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Buellia frigida
Scientific classification Edit this classification
Domain: Eukaryota
Kingdom: Fungi
Division: Ascomycota
Class: Lecanoromycetes
Order: Caliciales
Family: Caliciaceae
Genus: Buellia
Species:
B. frigida
Binomial name
Buellia frigida
Darb. (1910)
Synonyms[1][2]
  • Buellia quercina Darb. (1910)
  • Rinodina frigida (Darb.) C.W.Dodge (1948)
  • Beltraminia frigida (Darb.) C.W.Dodge (1973)

Buellia frigida is a species of saxicolous (rock-dwelling), crustose lichen in the family Caliciaceae. It was first described from samples collected from the British National Antarctic Expedition of 1901–1904. It is endemic to maritime and continental Antarctica, where it is common and widespread, at altitudes up to about 2,000 m (6,600 ft). The characteristic appearance of this lichen features shades of grey and black divided into small polygonal patterns. The crusts can generally grow up to 7 cm (2+3⁄4 in) in diameter (smaller sizes are more common), although neighbouring individuals may coalesce to form larger crusts. One of the defining characteristics of the lichen is a textured surface with deep cracks, creating the appearance of radiating lobes. These lobes, bordered by shallower fissures, give the lichen a distinctive appearance and textured surface.

In addition to its striking appearance, Buellia frigida shows adaptability to the harsh Antarctic climate conditions. The lichen has an extremely slow growth rate, estimated to be less than 1 mm (1⁄16 in) per century. Because of its ability to not only endure but to thrive in one of the Earth's coldest, harshest environments, Buellia frigida has been used as a model organism in astrobiology research. This lichen has been exposed to conditions simulating those encountered in space and on celestial bodies like Mars, including vacuum, ultraviolet radiation, and extreme dryness. B. frigida has demonstrated resilience to these space-related stressors, making it a candidate for studying how life can adapt to and potentially survive in the extreme environments found beyond Earth.

Taxonomy

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The lichen was formally described as a new species in 1910 by the British botanist Otto Darbishire. The type specimen was collected in 1902 by Reginald Koettlitz from Granite Harbour in McMurdo Sound; it was found growing on tuff. This and other samples were obtained as part of the British National Antarctic Expedition of 1901–1904. The diagnosis of the lichen was as follows (translated from Latin[note 1]):

Thick crust, brownish-gray, continuous or more often discontinuous, forming small spots, fissured and broken, often somewhat tubercular-granulous, with a darker and distinct margin, and a separate hypothallus; apothecia black, initially immersed in the thallus, marginate, later emerging, unmarginate, flat or convex, 0.5–1.0 mm wide; epithecium black or occasionally (in the same specimen) decolourised; hypothecium darkening to brownish or occasionally decolourised or carbonaceous; apothecia occasionally containing gonidia in an amphithecium (similar to Rinodina species), but when mature, always without an amphithecium; spores eight, brown, bicellular, 0.009–0.015 mm.

Darbishire observed that the newly described species appeared to belong to the genus Buellia. However, he noted that in its early stages of development, the apothecium sometimes had lecanorine characteristics, which led to some similarities with genus Rinodina. He also pointed out that the hypothecium, a specific layer of tissue in the lichen's apothecium, was often carbonaceous (blackened), particularly near the edges of the apothecium. Darbishire acknowledged the close relationship between the genera Buellia and Rinodina.[3] In 1948, Carroll William Dodge proposed to transfer the taxon to genus Rinodina; however, the name Rinodina frigida was not validly published by Dodge.[1] Later, in 1973, Dodge thought Beltraminia was a more appropriate genus for the taxon and he provided a description of the species as Beltraminia frigida in his work Lichen Flora of the Antarctic Continent and Adjacent Islands.[4] The genus Beltraminia has since been synonymised with Dimelaena.[5] In her 1968 monograph on Antarctic lichens, Elke Mackenzie agreed with Darbishire's original generic placement in Buellia, largely because of the lecideine structure of the mature apothecia, wherein the disc lacks a thalline margin.[2]

Darbishire also simultaneously described Buellia quercina, collected at the same type locality as B. frigidia, but with a more effigurate margin and lighter colour. MacKenzie proposes that there should be no taxonomic value placed in variations in the black, grey, and whitish colours of the thallus owing to variations in anatomical structure of the lichen, and has "no hesitation in reducing B. quercina to synonymy".[2]

