Lichen acclimation to changing environments: Photobiont switching vs. climate‐specific uniqueness in Psora decipiens

Unraveling the complex relationship between lichen fungal and algal partners has been crucial in understanding lichen dispersal capacity, evolutionary processes, and responses in the face of environmental change. However, lichen symbiosis remains enigmatic, including the ability of a single fungal partner to associate with various algal partners. Psora decipiens is a characteristic lichen of biological soil crusts (BSCs), across semi‐arid, temperate, and alpine biomes, which are particularly susceptible to habitat loss and climate change. The high levels of morphological variation found across the range of Psora decipiens may contribute to its ability to withstand environmental change. To investigate Psora decipiens acclimation potential, individuals were transplanted between four climatically distinct sites across a European latitudinal gradient for 2 years. The effect of treatment was investigated through a morphological examination using light and SEM microscopy; 26S rDNA and rbcL gene analysis assessed site‐specific relationships and lichen acclimation through photobiont switching. Initial analysis revealed that many samples had lost their algal layers. Although new growth was often determined, the algae were frequently found to have died without evidence of a new photobiont being incorporated into the thallus. Mycobiont analysis investigated diversity and determined that new growth was a part of the transplant, thus, revealing that four distinct fungal clades, closely linked to site, exist. Additionally, P. decipiens was found to associate with the green algal genus Myrmecia, with only two genetically distinct clades between the four sites. Our investigation has suggested that P. decipiens cannot acclimate to the substantial climatic variability across its environmental range. Additionally, the different geographical areas are home to genetically distinct and unique populations. The variation found within the genotypic and morpho‐physiological traits of P. decipiens appears to have a climatic determinant, but this is not always reflected by the algal partner. Although photobiont switching occurs on an evolutionary scale, there is little evidence to suggest an active environmentally induced response. These results suggest that this species, and therefore, other lichen species, and BSC ecosystems themselves may be significantly vulnerable to climate change and habitat loss.     

Fungal farmers or algal escorts: lichen adaptation from the algal perspective

Domestication of algae by lichen‐forming fungi describes the symbiotic relationship between the photosynthetic (green alga or cyanobacterium; photobiont) and fungal (mycobiont) partnership in lichen associations ( Goward 1992 ). The algal domestication implies that the mycobiont cultivates the alga as a monoculture within its thallus, analogous to a farmer cultivating a food crop. However, the initial photobiont ‘selection’ by the mycobiont may be predetermined by the habitat rather than by the farmer. When the mycobiont selects a photobiont from the available photobionts within a habitat, the mycobiont may influence photobiont growth and reproduction ( Ahmadjian & Jacobs 1981 ) only after the interaction has been initiated. The theory of ecological guilds ( Rikkinen et al. 2002 ) proposes that habitat limits the variety of photobionts available to the fungal partner. While some studies provide evidence to support the theory of ecological guilds in cyanobacterial lichens ( Rikkinen et al. 2002 ), other studies propose models to explain variation in symbiont combinations in green algal lichens ( Ohmura et al. 2006 ; Piercey‐Normore 2006 ; Yahr et al. 2006 ) hypothesizing the existence of such guilds. In this issue of Molecular Ecology, Peksa & ?kaloud (2011) test the theory of ecological guilds and suggest a relationship between algal habitat requirements and lichen adaptation in green algal lichens of the genus Lepraria. The environmental parameters examined in this study, exposure to rainfall, altitude and substratum type, are integral to lichen biology. Lichens have a poikilohydric nature, relying on the availability of atmospheric moisture for metabolic processes. Having no known active mechanism to preserve metabolic thallus moisture in times of drought, one would expect a strong influence of the environment on symbiont adaptation to specific habitats. Adaptation to changes in substrata and its properties would be expected with the intimate contact between crustose lichens in the genus Lepraria. Altitude has been suggested to influence species distributions in a wide range of taxonomic groups. This is one of the first studies to illustrate an ecological guild, mainly for exposure to rainfall (ombrophiles and ombrophobes), with green algal lichens.     

