Article

Lichens and weathering: importance for soil formation, nutrient cycling and adaptation to environmental change

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Abstract

Lichens comprise ca. 6% of the Earth's terrestrial vegetation, and are dominant in certain polar ecosystems, being primary colonists of rocks where they play a major role in the biogeochemical cycling of elements and contribute to soil formation. We present an historical overview of studies in the Antarctic, leading to recent collection opportunities on Signy Island providing new material to investigate how biodiversity has responded to regional and rapid environmental change. Mountainous, with an ice cap, glaciers, rugged topography, and a complex geology and pedology, Signy Island includes a wide range of terrestrial habitats. A small, inconspicuous lichen, Acarospora cf. badiofusca, was discovered colonizing iron-stained quartz mica schists on the lower slope of Manhaul Rocks, a recently exposed nunatak on the McLeod Glacier, Signy Island, maritime Antarctic. Thallus colour ranged from rust to paler orange and green. Many lichens are colourful, mostly due to the presence of secondary metabolites which are of fungal origin. In some cases colour may reflect chemical coordination reactions involving lichen biomass components and dissolved cations which can lead to metal complex and mineral formation. By far the greatest research effort into characterizing elements and minerals associated with lichens concerns those occurring beneath them, research driven partly from a desire to understand weathering processes. This study, for the first time in the maritime Antarctic, addressed the hypothesis that colour reflects element localization, and examined substance localization within lichen tissues and considered responses to stress. Methods utilised include macrophotography, X-Ray Diffraction with a position sensitive detector (PSD), Scanning Electron Microscopy in back-scattered and ED modes and electron probe microanalysis for the elements Fe, C and Si and by using a third generation variable pressure secondary detector employed as a panchromatic cathodoluminescence detector, SmartStitch image acquisition and montage creation software. The lichen's occurrence in this extreme habitat suggests the use of a complex combination of mechanisms to avoid or mitigate environmental stress. Future study of such species even has the potential to shed new evidence in investigation of the existence of life on other planets, for instance through evidence provided by 'biosignatures'. As a consequence of recent rapid warming and glacial retreat, new areas of rock and ground are being exposed, providing opportunities for lichen colonization and innovative multi-disciplinary, collaborative research. PURVIS, O. W., CONVEY, P., FLOWERDEW, M. J., PEAT, H. J., NAJORKA, J. & KEARSLEY, A. Iron localization in Acarospora colonizing schist following glacial retreat on Signy Island. Antarctic Science [in review].

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... Many lichens are colorful, mostly due to the presence of secondary metabolites which are of fungal origin. In some cases, color may reflect chemical coordination reactions involving lichen biomass components and dissolved cations which would lead to metal complex and mineral formation [3]. Among the fungal species 20% represents lichenized fungi [4], 85% of lichenized fungi comprised withgreen micro-algae, 10%with cyanobacteria and 4% with both cyanobacteria and green algae [1]. ...
... Nitrogen fixation mechanism mainly takes place in heterocyst of cyanobacterial member of lichen. Nitrogen fixation utilizes 8 electrons and 16 Mg ATPs to convert one N 2 to two NH 3 Mediated Hydrogenase/Bi directional/Reversible Hydrogenase encoded by hox gene, and are changed into molecules of Hydrogen (g) (H 2 ). However, 40% of gaseous Hydrogen gas will be recycled through Plastoquinone and Plastocyanin, by uptake Hydrogenase enzyme encoded by hup (hydrogen uptake) gene [17]. ...
Article
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Lichens are symbiotically associated of algae and fungi, actively involved in conversion of atmospheric nitrogen into organic form. Lichens are also involved in phosphate solubilization and biological nitrogen fixation. Lichens possess cyanobacteria as its primary phycobiont commonly referred as cyanolichens, but in some lichens cyanobacteria are located in special structure called cephalodia. The heterocyst of cyanobacteria convert nitrogen to amonia form in an anaerobic environment and translocate to the mycobiont. Nitrogen fixation has been estimated in lichen samples by 15N2 method or acetylene reduction assay. Acetylene reduction or Nitrogen fixation have been directly affected by environmental factors like desiccation, light, temperature, carbon fixation rate and photosynthesis.
... Thallus colours ranged from rust-coloured in exposed situations to grey-brown (green when moist) in shaded crevices ( Fig. 2) (Purvis et al. 2012(Purvis et al. , 2013Purvis 2014). Following the treatment by Øvstedal & Lewis Smith (2001), it was provisionally named 'Acarospora cf. ...