A 2016 molecular phylogenetics study of the Caliciaceae included B. frigida in its analysis. In the constructed phylogenetic tree, this species was identified as sister (closest evolutionary relative) to Amandinea coniops; the clade containing these two species was itself sister to Amandinea punctata. The authors note that the genus Buellia itself is not monophyletic, and suggest that the phylogenetic positioning of B. frigida warrants further investigation.[6]

Description

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Buellia frigida is a crustose lichen (sometimes placodioid) with a variable thallus size, more or less circular in outline. It has a diameter of up to 7 cm (2+3⁄4 in), although it is often much smaller. The thallus is characterised by a black hypothallus that extends approximately 5–7.5 millimetres (3⁄16–5⁄16 in) beyond the older central region of thallus;[4] this black area represents the growth zone.[7] In some instances, neighbouring thalli coalesce to form larger aggregations of up to 50 cm (20 in).[8] Its margin is somewhat fimbriate, sometimes barely visible, and its older, central thallus has a deeply rimose appearance, giving rise to the impression of radiating marginal lobes. These lobes are further defined by shallower cracks, creating a surface divided into polygonal areoles. The areoles have a somewhat cerebriform (brainlike) texture and can vary in colour from grey to black, with the tips of the marginal lobes typically appearing black. An amorphous layer, approximately 35–40 μm thick, covers the thallus.[4] This layer, mucilaginous in nature, may appear white when it is dry.[7]

Closeup of thallus surface in older central region, comprising angular grey to black areoles

The upper cortex of B. frigida is about 6–7 μm thick. It has a rounded or swollen top (capitate) and grows in a dense, upright, and parallel arrangement (fastigiate). However, it appears as a single layer of dark, thick-walled cells that are equal in diameter in all dimensions (isodiametric). The algal layer within the thallus varies in thickness, containing cells of Trebouxia measuring between 4–7 μm in diameter. The medulla, composed of loosely woven, thin-walled hyphae that are somewhat vertically arranged, also has variability in thickness.[4] The medulla stabilises the thallus structure and helps regulate water retention and gas exchange in the lichen.[7] Beneath the medulla, there is a basal layer, approximately 15 μm thick, of compact dark brown cells that elongate upward and merge with the medullary hyphae.[4] Medullary hyphae also help the thallus adhere tightly to the substratum.[7]

Buellia frigida forms black, slightly shiny apothecia, which are often more or less sessile on the older areoles. The apothecia start as flat discs but become convex as they mature. When young, they have a lecanorine appearance;[4] when mature they are lecideine in form, and up to about 1 mm in diameter.[7] The amphithecial cortex is about 15–17 μm thick, formed by a palisade of isodiametric cells. Algae that initially exist between the medullary hyphae disappear as the apothecia age. The medulla of the apothecia consists of vertical brown hyphae that are loosely woven and connected to the thalline medulla. The proper margin is not differentiated in older apothecia; instead, the amphithecial cortex darkens, and the medullary hyphae shrink together after the algae disappear, creating the impression of a dimidiate proper margin (i.e. divided into two equal or nearly equal halves). The hypothecium is brownish, with a thickness ranging from 30 to 80 μm in the centre and thinning towards the margin, where it merges with the amphithecial cortex. The ascus, which contains the ascospores, stands approximately 90–110 μm tall. Paraphyses, measuring 2 μm in diameter, darken above the asci and have an internal partition, or septum. The asci are clavate, with dimensions of 36–46 by 14.5–17 μm, and contain dark brown, bilocular ascospores (divided into two segments by a septum). These ascospores are occasionally only slightly constricted at the septum, and some may remain unilocular. They are typically ellipsoid, with dimensions of 9–13 by 5–8 μm.[4]

Asexual propagules, such as isidia or soredia, are not made by Buellia frigida.[7] The lichen, however, does create pycnidia that originate from under the algal layer, appearing ampulliform (with a rounded or bulbous form with a narrower portion or neck) to irregular and reaching sizes of up to 300 μm in diameter. A thin perifulcrum, consisting of very small-celled pseudoparenchyma, surrounds the pycnidia. Conidiophores have a few septa and are branched at the base, measuring approximately 10 by 1 μm. The terminal conidia are ellipsoid, measuring about 4 by 1 μm in size.[4]

Similar species

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Buellia subfrigida, described in 1993 and found in the Lützow-Holm Bay area and the Prince Olav Coast of East Antarctica, shares a close relationship with Buellia frigida. Both species are part of a species pair, with B. subfrigida likely evolving from the sexually reproducing B. frigida through the acquisition of soredia. Morphologically and chemically, these two species are similar. They both form circular thalli with distinct effigurate lobes at their margins, and have similar chemical profiles. However, B. subfrigida can be distinguished by its sorediate thallus. This adaptation allows B. subfrigida to grow in habitats that are seasonally inundated with water, a niche where B. frigida, despite its wide ecological amplitude (the limits of environmental conditions within which an organism can live and function), is rarely observed.[9]

Habitat, distribution, and ecology

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Pseudephebe minuscula (left) and Usnea sphacelata (right) are lichens that often establish themselves on the thalli of Buellia frigida in the Antarctic environment.