Morphological and phylogenetic study of algal partners associated with the lichen-forming fungus <Emphasis Type="Italic">Tephromela atra</Emphasis> from the Mediterranean region

Recent DNA sequence analyses have revealed the diversity of algal partners in lichen symbioses. Although morphologically similar, different genetic lineages of photobionts are detected in wide geographic ranges of the same lichen fungal species. We studied the photobiont of the genus Trebouxia, which are known as partners of diverse lichen-forming fungal species in the Mediterranean region. We studied the phylogeny of these algae with a multilocus dataset including three loci: ITS, rbcL, and actin type I gene. The two lineages found, informally named Trebouxia sp. 1 and Trebouxia sp. 2, are related to Trebouxia arboricola/decolorans. The cultivation under axenic conditions succeeded only for one of them so far. We used light microscopy, confocal laser scanning microscopy and transmission electron microscopy for phenotypic characterisation. The ultrastructural characters currently used to describe species in the genus do not support the segregation of Trebouxia sp.1 from Trebouxia arboricola. The preferential presence in Mediterranean climates of these strains suggests eco-physiological adaptation. Despite their asexuality in long living lichen symbioses, coccoid algal lichen partners have apparently diversified genetically and physiologically.     

The complexity of symbiotic interactions influences the ecological amplitude of the host: A case study in Stereocaulon (lichenized Ascomycota)

Symbiosis plays a fundamental role in nature. Lichens are among the best known, globally distributed symbiotic systems whose ecology is shaped by the requirements of all symbionts forming the holobiont. The widespread lichen‐forming fungal genus Stereocaulon provides a suitable model to study the ecology of microscopic green algal symbionts (i.e., phycobionts) within the lichen symbiosis. We analysed 282 Stereocaulon specimens, collected in diverse habitats worldwide, using the algal ITS rDNA and actin gene sequences and fungal ITS rDNA sequences. Phylogenetic analyses revealed a great diversity among the predominant phycobionts. The algal genus Asterochloris (Trebouxiophyceae) was recovered in most sampled thalli, but two additional genera, Vulcanochloris and Chloroidium, were also found. We used variation‐partitioning analyses to investigate the effects of climatic conditions, substrate/habitat characteristic, spatial distribution and mycobionts on phycobiont distribution. Based on an analogy, we examined the effects of climate, substrate/habitat, spatial distribution and phycobionts on mycobiont distribution. According to our analyses, the distribution of phycobionts is primarily driven by mycobionts and vice versa. Specificity and selectivity of both partners, as well as their ecological requirements and the width of their niches, vary significantly among the species‐level lineages. We demonstrated that species‐level lineages, which accept more symbiotic partners, have wider climatic niches, overlapping with the niches of their partners. Furthermore, the survival of lichens on substrates with high concentrations of heavy metals appears to be supported by their association with toxicity‐tolerant phycobionts. In general, low specificity towards phycobionts allows the host to associate with ecologically diversified algae, thereby broadening its ecological amplitude.     

Joint Dispersal Does Not Imply Maintenance of Partnerships in Lichen Symbioses

Dispersal of symbiotic partners by joint propagules is considered as an efficient strategy to maintain successful associations and to circumvent low symbiont availability. Joint dispersal is widespread in diverse symbioses and a particularly common reproductive mode in lichens. We were interested in the implications of joint symbiont dispersal on population genetic structure and investigated patterns of symbiont association in populations of two closely related lichen species in the genus Physconia, with similar range of compatible algal partners. One of the lichen species is characterized by joint dispersal of both symbionts, whereas the other species propagates by meiotic fungal spores alone. The latter species must re-establish the symbiotic stage with appropriate algae sampled from the environment. Both fungal species have specialized on photobionts representing a monophyletic lineage of the algal genus Trebouxia. The results indicate no correlated association of symbiont genotypes in the species with joint symbiont dispersal. We rather show that algal gene diversity in populations of lichenized fungi with different propagation strategies is not necessarily different. The association with algae that differ from the co-dispersed genotypes during the vegetative development of the thalli is the most likely explanation for the observed pattern. Maintenance of symbiotic associations is an option but not a strict consequence of joint symbiont dispersal in lichens.     

