A critical review of soil algae as a crucial soil biological component of high ecological and economic significance.

Aero-terrestrial algae are ecologically and economically valuable bioresources contributing to carbon sequestration, sustenance of soil health, and fertility. Compared to aquatic algae, the literature on subaerial algae is minimal, including studies of distinctive habitats such as forest soils, agricultural fields, deserts, polar regions, specific subaerial zones, artificial structures, and tropical soils. The primary goal here was to identify the gaps and scope of research on such algae. Accordingly, the literature was analyzed per sub-themes, such as the "nature of current research data on terrestrial algae," "methodological approaches," "diversity," "environmental relationships," "ecological roles," and "economic significance." The review showed there is a high diversity of algae in soils, especially members belonging to the Cyanophyta (Cyanobacteria) and Chlorophyta. Algal distributions in terrestrial environments depend on the microhabitat conditions, and many species of soil algae are sensitive to specific soil conditions. The ecological significance of soil algae includes primary production, the release of biochemical stimulants and plant growth promoters into soils, nitrogen fixation, solubilization of minerals, and the enhancement and maintenance of soil fertility. Since aero-terrestrial habitats are generally stressed environments, algae of such environments can be rich in rare metabolites and natural products. For example, epilithic soil algae use wet adhesive molecules to fix them firmly on the substratum. Exploring the ecological roles and economic utility of soil and other subaerial algae could be helpful for the development of algae-based industries and for achieving sustainable soil management.

Terrestrial algae: pioneer organisms of carbonate rock solutional weathering in South China karst.

The formation of soil in karst ecosystem has always been a scientific problem of great concern to human beings. Algae can grow on the exposed and non-nutrition carbonate surface, inducing and accelerating weathering of rock substrates, thus promoting soil formation. Yet the actual contribution of algae to solutional weathering intensity remains unclear. In this study, we performed weathering simulation experiment on two algae species (Klebsormidium dissectum (F.Gay) H.Ettl & G.Gärtner and Chlorella vulgaris Beijerinck), which were screened from carbonated rock surfaces from a typical karst region in South China. The results showed: (1) both algae have solutional weathering effect on carbonate rock, (2) there is no difference of solutional intensity observed, yet the solutional modes are different, suggesting different ecological adaptative strategies, (3) algae on carbonate rocks have higher carbonic anhydrase activity (CAA) and secrete more extracellular polysaccharide (EPS), accelerating rock weathering. (4) The absolute dissolution amount of carbonate rock with algae participation is 3 times of that of without algae. These results indicate the significant impact of terrestrial algae on carbonate rock solutional weathering and provides quantitative evidence that terrestrial algae are pioneer species. It also contributes to our further understanding of soil formation in karst ecosystems in South China.

Biological Soil Crust From Mesic Forests Promote a Specific Bacteria Community.

Biological soil crusts (biocrusts) harbor a diverse community of various microorganisms with microalgae as primary producers and bacteria living in close association. In mesic regions, biocrusts emerge rapidly on disturbed surface soil in forest, typically after clear-cut or windfall. It is unclear whether the bacterial community in biocrusts is similar to the community of the surrounding soil or if biocrust formation promotes a specific bacterial community. Also, many of the interactions between bacteria and algae in biocrusts are largely unknown. Through high-throughput-sequencing analysis of the bacterial community composition, correlated drivers, and the interpretation of biological interactions in a biocrust of a forest ecosystem, we show that the bacterial community in the biocrust represents a subset of the community of the neighboring soil. Bacterial families connected with degradation of large carbon molecules, like cellulose and chitin, and the bacterivore Bdellovibrio were more abundant in the biocrust compared to bulk soil. This points to a closer interaction and nutrient recycling in the biocrust compared to bulk soil. Furthermore, the bacterial richness was positively correlated with the content of mucilage producing algae. The bacteria likely profit from the mucilage sheaths of the algae, either as a carbon source or protectant from grazing or desiccation. Comparative sequence analyses revealed pronounced differences between the biocrust bacterial microbiome. It seems that the bacterial community of the biocrust is recruited from the local soil, resulting in specific bacterial communities in different geographic regions.

Six Newly Sequenced Chloroplast Genomes From Trentepohliales: The Inflated Genomes, Alternative Genetic Code and Dynamic Evolution.

Cephaleuros is often known as an algal pathogen with 19 taxonomically valid species, some of which are responsible for red rust and algal spot diseases in vascular plants. No chloroplast genomes have yet been reported in this genus, and the limited genetic information is an obstacle to understanding the evolution of this genus. In this study, we sequenced six new Trentepohliales chloroplast genomes, including four Cephaleuros and two Trentepohlia. The chloroplast genomes of Trentepohliales are large compared to most green algae, ranging from 216 to 408 kbp. They encode between 93 and 98 genes and have a GC content of 26-36%. All new chloroplast genomes were circular-mapping and lacked a quadripartite structure, in contrast to the previously sequenced Trentepohlia odorata, which does have an inverted repeat. The duplicated trnD -GTC, petD, and atpA genes in C. karstenii may be remnants of the IR region and shed light on its reduction. Chloroplast genes of Trentepohliales show elevated rates of evolution, strong rearrangement dynamics and several genes display an alternative genetic code with reassignment of the UGA/UAG codon presumably coding for arginine. Our results present the first whole chloroplast genome of the genus Cephaleuros and enrich the chloroplast genome resources of Trentepohliales.