Buellia frigida is endemic to the maritime and continental Antarctic, where it grows in ice-free areas on exposed rock surfaces.[8] On these surfaces, it colonises more frequently in sheltered areas like crevasses or drainage channels. Within crevasses, chains of thalli commonly enlarge closer to the ground. In its habitat, Buellia frigida is often the only species capable of establishing on smooth, ice-polished rock. Once its thallus is about 2 cm (1 in) or more in diameter, Pseudephebe minuscula or Usnea sphacelata often begin growing near its centre. This secondary lichen growth leads to the degradation of underlying B. frigida, leaving outer rings of healthy crustose lichen.[10] The umbilicate lichen Umbilicaria decussata is another species that has been recorded growing on Buellia frigida.[11] Buellia frigida forms associations with various species in distinct habitats. Near Syowa Station, a limited community primarily consisting of Buellia frigida and Rhizocarpon flavum is found on slopes devoid of nesting colonies of petrels and other birds. Conversely, the nitrogen-enriched areas beneath bird nests have a more diverse lichen community, which, in addition to B. frigida, includes species from the genera Caloplaca, Umbilicaria, and Xanthoria.[12] Phaeosporobolus usneae is a lichenicolous (lichen-dwelling) fungus that has been found parasitising the thalli of B. frigida in Bunger Hills (Wilkes Land).[8]

The distribution of Buellia frigida spans across Antarctica, from the Peninsula to rocky coastal areas and exposed rock formations in the interior.[8] It is the most widespread lichen in east Antarctica, including the Larsemann Hills,[13] but it is somewhat rare in Marie Byrd Land and the King Edward VII Land, becoming more frequent in Victoria Land and most common on Antarctica's eastern coast.[4] It is most abundant in Victoria Land's dry valley region and higher elevations above 600 m (2,000 ft), known for cloud cover and summer snow.[14] The lichen has been found at altitudes of up to 2,015 m (6,611 ft).[8] About 2,500 m (8,200 ft) is considered to be the altitudinal limit at which lichens can survive in the Antarctic. Above this height, the long periods of exposure to −60 to −70 °C (−76 to −94 °F) winter temperatures and the lack of insulating snow cover on windblown rock faces is too harsh to support lichen life.[15] On the less lichen-populated Antarctic Peninsula, it is confined to the western part, south of 67°S latitude. Collections of Buellia frigida are typically made in coastal areas, and it is not known how far inland the lichen occurs in the interior of the continent.[2]

Physiological adaptations and growth

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Several Buellia frigida thalli growing around the base of a large rock; photographed in 2015 as part of the GANOVEX 11 expedition in northern Victoria Land

This lichen is routinely exposed to high fluxes of photosynthetically active radiation, desiccation, and cold temperatures.[8] The Net Assimilation Rate (NAR) gauges the rate at which an organism, typically a plant or lichen, converts light and carbon dioxide into organic substances through photosynthesis, minus the rate of respiration. Buellia frigida's maximum NAR occurs at 10 °C (50 °F), given full thallus hydratation. This metric sheds light on the lichen's photosynthetic efficiency in polar ecosystems.[16] Buellia frigida is well adapted to the harsh conditions of Antarctica. Its dark colouration is the result of pigmentation that helps protect it from harmful ultraviolet radiation, which is even greater at high latitudes and altitudes.[15] When the lichen thallus is hydrated, it becomes swollen, which reduces the density of its black pigmentation in the cortex. This effectively allows the algal layer to become exposed to light, enabling photosynthesis. In contrast, when the lichen becomes dry, the thallus again shrinks, increasing the density of its pigmentation and shielding itself from light; this effect is most prevalent in the marginal areas, which contain the most algae.[7] In situ measurements of this lichen's photosynthetic activity were conducted in continental Antarctica, revealing that it thrives in its habitat. Its high photosynthetic rate indicates adaptation to Antarctica's extreme conditions like low temperatures and intense light. This adaptability is crucial for its survival in this region, where it is exposed to fluctuating moisture levels due to drying cycles of meltwater-soaked thalli.[17] The photobiont partner of Buellia frigida has a higher cold resistance potential and a longer retention of photosynthetic capacity during exposure to freezing temperatures than the counterpart photobiont of several other Antarctic and European lichens.[18]