... Th. Fr.' (Purvis et al. 2012(Purvis et al. , 2013Purvis 2014) Smith indicated that Antarctic specimens named as A. badiofusca differed in apothecial anatomy compared with northern European specimens. Lichen pigmentation is often considered an adaptation for coping with high illumination (Gauslaa & McEvoy 2005;Elix & Stocker-Wörgötter 2008). ...
Article
Myriospora signyensis Purvis, Fdez-Brime, M. Westb. & Wedin is described from Signy Island, South Orkney Islands, Antarctica, where it occurs predominantly on quartz mica schist. This represents the first record of the genus for Antarctica. The distinctive interrupted photobiont arrangement places it within the genus Myriospora (formerly known as the ‘ Acarospora ’ smaragdula group, or Silobia ). The new species is characterized by having large, distinctly elevated, sessile apothecia with a prominent margin and a thallus that is usually lobed at the margins and variously orange-red, rust-coloured or brown-pigmented. Molecular phylogenetic analyses inferred with strong support that M. signyensis is closely related to M. scabrida which is similar in having a lobed, imbricate thallus with large and frequently somewhat raised apothecia, but which differs in never being rusty red, by frequently having a larger number of apothecia per areole/squamule and by having a thick and distinctive thalline epinecral layer. Myriospora signyensis is otherwise most similar to M. dilatata but the thallus of M. dilatata is never imbricate-lobate and the ascomata of M. signyensis have larger and more distinctly raised and sessile apothecia. A worldwide key to the 10 species currently recognized in the genus is presented.
... Thallus colours ranged from rust-coloured in exposed situations to grey-brown (green when moist) in shaded crevices ( Fig. 2) (Purvis et al. 2012(Purvis et al. , 2013Purvis 2014). Following the treatment by Øvstedal & Lewis Smith (2001), it was provisionally named 'Acarospora cf. ...
... Th. Fr.' (Purvis et al. 2012(Purvis et al. , 2013Purvis 2014) Smith indicated that Antarctic specimens named as A. badiofusca differed in apothecial anatomy compared with northern European specimens. Lichen pigmentation is often considered an adaptation for coping with high illumination (Gauslaa & McEvoy 2005;Elix & Stocker-Wörgötter 2008). ...
Article
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As an essential nutrient and energy source for the growth of microbial organisms, iron is metabolically cycled between reduced and oxidized chemical forms. The resulting flow of electrons is invariably tied to reactions with other redox-sensitive elements, including oxygen, carbon, nitrogen, and sulfur. Therefore, iron is intimately involved in the geochemistry, mineralogy, and petrology of modern aquatic systems and their associated sediments, particulates, and porewaters. In the geological past, iron played an even greater role in marine geochemistry, as evidenced by the vast deposits of Precambrian iron-rich sediments, the "banded iron formations." These deposits are now being used as proxies for understanding the chemical composition of the ancient oceans and atmosphere.
Article
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Five of six Rb-Sr muscovite mineral isochron ages from the Scotia Metamorphic Complex of the South Orkney Islands, West Antarctica, average 190 ± 4 Ma. The muscovite ages are interpreted to date foliation-formation and thus also accretion and subduction at the Gondwana margin. Coincident picrite and ferropicrite magmatism, indicative of melts from deep-seated depleted mantle, permits a causative link between accretion and the arrival of the Karoo – Ferrar – Chon Aike mantle plume in the Early Jurassic. Three biotite Rb-Sr mineral isochron ages are consistently younger and average 176 ± 5 Ma. The biotite ages may record post-metamorphic cooling or more likely retrogressive metamorphic effects during uplift.
Book
Fungi in Biogeochemical Cycles Fungi have important roles in the cycling of elements in the biosphere but are frequently neglected within microbiological and geochemical research spheres. Symbiotic mycorrhizal fungi are responsible for major transformations and redistribution of inorganic nutrients, while free-living fungi have major roles in the decomposition of organic materials, including xenobiotics. Fungi are also major biodeterioration agents of stone, wood, plaster, cement and other building materials, and are important components of rock-inhabiting microbial communities. The aim of this book is to promote further understanding of the key roles that free-living and symbiotic fungi (in mycorrhizas and lichens) play in the biogeochemical cycling of elements, the chemical and biological mechanisms that are involved, and their environmental and biotechnological significance. Where appropriate, relationships with bacteria are also discussed to highlight the dynamic interactions that can exist between these major microbial groups and their integrated function in several kinds of habitat.