Thorsmoerkia curvula gen. et spec. nov. (Trebouxiophyceae, Chlorophyta), a semi-terrestrial microalga from Iceland exhibits high levels of unsaturated fatty acids.

A terrestrial green alga was isolated at Iceland, and the strain (SAG 2627) was described for its morphology and phylogenetic position and tested for biotechnological capabilities. Cells had a distinctly curved, crescent shape with conical poles and a single parietal chloroplast. Phylogenetic analyses of 18S rDNA and rbcL markers placed the strain into the Trebouxiophyceae (Chlorophyta). The alga turned out to belong to an independent lineage without an obvious sister group within the Trebouxiophyceae. Based on morphological and phylogenetic data, the strain was described as a new genus and species, Thorsmoerkia curvula gen. et sp. nov. Biomass was generated in column reactors and subsequently screened for promising metabolites. Growth was optimized by pH-regulated, episodic CO2 supplement during the logarithmic growth-phase, and half of the biomass was thereafter exposed to nitrogen and phosphate depletion. The biomass yield reached up to 53.5 mg L-1 day-1. Fatty acid (FA) production peaked at 24 mg L-1 day-1 and up to 83% of all FAs were unsaturated. At the end of the log phase, approximately 45% of dry mass were lipids, including eicosapentaenoic acid. Carotenoid production reached up to 2.94 mg L-1 day-1 but it was halted during the stress phase. The N-linked glycans of glycoproteins were assessed to reveal chemotaxonomic patterns. The study demonstrated that new microalgae can be found at Iceland, potentially suitable for applied purposes. The advantage of T. curvula is its robustness and that significant amounts of lipids are already accumulated during log phase, making a subsequent stress exposure dispensable.

Klebsormidin A and B, Two New UV-Sunscreen Compounds in Green Microalgal Interfilum and Klebsormidium Species (Streptophyta) From Terrestrial Habitats.

The terrestrial green algal members of the genera Interfilum and Klebsormidium (Klebsormidiophyceae, Streptophyta) are found in biological soil crusts of extreme habitats around the world where they are regularly exposed, among other abiotic stress factors, to high levels of ultraviolet radiation (UVR). As a consequence those species synthesize and accumulate either one or two mycosporine-like amino acids (MAAs), but with a missing structural elucidation up to now. Therefore, in the present study both MAAs were chemically isolated and structurally elucidated. The two new compounds exhibit absorption maxima of 324 nm. MAA 1 has a molecular weight of 467 and MAA 2 of 305, and the latter (MAA 2) was identified as N-(4,5-dihydroxy-5-(hydroxymethyl)-2-methoxy-3-oxocyclohex-1-en-1-yl)-N-methylserine using one- and two-dimensional 1H and 13C-NMR spectroscopy. MAA 1 contains an additional sugar moiety. As trivial names for these two novel MAAs we suggest klebsormidin A and klebsormidin B. Different species from all previously described phylogenetic clades of Klebsormidiophyceae were chemically screened for their MAA composition in aqueous extracts using RP-HPLC and LC-MS. The novel klebsormidin A was present throughout all clades and hence could be suitable as a chemotaxonomic marker. Additionally, controlled UVR-exposure experiments with all investigated species showed that MAA biosynthesis and intracellular enrichment is strongly induced by short wavelengths, supporting the function of these compounds as natural UV-sunscreen as well as explaining the cosmopolitan distribution and ecological success of Interfilum and Klebsormidium in terrestrial habitats.

Evo-physio: on stress responses and the earliest land plants.

Embryophytes (land plants) can be found in almost any habitat on the Earth's surface. All of this ecologically diverse embryophytic flora arose from algae through a singular evolutionary event. Traits that were, by their nature, indispensable for the singular conquest of land by plants were those that are key for overcoming terrestrial stressors. Not surprisingly, the biology of land plant cells is shaped by a core signaling network that connects environmental cues, such as stressors, to the appropriate responses-which, thus, modulate growth and physiology. When did this network emerge? Was it already present when plant terrestrialization was in its infancy? A comparative approach between land plants and their algal relatives, the streptophyte algae, allows us to tackle such questions and resolve parts of the biology of the earliest land plants. Exploring the biology of the earliest land plants might shed light on exactly how they overcame the challenges of terrestrialization. Here, we outline the approaches and rationale underlying comparative analyses towards inferring the genetic toolkit for the stress response that aided the earliest land plants in their conquest of land.

DNA cloning demonstrates high genetic heterogeneity in populations of the subaerial green alga Trentepohlia (Trentepohliales, Chlorophyta).

