Buellia frigida

The lichen was formally described as a new species in 1910 by the British botanist Otto Derbishire. The type specimen were collected in 1902 by Reginald Koettlitz from Granite Harbour in McMurdo Sound; they were 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):

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) decolourized; hypothecium darkening to brownish or occasionally decolourized 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.[2] 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.[3] The genus Beltraminia has since been synonymised with Dimelaena.[4] 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.[5]

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 owning to variations in anatomical structure of the lichen, and has "no hesitation in reducing B. quercina to synonymy".[5]

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 characterized by a black hypothallus that extends approximately 5–7.5 millimetres (3⁄16–5⁄16 in) beyond the older central region of thallus;[3] this black area represents the growth zone.[6] In some instances, neighbouring thalli coalesce to form larger aggregations of up to 50 cm (20 in).[7] 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.[3] This layer, mucilaginous in nature, may appear white when it is dry.[6]

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, isodiametric cells. 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.[3] The medulla stabilises the thallus structure and helps regulate water retention and gas exchange in the lichen.[6] 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.[3] Medullary hyphae also help the thallus adhere tightly to the substratum.[6]

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;[3] when mature they are lecideine in form, and up to about 1 mm in diameter.[6] 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, are septate and darken above the asci. 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.[3]

Asexual propagules, such as isidia or soredia, are not made by Buellia frigida.[6] 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.[3]

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.[7] On these exposed surfaces, colonisation is more frequent in cases where is some shelter provided by a crevasse or a drainage channel. In these crevasses, it is common to see chains of thalli that increase in size with increasing closeness to the ground. In its habitat, Buellia frigida is often the only species that can become established on smooth, ice-polished rock. Once its thallus is about 2 cm (1 in) or more in diameter, Pseudephebe minuscula or Usnea sphacelata often start growing near the centre of the thallus. As the secondary lichens grow, the underlying crustose B. frigida degrades, leaving outer rings of healthy crustose lichen.[8] The umbilicate lichen Umbilicaria decussata is another species that has been recorded growing on Buellia frigida.[9] 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 bird colonies. Conversely, the 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.[10] Phaeosporobolus usneae is a lichenicolous (lichen-dwelling) fungus that has been recorded from the thalli of B. frigida in Bunger Hills (Wilkes Land).[7]

Buellia frigida can be found throughout Antarctica, spanning from the Antarctic Peninsula to rocky coastal areas and exposed rock formations in the continent's interior.[7] It is the most widespread lichen in east Antarctica, including the Larsemann Hills,[11] 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.[3] Buellia frigida is most abundant in the dry valley region and other areas of Victoria Land at higher elevations, above 600 m (2,000 ft), where there is frequent cloud cover and summer snow flurries.[12] The lichen has been found at altitudes of up to 2,015 m (6,611 ft).[7] 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.[13] In the Antarctic Peninsula, where the lichen is less prevalent, it has only been found in the western part of the peninsula, south of latitude 67°S. 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.[5]

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.[7] 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. In Buellia frigida, the maximum NAR is observed at a temperature of 10 °C (50 °F), provided the entire thallus is fully hydrated. This metric sheds light on the lichen's photosynthetic efficiency in polar ecosystems.[14] 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.[13] 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.[6] In situ measurements of this lichen's photosynthetic activity were conducted in continental Antarctica, revealing that it thrives in its habitat. Buellia frigida exhibited a high photosynthetic rate, indicating its adaptation to the extreme environmental conditions of Antarctica, such as low temperatures and strong 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.[15] The photobiont partner of Buellia frigida has been shown to have 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.[16]

The availability of moisture plays a vital role in the distribution of Buellia frigida. Observations at Cape Geology in southern Victoria Land showed that the lichen relies on meltwater from snowpack and occasional snowfalls as its primary source of moisture during the early austral summer. Despite the intense irradiance, the lichen appears well-adapted to the combination of hydration, low temperatures, and strong light. The distribution of lichen thalli on rock surfaces is influenced by the frequency and duration of meltwater moistening, highlighting its dependence on moisture availability.[17]

Research conducted in continental Antarctica has revealed that Buellia frigida has extremely slow radial growth rates. 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.[18] 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.[19] 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.[20] Geographic information system technology has been successfully used to detect small changes in the growth of Buellia frigida, by computing the changes in vegetation occurring over a 42-year period.[21]

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. This limited dispersal, despite the potential for wind-dispersed spores, further underscores the lichen's specialization in colonising specific areas with suitable conditions, including moisture availability during the short Antarctic summer.[22]

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

Buellia frigida has proven to be a useful model organism for advancing astrobiology research, shedding light on the adaptability of life beyond Earth and offering critical insights into the challenges and potential for survival in space and on other celestial bodies. Astrobiologists have utilized this extremotolerant species to explore its ability to endure extreme environmental conditions, mirroring those found in space and on celestial bodies like Mars. Multiple studies have demonstrated that B. frigida exhibits remarkable resistance to non-terrestrial abiotic factors, including space exposure, hypervelocity impacts, and Mars-simulated conditions, making it an ideal model organism for understanding the biological responses to extreme environments.[6]

In these investigations, B. frigida has been subjected to a range of stressors, such as vacuum, UV radiation, and extreme desiccation, to evaluate 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.[23] Furthermore, studies have underscored the significance of protective mechanisms within lichens, including morphological and anatomical traits, secondary lichen compounds, and the ability to enter anhydrobiosis when desiccating. These mechanisms collectively contribute to the exceptional resilience of B. frigida and other extremotolerant lichens.[24]

Moreover, B. frigida has been included in space experiments, both on the International Space Station and in simulated Mars conditions, to assess its survival and resistance potential. While exposure to low Earth orbit conditions resulted in some damage to the lichen symbionts, these experiments provide essential insights into the limits and limitations of terrestrial organisms in extraterrestrial environments.[25] The genetic integrity of B. frigida has also been studied, revealing changes in DNA profiles due to space exposure, emphasizing the intricate nature of lichen adaptation to non-terrestrial environments.[26]

Another study examined the impact of space conditions on Buellia frigida by utilizing the Randomly Amplified Polymorphic DNA (RAPD) technique to assess DNA integrity and damage. The RAPD profiles of the lichen samples exposed to space conditions displayed noticeable changes when compared to unexposed profiles, signifying alterations in DNA integrity. This study highlights the significance of genetic integrity for cell and organism survival, underlining the importance of understanding DNA damage in the context of space and Mars analogue conditions.[27]

• List of Buellia species