Lichens of St Helena and Ascension Island

Lichens are the dominant organisms on most of the South Atlantic island of St Helena. In total, 220 different species were found during a recent survey, most of which have never been reported from the island. Previously, less than 50 lichen species were reported from the island, one half of which are most probably incorrect records. The total number of lichens known from the island now stands at 225. Most species could be identified, but the following, most probably endemic, species are described as new to science: Dolichocarpus seawardii , which is only the second species in this genus, the type being from Chile; Dermatiscum pusillum , which is only the third species in this African genus; Dimelaena triseptata ; Xanthoparmelia beccae ; and four Ramalina species, Ramalina geniculatella , R. ketner‐oostrae , R. rigidella , and R. sanctae‐helenae . The lichen flora has many species in common with that of the geologically much younger Ascension Island, where just under 100 species were recently found by the author, most of which are equally new to that island. Lecanora sanctae‐helenae, previously known as the only endemic lichen of St Helena, was also found to be abundant on Ascension Island. © 2008 The Linnean Society of London, Botanical Journal of the Linnean Society, 2008, 158 , 147–171.     

中国石蕊科地衣研究之五中国石蕊属地衣一新种

本文报道了产于中国西南地区的石蕊属地衣一新种:亚厚叶石蕊(Cladoniasubincrassata S.Y.Guo),其主要的次生代谢产物为松萝酸和泽屋菇.文中还从形态、化学和地理分布方面将新种和邻近种厚叶石蕊(Cladonia incrassata)进行了比较.     

中国石蕊科地衣研究之三 中国新记录属:扇盘衣属

本文报道了主要分布于澳洲的扇盘衣属地衣,缝裂扇盘衣在中国的首次发现,从而为中国地衣区系增加了一个新记录属。文中报道的该属的地衣不仅在中国,即使在世界范围也十分珍异。因而,对于该属及种的特征从形态学、解剖学与化学方面给以简要描述。     

THE EVOLUTION OF PARASITES FROM THEIR HOSTS: A CASE STUDY IN THE PARASITIC RED ALGAE

Morphological similarities of many parasites and their hosts have led to speculation that some groups of plant, animal, fungal, and algal parasites may have evolved directly from their hosts. These parasites, which have been termed adelphoparasites in the botanical literature, and more recently, agastoparasites in the insect literature, may evolve monophyletically from one host and radiate secondarily to other hosts or, these parasites may arise polyphyletically, each arising from its own host. In this study we compare the internal transcribed spacer regions of the nuclear ribosomal repeats of species and formae specialis (host races) included in the red algal parasite genus Asterocolax with its hosts, which all belong to the Phycodrys group of the Delesseriaceae and with closely related nonhost taxa of the Delesseriaceae. These analyses reveal that species of Asterocolax have evolved polyphyletically. Asterocolax erythroglossi from the North Atlantic host Erythroglossum laciniatum appears to have evolved from its host, whereas taxa included in the north Pacific species Asterocolax gardneri have had two independent origins. Asterocolax gardneri from the host Polyneura latissima probably arose directly from this host. In contrast, all other A. gardneri formae specialis appear to have originated from either Phycodrys setchellii or P. isabelliae and radiated secondarily onto other closely related taxa of the Phycodrys group, including Nienburgia andersoniana and Anisocladella pacifica. Gamete crossing experiments confirm that A. gardneri from each host is genetically isolated from both its host, and from other A. gardneri and their hosts. Cross-infection experiments reveal that A. gardneri develops normally only on its natural host, although some abberrant growth may occur on alternate hosts. The ability of red algal parasites to radiate secondarily to other red algal taxa, where they may become isolated genetically and speciate, suggests that this process of speciation is not a “genetic dead end” but one that may give rise to related clusters of parasite species.     