Moisture availability is a crucial aspect Buellia frigida's distribution. At Cape Geology, southern Victoria Land, it primarily relies on meltwater from snowpack and occasional snowfalls for moisture in early summer. Despite the strong sunlight, the lichen appears well-adapted to the combination of hydration, low temperatures, and intense light exposure. The distribution of lichen thalli on rock surfaces is influenced by the frequency and duration of meltwater moistening, showing its dependence on moisture availability.[19]

Research in continental Antarctica reveals the extremely slow radial growth rates of Buellia frigida. In an ecological monitoring study conducted in Yukidori Valley, no measurable increase in size was noted for any of the measured thalli after a five-year period.[20] In the McMurdo Dry Valleys, the lichen growth rates varied across different sites, suggesting a response to climate changes in the region, including alterations in snowfall patterns. This adaptation over time demonstrates the lichen's resilience to changing environmental conditions in Antarctica, emphasizing its role as a potential indicator of climate change in the region.[21] Geographic information system technology has been used to detect subtle changes in the growth of Buellia frigida over a 42-year period.[22] Based on a radial growth rate of less than 1 millimetre (1⁄16 in) per century, some thalli are estimated to be well over 1000 years old.[23]

Additionally, studies on the population genetics of Buellia frigida indicate limited dispersal among regions in Antarctica, likely influenced by prevailing wind patterns and physical barriers such as glaciers. While the spores of B. frigida have the potential for wind-assisted dispersal, the lichen predominantly colonises specific areas conducive to its growth, particularly those with sufficient moisture during the short Antarctic summer, indicating a selective dispersal pattern influenced by environmental factors.[24] In another study, samples of B. frigida collected from eastern Antarctica's Vestfold Hills and Mawson Station were genetically analysed, finding minimal genetic variation: only three genotypes in the Vestfold Hills, differing by a single nucleotide. The most common genotype of B. frigida there matched specimens from Mawson Station, showing low genetic diversity across this large Antarctic region.[25]

In astrobiology research

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Buellia frigida is one of the few lichens to have been on board the International Space Station.

Buellia frigida serves as a key model organism in astrobiology, offering insight into life's adaptability beyond Earth and the potential for survival in space. Astrobiologists use this extremotolerant species to study its endurance under harsh conditions akin to those in space and Mars. Studies show B. frigida's resistance to non-terrestrial abiotic factors, including space exposure, hypervelocity impacts, and Mars-simulated conditions, making it ideal for understanding the biological responses to extreme environments.[7]

Investigations subject B. frigida to stressors like vacuum, UV radiation, and desiccation to assess its viability and photosynthetic activity. The results consistently show that B. frigida maintains high post-exposure viability and sustains minimal damage to its photosynthetic capacity when exposed to these space-related conditions.[26] Studies highlight the lichen's protective mechanisms, including morphological traits, secondary compounds, and anhydrobiosis during desiccation. These mechanisms collectively contribute to the resilience of B. frigida and other extremotolerant lichens.[27]

Buellia frigida has undergone space experiments on the International Space Station (ISS) and in simulated Mars conditions to assess its survival and resistance.[28] One study showed that exposure to low Earth orbit conditions resulted in reduced viability of its fungal and algal components, but the fungal partner was less affected than the algal partner. Despite this, the lichen maintained its structural integrity, demonstrating a degree of resilience to an extraterrestrial environment. The finding suggested some adaptability of this terrestrial organism to space conditions.[28]

Contrasting results emerged from the European Space Agency's Biology and Mars Experiment (BIOMEX) project, also conducted on the ISS. These experiments showed high mortality rates for both algal and fungal symbionts of B. frigida under similar low Earth orbit conditions, indicating a lower survival potential in extreme extraterrestrial environments, casting doubt on the feasibility of Mars as a habitable environment for this lichen.[29] Further, in the same BIOMEX project, researchers studied the DNA integrity of B. frigida over 1.5 years. They used the Randomly Amplified Polymorphic DNA technique and observed significant DNA alterations in space-exposed lichen compared to Earth-based controls, reinforcing the notion of limited resistance of Buellia frigida to the conditions of space and Mars-like environments.[30]

See also

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Notes

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  1. ^ Passage translated by GPT-4.

