitat and climate. Adaptive plasticity in limb morphology is hypothesized to have facilitated divergence along the structural niche axis in Anolis, but very little work has explored plasticity in physiological traits. Here, we experimentally ask whether Puerto Rican Anolis cristatellus from mesic and xeric habitats differ in desiccation rates, and whether these lizards exhibit an acclimation response to changes in relative humidity. We first present microclimatic data collected at lizard perch sites that demonstrate that abiotic conditions experienced by lizards differ between mesic and xeric habitat types. In Experiment 1, we measured desiccation rates of lizards from both habitats maintained under identical laboratory conditions. This experiment demonstrated that desiccation rates differ between populations; xeric lizards lose water more slowly than mesic lizards. In Experiment 2, lizards from each habitat were either maintained under the conditions of Experiment 1, or under extremely low relative humidity. Desiccation rates did not differ between lizards from the same habitat maintained under different treatments and xeric lizards maintained lower desiccation rates than mesic lizards within each treatment. Our results demonstrate that A. cristatellus does not exhibit an acclimation response to abrupt changes of hydric conditions, and suggest that tropical Anolis lizards might be unable to exhibit physiological plasticity in desiccation rates in response to varying climatic conditions.     

Response of Cyanobacteria and Algae from Antarctic Wetland Habitats to Freezing and Desiccation Stress

Antarctic wetlands are characterized by the presence of liquid water during short austral summer. Filamentous cyanobacteria are often dominant there and are exposed to severe conditions, of which the changes in the desiccation–rehydration and freeze–thaw cycles are two of the most stressful. Vigor, after freezing and desiccation, was laboratory tested in cyanobacterial and algal strains from wetland habitats collected in maritime and continental Antarctica. Whereas minor sub-zero temperatures (−4°C), demonstrating summer diurnal freeze–thaws did not cause significant damage on either cyanobacteria or algae, low sub-zero temperatures (−40, −100, −196°C), demonstrating annual winter freeze, caused little harm to cyanobacteria, but was fatal for more than 50% of the population of algae. Freezing and desiccation tolerance of these strains was compared using multiregression methods: cyanobacteria from continental Antarctica were significantly more tolerant to low sub-zero temperatures than similar strains from maritime Antarctica (P = 0.026; F = 3.66); and cyanobacteria from seepages habitat were less tolerant to freezing and desiccation than cyanobacteria from other wetlands (P = 0.002; F = 5.69).