The lichen-forming ascomycete Evernia mesomorpha associates with multiple genotypes of Trebouxia jamesii

The epiphyte Evernia mesomorpha forms a lichen association with green algae in the genus Trebouxia. Little is known about the population structure of E. mesomorpha. Here, population structure of the algal and fungal symbionts was examined for 290 lichen thalli on 29 jack pine (Pinus banksiana) trees in Manitoba. Through phylogenetic analysis of internal transcribed spacer (ITS) nuclear ribosomal DNA (rDNA) sequences, five algal genotypes were detected that were nested within T. jamesii. Two fungal genotypes were detected that formed a clade with two other Evernia species. The genus Evernia was paraphyletic with E. prunastri, sister to Parmelia saxatilis. Restriction fragment length polymorphism (RFLP) of ITS rDNA showed multiple algal genotypes in 45% of the 290 lichen thalli collected, whereas all thalli only contained one fungal genotype. Low population subdivision of algal and fungal genotypes among trees suggested that the algal symbiont was being dispersed in the lichen soredium. Low fungal specificity for multiple algal genotypes and a hypothesized algal switch may be important life history strategies for E. mesomorpha to adapt to changing environmental conditions.     

Heveochlorella (Trebouxiophyceae): a little‐known genus of unicellular green algae outside the Trebouxiales emerges unexpectedly as a major clade of lichen photobionts in foliicolous communities

Foliicolous lichens are formed by diverse, highly specialized fungi that establish themselves and complete their life cycle within the brief duration of their leaf substratum. Over half of these lichen‐forming fungi are members of either the Gomphillaceae or Pilocarpaceae, and associate with Trebouxia‐like green algae whose identities have never been positively determined. We investigated the phylogenetic affinities of these photobionts to better understand their role in lichen establishment on an ephemeral surface. Thallus samples of Gomphillaceae and Pilocarpaceae were collected from foliicolous communities in southwest Florida and processed for sequencing of photobiont marker genes, algal cultivation and/or TEM. Additional specimens from these families and also from Aspidothelium (Thelenellaceae) were collected from a variety of substrates globally. Sequences from rbcL and nuSSU regions were obtained and subjected to Maximum Likelihood and Bayesian analyses. Analysis of 37 rbcL and 7 nuSSU algal sequences placed all photobionts studied within the provisional trebouxiophycean assemblage known as the Watanabea clade. All but three of the sequences showed affinities within Heveochlorella, a genus recently described from tree trunks in East Asia. The photobiont chloroplast showed multiple thylakoid stacks penetrating the pyrenoid centripetally as tubules lined with pyrenoglobuli, similar to the two described species of Heveochlorella. We conclude that Heveochlorella includes algae of potentially major importance as lichen photobionts, particularly within (but not limited to) foliicolous communities in tropical and subtropical regions worldwide. The ease with which they may be cultivated on minimal media suggests their potential to thrive free‐living as well as in lichen symbiosis.     

Carotenoid composition and metabolism in green and blue-green algal lichens in the field

The carotenoid composition of 33 species of green algal lichens and 5 species of blue-green algal lichens was examined and compared with that of the leaves of higher plants. As in higher plants, green algal lichen species which were found in both shade and full sunlight exhibited higher levels of the carotenoids involved in photoprotective thermal energy dissipation (zeaxanthin as well as the total xanthophyll cycle pool) in the sun than in the shade. This was particularly true when thalli were moist during exposure to high light, or presumably became desiccated in full sunlight. However, the reverse trend in the carotenoid composition of green algal lichens was also observed in those species which were found predominantly either in the shade or in full sunlight. In this case sun-exposed lichens often possessed lower levels of zeaxanthin and of the components of the xanthophyll cycle than lichens which were found in the shade. In contrast to higher plants, the lichens from all habitats exhibited a relatively high ratio of carotenoids to chlorophylls (more characteristic of sun leaves), very low levels of α-carotene (similar to that found in sun leaves), and a level of β-carotene similar to that found in shade leaves. Zeaxanthin, but not the expoxides of the xanthophyll cycle, was also frequently found in blue-green algal lichens. A trend for increasing levels of zeaxanthin with increasing growth light regime was observed inPeltigera rufescens, the species which was found to occur over the widest range of light environments. The level of zeaxanthin per chlorophylla in these blue-green algal lichens was in a range similar to that per chlorophylla+b in green algal lichens. However, zeaxanthin was also absent in one species,Collema cristatum, in full sunlight. Thus, the zeaxanthin content of the blue-green algal lichens can be similar to that of higher plants, or it can be rather dissimilar, as was also the case in the green algal lichen species. The presence of large amounts of ketocarotenoids in blue-green algal lichens is also noteworthy.     