References

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  1. ^ a b "Homotypic Synonyms". Index Fungorum. Archived from the original on 28 January 2021. Retrieved 23 September 2023.
  2. ^ a b c d MacKenzie Lamb, I. (1968). Antarctic Lichens. II. The Genera Buellia and Rinodina (PDF) (Report). British Antarctic Survey Scientific Reports. British Antarctic Survey. Archived (PDF) from the original on 13 November 2023. Retrieved 13 November 2023.
  3. ^ Darbishire, Otto Vernon (1910). "Lichenes". National Antarctic Expedition. 1901–1904, Natural History. 5: 1–11.
  4. ^ a b c d e f g h i Dodge, Carroll W. (1973). Lichen Flora of the Antarctic Continent and Adjacent Islands. Canaan, New Hampshire: Phoenix Publishing. pp. xviii, 366. ISBN 978-0914016014.
  5. ^ "Record Details: Beltraminia Trevis., Revta Period. Lav. Regia Accad. Sci., Padova 5: 66 (1857)". Index Fungorum. Archived from the original on 1 October 2023. Retrieved 23 September 2023.
  6. ^ Prieto, Maria; Wedin, Mats (2017). "Phylogeny, taxonomy and diversification events in the Caliciaceae". Fungal Diversity. 82 (1): 221–238. doi:10.1007/s13225-016-0372-y.
  7. ^ a b c d e f g h Meeßen, J.; Sánchez, F. J.; Brandt, A.; Balzer, E.-M.; de la Torre, R.; Sancho, L. G.; de Vera, J.-P.; Ott, S. (2013). "Extremotolerance and resistance of lichens: comparative studies on five species used in astrobiological research I. Morphological and anatomical characteristics". Origins of Life and Evolution of Biospheres. 43 (3): 283–303. Bibcode:2013OLEB...43..283M. doi:10.1007/s11084-013-9337-2. PMID 23868319.
  8. ^ a b c d e f Øvstedal, D.O.; Lewis Smith, R.I. (2001). Lichens of Antarctica and South Georgia. A Guide to Their Identification and Ecology. Cambridge, UK: Cambridge University Press. p. 119. ISBN 978-0-521-66241-3.
  9. ^ Inoue, Masakane (1993). "Buellia subfrigida sp. nov. (lichens, Buelliaceae) from Liitzow-Holm Bay area and Prince Olav Coast, East Antarctica―the asexual sorediate species forming a species pair with B. frigida Darb". Nankyoku Shiryô (Antarctic Record). 37 (1): 19–23. doi:10.15094/00008798.
  10. ^ Lewis Smith, R.I. (1988). "Classification and ordination of cryptogamic communities in Wilkes Land, Continental Antarctica". Vegetatio. 76 (3): 155–166. doi:10.1007/BF00045476.
  11. ^ Lewis Smith, Ronald I. (1990). "Plant community dynamics in Wilkes Land. Antarctica". Proceedings of the NIPR Symposium on Polar Biology. 3: 229–244.
  12. ^ Longton 1988, pp. 78–79.
  13. ^ Singh, Shiv Mohan; Nayaka, Sanjeeva; Upreti, D.K. (2007). "Lichen communities in Larsemann Hills, East Antarctica". Current Science. 93 (12): 1670–1672.
  14. ^ Longton 1988, p. 70.
  15. ^ a b Lewis-Smith, Ronald I. (2007). "Lichens". In Riffenburgh, Beau (ed.). Encyclopedia of the Antarctic. New York: Taylor & Francis. pp. 593–594. ISBN 978-0-415-97024-2.
  16. ^ Longton 1988, p. 146.
  17. ^ Schroeter, B.; Green, T.G.A.; Seppelt, R.D.; Kappen, L. (1992). "Monitoring photosynthetic activity of crustose lichens using a PAM-2000 fluorescence system". Oecologia. 92 (4): 457–462. Bibcode:1992Oecol..92..457S. doi:10.1007/bf00317836. PMID 28313215.
  18. ^ Sadowsky, Andres; Ott, Sieglinde (2012). "Photosynthetic symbionts in Antarctic terrestrial ecosystems: the physiological response of lichen photobionts to drought and cold". Symbiosis. 58 (1–3): 81–90. doi:10.1007/s13199-012-0198-7.
  19. ^ Kappen, L.; Schroeter, B.; Green, T.G.A.; Seppelt, R.D. (1998). "Microclimatic conditions, meltwater moistening, and the distributional pattern of Buellia frigida on rock in a southern continental Antarctic habitat". Polar Biology. 19 (2): 101–106. doi:10.1007/s003000050220.