Chapter
This chapter discusses pedogenetic significance of lichens, their significance in biophysical and biochemical weathering, and role in plant succession and soil development. The physical weathering of the substratum on which saxicolous lichens grow is described in terms of rhizine penetration and thallus expansion and contraction. Rhizines, originating from the medulla, penetrated the cleavage planes in calcitic fossil debris in limestone and caused mechanical disintegration of glass surfaces. Rhizines are abundant, but not universal in foliose species and are either scattered or confined to special areas of the lower thallus surface. The extent of biogeophysical weathering below lichen thalli appears to be influenced strongly by the nature of the thallus and by the chemical and physical composition of the rock substratum. The low solubility and weak acidity of lichen compounds largely preclude their effectiveness as biogeochemical weathering agents if these compounds were to function solely as acids. Lichens accumulate several elements, such as nitrogen, phosphorus, and sulfur, and are stored in an available or potentially available form, and can be used by mosses and higher plants that may replace lichens during soil development.
Article
Introduction Fungi are chemoheterotrophic organisms, ubiquitous in subaerial and subsoil environments, and important as decomposers, animal and plant symbionts and pathogens, and spoilage organisms of natural and man-made materials (Gadd, 1993, 1999; Burford et al., 2003a). A fungal role in biogeochemical cycling of the elements (e.g. C, N, P, S, metals) is obvious and interlinked with the ability to adopt a variety of growth, metabolic and morphological strategies, their adaptive capabilities to environmental extremes and their symbiotic associations with animals, plants, algae and cyanobacteria (Burford et al., 2003a; Braissant et al., 2004; Gadd, 2004). Fungal polymorphism and reproduction by spores underpin successful colonization of different environments. Most fungi exhibit a filamentous growth habit, which provides an ability for adoption of either explorative or exploitative growth strategies, and the formation of linear organs of aggregated hyphae for protected fungal translocation (see Fomina et al., 2005b). Some fungi are polymorphic, occurring as both filamentous mycelium and unicellular yeasts or yeast-like cells, e.g. black meristematic or microcolonial fungi colonizing rocks (Sterflinger, 2000; Gorbushina et al., 2002, 2003). Fungi can also grow inside their own parental hyphae utilizing dead parts of the colony under the protection of parental cell walls (Gorbushina et al., 2003). The ability of fungi to translocate nutrients through the mycelial network is another important feature for exploring heterogeneous environments (Jacobs et al., 2002, 2004; Lindahl&Olsson, 2004). The earliest fossil record of fungi in terrestrial ecosystems occurred during the Ordovician period (480 to 460 MYBP) (Heckman et al., 2001).
Chapter
The upper cortex and extracellular hyphal wall matrix are min-eralized in both rust-coloured Acarospora sinopica and the paler A. smaragdula 'f. subochracea' in the form of microgranular or mi-crobotryoidal phases. Analysis confirmed the distinctive colours are not simply due to hydrated iron oxides, as previously believed, and suggests mixed sulphide and oxide phases with little crystallinity, as well as other elements arising from clay minerals are present. These aspects highlight the need for a more detailed study employing a range of micro-analytical techniques, including analytical TEM, which will allow mineral characterisation and localisation down to the nanometre scale.
Article
Cryptoendolithic (hidden in rock) lichen-dominated microbial communities from the Ross Desert of Antarctica were shown to produce oxalate (oxalic acid). Oxalate increased mineral dissolution, which provides nutrients, creates characteristic weathering patterns, and may ultimately influence the biological residence time of the community. Oxalate was the only organic acid detectable by HPLC, and its presence was verified by GC/MS. Community photosynthetic metabolism was involved in oxalate production since rates of (14)C-oxalate production from (14)C02 were higher in light than in dark incubations. Flaking of the sandstone at the level of the lichen-dominated zone a few millimeters beneath the rock surface can be explained by dissolution of the sandstone cement, which was enhanced by Si, Fe, and Al oxalate complex formation. Added oxalate was observed to increase the solubility of Si, Fe, Al, P, and K. Oxalate's ability to form soluble trivalent metal-oxalate complexes correlated with the observed order of metal oxide depletion from the lichen-dominated zone (Mn > Fe > Al). Thermodynamic calculations predict that Fe oxalate complex formation mobilizes amorphous Fe oxides (ferrihydrite) in the lichen-dominated zone, and where oxalate is depleted, ferrihydrite should precipitate. Hematite, a more crystalline Fe oxide, should remain solid at in situ oxalate concentrations. Oxalate was not a carbon source for the indigenous heterotrophs, but the microbiota were involved in oxalate mineralization to CO2, since oxalate mineralization was reduced in poisoned incubations. Photooxidation of oxalate to C02 coupled with photoreduction of Fe(Ill) may be responsible for oxalate removal in situ, since rates of (14)C-oxalate mineralization in dark incubations were at least 50% lower than those in the light. Removal of oxalate from Si, Fe, and Al complexes should allow free dissolved Si, Fe, and Al to precipitate as amorphous silicates and metal oxides. This may explain increased siliceous crust (rock varnish or desert varnish) formation near the surface of colonized rocks were light intensity is greatest.