Combined observational and experimental data provide limited support for facilitation in lichens

It is increasingly recognized that facilitative interactions can shape communities. One of the mechanisms through which facilitation may operate is when one species facilitates the colonization of another through the exchange of shared symbionts. Lichens are symbiotic associations composed of a mycobiont (lichenised‐fungus) and one or two photobionts (algae or cyanobacteria). Different lichen species may have overlapping specificity for photobionts, creating the possibility that facilitation drives lichen community assembly. To investigate whether facilitation occurs in lichens, we combined an observational study (a) with a manipulative field experiment (b). For (a), we quantified the effect of local patch conditions, facilitation and the size of the surrounding metapopulation on colonizations of an epixylic lichen species (Cladonia botrytes) in an area of managed boreal forest. This was done by twice surveying lichens on 293 stumps, located in stands of three age classes. For (b), we treated unoccupied surfaces of 56 cut stumps with algal mixtures of an Asterochloris photobiont and recorded C. botrytes colonizations over three years. In (a), colonization rates of C. botrytes increased with increasing abundance of other lichen species with specificity for Asterochloris photobionts, consistent with an effect of facilitation. However, in the field experiment (b), colonizations of the focal species did not provide support for facilitation. We conclude that our study provides limited support for facilitation in green‐algal lichens, underscoring the importance of combining observational studies with experiments when studying species interactions.     

NEW ULTRASTRUCTURAL ASPECTS OF PYRENOIDS OF THE LICHEN PHOTOBIONT TREBOUXZA (MICROTHAMNIALES,CHLOROPHYTA)1

The pyrenoid structure of Trebouxia, a photobiont of two lichen species, Umbilicaria cinereorufescens (Schaer.) Frey and Parmelia sulcata Taylor, was investigated. In both lichen species, the pyrenoid of the photobiont exhibited straight, unbranched, long or short tubules. In the first lichen species, multiple pyrenoids were observed occasionally, while in the second one, homogeneous masses, called protein bodies, appeared between the thylakoids. These protein bodies were previously observed in some other species of the family Umbilicariaceae. Serial sections from single pyrenoids showed that tubules of the Impressa-type pyrenoid were closely associated with pyrenoglobuli. The three-dimensional reconstruction of a complete chloroplast of a P. sulcata algal cell showed that the protein bodies were spatially separate structures. Immunolocalization techniques to detect the presence of ribulose-bisphosphate carboxylase (Rubisco) in the chloroplast showed that this enzyme was present primarily in the pyrenoid matrix. When protein bodies were present in the chloroplast, Rubisco appeared to be localized in these structures. The presence of pyrenoid satellites and protein bodies with reactivity to anti-Rubisco may be related to the nutritional conditions of the thalli.     