  20. ^ Kanda, Hiroshi; Inoue, Masakane (1994). "Ecological monitoring of moss and lichen vegetation in the Syowa station area, Antarctica". Proceedings of the NIPR Symposium on Polar Biology. 7: 221–231.
  21. ^ Allan Green, T.G.; Brabyn, Lars; Beard, Catherine; Sancho, Leopoldo G. (2011). "Extremely low lichen growth rates in Taylor Valley, Dry Valleys, continental Antarctica". Polar Biology. 35 (4): 535–541. doi:10.1007/s00300-011-1098-7.
  22. ^ Brabyn, Lars; Green, Allan; Beard, Catherine; Seppelt, Rod (2005). "GIS goes nano: Vegetation studies in Victoria Land, Antarctica". New Zealand Geographer. 61 (2): 139–147. doi:10.1111/J.1745-7939.2005.00027.X.
  23. ^ Sancho, Leopoldo G.; Allan Green, T.G.; Pintado, Ana (2007). "Slowest to fastest: Extreme range in lichen growth rates supports their use as an indicator of climate change in Antarctica". Flora – Morphology, Distribution, Functional Ecology of Plants. 202 (8): 667–673. doi:10.1016/j.flora.2007.05.005.
  24. ^ Jones, T.C.; Hogg, I.D.; Wilkins, R.J.; Green, T.G.A. (2015). "Microsatellite analyses of the Antarctic endemic lichen Buellia frigida Darb. (Physciaceae) suggest limited dispersal and the presence of glacial refugia in the Ross Sea region". Polar Biology. 38 (7): 941–949. doi:10.1007/s00300-015-1652-9.
  25. ^ Dyer, P.S.; Murtagh, G.J. (2001). "Variation in the ribosomal ITS-sequence of the lichens Buellia frigida and Xanthoria elegans from the Vestfold Hills, Eastern Antarctica". The Lichenologist. 33 (2): 151–159. doi:10.1006/lich.2000.0306.
  26. ^ Meeßen, J.; Backhaus, T.; Sadowsky, A.; Mrkalj, M.; Sánchez, F.J.; de la Torre, R.; Ott, S. (2014). "Effects of UVC254 nm on the photosynthetic activity of photobionts from the astrobiologically relevant lichens Buellia frigida and Circinaria gyrosa". International Journal of Astrobiology. 13 (4): 340–352. Bibcode:2014IJAsB..13..340M. doi:10.1017/s1473550414000275.
  27. ^ Backhaus, T.; de la Torre, R.; Lyhme, K.; de Vera, J.-P.; Meeßen, J. (2014). "Desiccation and low temperature attenuate the effect of UVC254 nm in the photobiont of the astrobiologically relevant lichens Circinaria gyrosa and Buellia frigida". International Journal of Astrobiology. 14 (3): 479–488. doi:10.1017/s1473550414000470.
  28. ^ a b Meeßen, J.; Wuthenow, P.; Schille, P.; Rabbow, E.; de Vera, J.-P.P.; Ott, S. (2015). "Resistance of the lichen Buellia frigida to simulated space conditions during the preflight tests for BIOMEX—viability assay and morphological stability". Astrobiology. 15 (8): 601–615. Bibcode:2015AsBio..15..601M. doi:10.1089/ast.2015.1281. PMC 4554929. PMID 26218403.
  29. ^ Backhaus, Theresa; Meeßen, Joachim; Demets, René; de Vera, Jean-Pierre; Ott, Sieglinde (2019). "Characterization of viability of the lichen Buellia frigida after 1.5 years in space on the International Space Station". Astrobiology. 19 (2): 233–241. Bibcode:2019AsBio..19..233B. doi:10.1089/ast.2018.1894. PMID 30742495.
  30. ^ Backhaus, Theresa; Meeßen, Joachim; Demets, René; Paul de Vera, Jean-Pierre; Ott, Sieglinde (2019). "DNA damage of the lichen Buellia frigida after 1.5 years in space using Randomly Amplified Polymorphic DNA (RAPD) technique". Planetary and Space Science. 177: 104687. Bibcode:2019P&SS..17704687B. doi:10.1016/j.pss.2019.07.002.

Cited literature

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  • Longton, R.E. (1988). Biology of Polar Bryophytes and Lichens. Cambridge, UK: Cambridge University Press. ISBN 978-0-521-09338-5.
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