Article
The nature and composition of the Fe minerals in the rusty ferruginous material frequently located in the zone of contact between the thallus of Stereocaulon vesuvianum and the leucite bearing rock of Mt. Vesuvius have been studied by microscopic and submicroscopic investigations (SEM, TEM with EDXRA) complemented by X-ray diffraction and chemical analysis. Ferrihydrite is likely to be the main component of the short-range order iron oxyhydroxide pool, although the possibility that significant feroxyhite may be present cannot be completely excluded. Hematite and goethite are the crystalline iron oxides. The organic acids produced by lichens play a key role in the enrichment of poorly-ordered phases at the rock-lichen interface. It is suggested that the peculiar morphology of the Stereocaulon vesuvianum thallus and the irregularity of the volcanic rock surface lead to different microsites in the rock-lichen interfaces which have their own conditions of pH, humidity and redox potential, favourable for the neoformation of crystalline phases.
Article
New K/Ar and Rb/Sr data are presented for part of the supposed late Palaeozoic/early Mesozoic metamorphic complex in West Antarctica (here renamed the 'Scotia metamorphic complex'). The results, combined with a review of other evidence, fail to confirm a pre-Mesozoic age for the subduction complex in this region, although rocks of the albite-epidote-amphibolite facies could be as old as Permian. The remaining metamorphic rocks (blueschists and greenschists from the South Shetland Islands) appear to be significantly younger (70-100 m.y.) and were probably formed, in part at least, during Cretaceous subduction. -R.A.H.
Article
The cold, dry ecosystems of Antarctica have been shown to harbor traces left behind by microbial activity within certain types of rocks, but only two indirect biomarkers of cryptoendolithic activity in the Antarctic cold desert zone have been described to date. These are the geophysical and geochemical bioweathering patterns macroscopically observed in sandstone rock. Here we show that in this extreme environment, minerals are biologically transformed, and as a result, Fe-rich diagenetic minerals in the form of iron hydroxide nanocrystals and biogenic clays are deposited around chasmoendolithic hyphae and bacterial cells. Thus, when microbial life decays, these characteristic neocrystalized minerals act as distinct biomarkers of previous endolithic activity. The ability to recognize these traces may have potential astrobiological implications because the Antarctic Ross Desert is considered a terrestrial analogue of a possible ecosystem on early Mars.
Article
Abstract Whole-rock and mineral analyses of polydeformed mica-schist, quartzite, marble and amphibolite are presented from Signy Island, South Orkney Islands, part of the Scotia metamorphic complex. Whole-rock chemistry suggests that the amphibolites are the metamorphosed equivalent of enriched tholeiitic and alkali basalts of an oceanic intraplate basalt series. These, together with limestones and Mn-rich cherts of an oceanic island assemblage were tectonically mixed with trench or trench inner slope basin sediments in a subduction zone environment. Variation in mineral chemistry indicates an increase in temperature and decrease in pressure during metamorphism; pressures of 8 kbar and temperatures of approximately 545°C were reached during amphibolite facies metamorphism in the latter stages of deformation. These new data provide good evidence to support the previous interpretation of the Scotia metamorphic complex as a subduction complex.
Article
The application of element mapping in the scanning electron microscope with electron probe microanalysis across the lichen–rock interface is described with reference to Trapelia involuta growing on a granite substratum. The preparation of samples containing both organic and mineral components required the development of specialized techniques to maintain both chemical and structural integrity at the 2 μm resolution of the X-ray element maps. X-ray element maps show the distribution of entrained rock particles at the lichen–rock interface and chemical localization which is strongly related to anatomical structure for the essential elements S, Fe, Ca, Na, K and P. The ability to map element distribution across the lichen–rock interface has wide-ranging potential applications in studies such as the biodeterioration of buildings and monuments and the mobilization and uptake of toxic elements from contaminated substrata.