CHEMOTAXONOMY IN MARINE ALGAE: CHEMICAL SEPARATION OF SOME LAURENCIA SPECIES (RHODOPHYTA) FROM THE GULF OF CALIFORNIA1

Species separation in the genus Laurencia (Rhodomelaceae, Rhodophyta) is complicated by the high degree of morphological variation within the species. Chemical investigations on a worldwide basis of over 15 species indicate that 1 or more of the halogenated natural products synthesized by Laurencia are unique to each species. Our chemical investigations of Laurencia pacifica, as presently understood from the Gulf of California, indicate that more than 1 species had been included under this name. Thin layer chromatographic (TLC) comparisons of the halogenated components of 3 recognizable forms of “L. pacifica” were completed. The results revealed 3 distinct forms, with halogenated products unique to each form. In each form the observed chemical characters had been previously isolated and identified and could now be positively assigned to their algal source. Comparisons were also conducted with L. pacifica Kylin (1941) from the type locality of the species, La Jolla, California, and revealed that it contained another halogenated product different from those isolated from the Gulf species. We conclude that 3 species of Laurencia have been elucidated in the Gulf of California and these are separate from L. pacifica Kylin. Each species can be distinguished by its characteristic array of halogenated compounds. Comparative thin layer chromatography of the lipid components of morphologically similar Laurencia species should prove to be a useful new taxonomic aid.     

High photobiont diversity associated with the euryoecious lichen-forming ascomycete Lecanora rupicola (Lecanoraceae, Ascomycota)

The diversity and phylogenetic position of photobionts in the widespread saxicolous, crustose lichen-forming ascomycete Lecanora rupicola s.l. is presented. The algal partners of this lichen species complex belong to diverse and unrelated lineages in the genus Trebouxia . Specimens were sampled from different habitats and geographical origins. Either whole thallus DNA extractions or minute fragments of the algal layer of the lichen thallus were subjected to polymerase chain reaction, using primers that specifically amplify internal transcribed spacer rDNA of the photobionts. No correlations between different chemical races of L. rupicola with particular lineages of Trebouxia spp. were found. Irrespective of the different algal partners, all lichen thalli abundantly developed ascomata. L. rupicola apparently maintains full fecundity with a low degree of selectivity for photobionts, which promotes the occurrence of this lichen-forming species in ample ecological situations.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 283–293.     

Algal and Fungal Diversity in Antarctic Lichens

The composition of lichen ecosystems except mycobiont and photobiont has not been evaluated intensively. In addition, recent studies to identify algal genotypes have raised questions about the specific relationship between mycobiont and photobiont. In the current study, we analyzed algal and fungal community structures in lichen species from King George Island, Antarctica, by pyrosequencing of eukaryotic large subunit (LSU) and algal internal transcribed spacer (ITS) domains of the nuclear rRNA gene. The sequencing results of LSU and ITS regions indicated that each lichen thallus contained diverse algal species. The major algal operational taxonomic unit (OTU) defined at a 99% similarity cutoff of LSU sequences accounted for 78.7–100% of the total algal community in each sample. In several cases, the major OTUs defined by LSU sequences were represented by two closely related OTUs defined by 98% sequence similarity of ITS domain. The results of LSU sequences indicated that lichen‐associated fungi belonged to the Arthoniomycetes, Eurotiomycetes, Lecanoromycetes, Leotiomycetes, and Sordariomycetes of the Ascomycota, and Tremellomycetes and Cystobasidiomycetes of the Basidiomycota. The composition of major photobiont species and lichen‐associated fungal community were mostly related to the mycobiont species. The contribution of growth forms or substrates on composition of photobiont and lichen‐associated fungi was not evident.     

Phaeocystis and its interaction with viruses

Over the years, viruses have been shown to be mortality agents for a wide range of phytoplankton species, including species within the genus Phaeocystis (Prymnesiophyceae). With its polymorphic life cycle, its worldwide distribution, and the capacity of several of the Phaeocystis species to form dense blooms, this genus is a key player for our understanding of biogeochemical cycling of elements. This paper provides an overview of what is know to date about the ecological role of viruses in regulating Phaeocystis population dynamics. It explores which variables affect the algal host–virus interactions, and examines the impact of virally induced cell lysis of Phaeocystis on the function and structure of the pelagic food web as well as on the flow of organic carbon and nutrients.