Article
Using the scanning electron microscope with microprobe analysis, observations have been made on the weathering of rock-forming minerals—feldspars, ferromagnesian minerals, quartz and serpentine—principally by crustose lichens. A variety of phenomena can be recognized, namely, etching patterns, decomposition features and secondary products which can be related to differences in mineral structure and composition. Such weathering has been proved to involve the chelating effects of oxalic acid in certain lichens, although lichen acids could also be implicated.
Article
Biophysical and biogeochemical weathering of amphibole syenite associated with the Stettin complex near Wausau, Wisconsin, has been examined by HRTEM, WDS, LM, and XRD. The rock consists of microperthitic feldspar, ferriannite, quartz, and ferrohastingsite. Crustose saxicolous lichens, Rhizocarpon grande and Porpidea albocaerulescens, penetrate the rock surface to a depth of 10 mm. Within the intact rock, amphibole surfaces along hyphae-filled cracks are highly corroded. Fungal hyphae exploit grain boundaries, cleavages, and cracks to gain access to mineral surfaces, resulting in accumulations of cleavage-bound mineral fragments as small as 5 μm within the lower thallus. Bacterial microcolonies are common and all mineral surfaces are completely coated in extracellular acidic mucopolysaccharides from fungal and bacterial sources. In the cases of amphibole, quartz, and feldspar, dissolution does not appear to involve pervasive leaching, for even the smallest mineral fragments retain their chemical and structural identity. Biotite directly in contact with the lichen thallus is intimately interpenetrated by fungal hyphae growing along (001) cleavages and is partially converted to vermiculite. No siliceous relics have been identified. Biologically mediated weathering involves a complex dissolution/ selective transport/recrystallization mechanism occurring within the acidic extracellular gels coating all mineral surfaces. A specialized weathering microenvironment around each mineral grain initially produces minute phyllosilicate crystallites. A rind of clay minerals forms around the dissolving parent phase, eventually culminating in abundant 5–10 μm diameter polymer-bound aggregates of face-to-face oriented clay minerals of homogeneous composition.Physiochemical weathering of ferrohastingsite produces topotactically oriented smectite and goethite. The cleavage-controlled reaction is neither isochemical nor isovolumetric.
Article
The orange coloured cortical anthraquinone compound parietin synthesised by the mycobiont protects the lichen photobiont against excessive solar radiation. This study aims at searching for seasonal acclimation of the sun-screening parietin in a natural lichen population. The widespread Xanthoria parietina, sampled at an open seashore rock at 58°N, shows a distinct seasonal variation with low parietin contents at winter solstice increasing to twice as high levels at summer solstice. The variation is large enough to be observed by the human eye. The annual cycle is consistent with a solar radiation protective function of parietin operating also on a temporal scale. The vernal rise in parietin at increasing solar power is faster than the autumnal decline, suggesting that acclimation to increased light stress in spring is faster than the autumnal acclimation to gradually lowered irradiances.ZusammenfassungDer orangefarbene, anthraquinone Rindenbestandteil Parietin, der von den Mycobionten synthetisiert wird, schützt den Photobionten der Flechte gegen intensive Sonneneinstrahlung. Diese Untersuchung zielt darauf ab, die saisonalen Anpassungen des vor Sonne schützenden Parientins in einer natürlichen Flechtenpopulation zu finden. Die weitverbreitete Xanthoria parietina, die an offenen Felsküsten auf 58°N gesammelt wurde, zeigt eine deutliche saisonale Variation mit geringen Parietingehalten zur Wintersonnenwende, die zur Sommersonnenwende auf das Doppelte zunehmen. Die Variation ist groß genug, um vom menschlichen Auge wahrgenommen zu werden. Der jährliche Zyklus stimmt mit der Schutzfunktion vor Sonneneinstrahlung überein, die ebenfalls auf einer zeitlichen Skala wirkt. Der Anstieg des Parietins im Frühjahr mit zunehmender Sonnenkraft ist schneller als die Abnahme im Herbst, was vermuten läßt, dass die Anpassung an den zunehmenden Lichtstress im Frühjahr schneller ist als die Anpassung an die graduell verringerte Strahlung im Herbst.
Article
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In the frigid desert of the Antarctic dry valleys there are no visible life forms on the surface of the soil or rocks. Yet in certain rock types a narrow subsurface zone has a favorable microclimate and is colonized by microorganisms. Dominant are lichens of unusual organization. They survive not by physiological adaptation to lower temperatures, but by changing their mode of growth, being able to grow between the crystals of porous rocks. Their activity results in mobilization of iron compounds and in rock weatherning with a characteristic pattern of exfoliation. This simple ecosystem lacks both higher consumers and predators.
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