Mats of the green alga Trentepohlia, a genus widely distributed in the tropics as well as temperate regions, have always been perceived as homogeneous (i.e., formed by only one species). As such, their general nature and specific feature play a supportive role in the species delimitation. However, the presence of morphologically dissimilar thalli was observed under the light microscope and when cultivating a piece of a single mat. To address this, we performed DNA cloning of the rbcL gene on mat fragments of T. abietina, T. annulata, T. jolithus and T. umbrina sampled in Europe to reveal if they are composed of one or more species. We revealed that more Trentepohlia haplotypes may coexist in a single mat. In consideration of this, we conclude that the use of material isolated in unialgal culture will be almost mandatory for a taxonomic reassessment of this complicated genus. Another direct implication of this problem is that herbarium specimens consisting of field-collected material should not be used for direct sequencing. We further hypothesize the reasons why multiple haplotypes of Trentepohlia occur more frequently in the tuft-like mats. Possibly, fragments and/or cells of other microalgae, including other species of Trentepohlia, might be retained in such mats more easily than in the crustose trentepohlialean mats.

Survey of the occurrence of desiccation-induced quenching of basal fluorescence in 28 species of green microalgae.

MAIN CONCLUSION: Desiccation-induced chlorophyll fluorescence quenching seems to be an indispensable part of desiccation resistance in the surveyed 28 green microalgal species. Lichens are desiccation tolerant meta-organisms. In the desiccated state photosynthesis is inhibited rendering the photobionts potentially sensitive to photoinhibition. As a photoprotective mechanism, strong non-radiative dissipation of absorbed light leading to quenching of chlorophyll fluorescence has been proposed. Desiccation-induced quenching affects not only variable fluorescence, but also the so-called basal fluorescence, F0. This phenomenon is well-known for intact lichens and some free living aero-terrestrial algae, but it was often absent in isolated lichen algae. Therefore, a thorough screening for the appearance of desiccation-induced quenching was undertaken with 13 different aero-terrestrial microalgal species and lichen photobionts. They were compared with 15 aquatic green microalgal species, among them also three marine species. We asked the following questions: Do isolated lichen algae show desiccation-induced quenching? Are aero-terrestrial algae different in this respect to aquatic algae and is the potential for desiccation-induced quenching coupled to desiccation tolerance? How variable is desiccation-induced quenching among species? Most of the aero-terrestrial algae, including all lichen photobionts, showed desiccation-induced quenching, although highly variable in extent, whereas most of the aquatic algae did not. All algae displaying quenching were also desiccation tolerant, whereas all algae unable to perform desiccation-induced quenching were desiccation intolerant. Desiccation-induced fluorescence quenching seems to be an indispensable part of desiccation resistance in the investigated species.

Polyols and UV-sunscreens in the Prasiola-clade (Trebouxiophyceae, Chlorophyta) as metabolites for stress response and chemotaxonomy.

In many regions of the world, aeroterrestrial green algae of the Trebouxiophyceae (Chlorophyta) represent very abundant soil microorganisms, and hence their taxonomy is crucial to investigate their physiological performance and ecological importance. Due to a lack in morphological features, taxonomic and phylogenetic studies of Trebouxiophycean algae can be a challenging task. Since chemotaxonomic markers could be a great assistance in this regard, 22 strains of aeroterrestrial Trebouxiophyceae were chemically screened for their polyol-patterns as well as for mycosporine-like amino acids (MAAs) in their aqueous extracts using RP-HPLC and LC-MS. d-sorbitol was exclusively detected in members of the Prasiolaceae family. The novel MAA prasiolin and a related compound ("prasiolin-like") were present in all investigated members of the Prasiola-clade, but missing in all other tested Trebouxiophyceae. While prasiolin could only be detected in field material directly after extraction, the "prasiolin-like" compound present in the other algae was fully converted into prasiolin after 24 h. These findings suggest d-sorbitol and prasiolin-like compounds are suitable chemotaxonomic markers for the Prasiolaceae and Prasiola-clade, respectively. Additional UV-exposure experiments with selected strains show that MAA formation and accumulation can be induced, supporting their role as UV-sunscreen.

MOLECULAR PHYLOGENY OF ANTARCTIC PRASIOLA (PRASIOLALES, TREBOUXIOPHYCEAE) REVEALS EXTENSIVE CRYPTIC DIVERSITY(1).

Trebouxiophytes of the genus Prasiola are well known in Antarctica, where they are among the most important primary producers. Although many aspects of their biology have been thoroughly investigated, the scarcity of molecular data has so far prevented an accurate assessment of their taxonomy and phylogenetic position. Using sequences of the chloroplast genes rbcL and psaB, we demonstrate the existence of three cryptic species that were previously confused under Prasiola crispa (Lightfoot) Kützing. Genuine P. crispa occurs in Antarctica; its presence was confirmed by comparison with the rbcL sequence of the type specimen (from the Isle of Skye, Scotland). Prasiola antarctica Kützing is resurrected as an independent species to designate algae with gross morphology identical to P. crispa but robustly placed in a separate lineage. The third species is represented by specimens identified as P. calophylla (Carmichael ex Greville) Kützing in previous studies, but clearly separated from European P. calophylla (type locality: Argyll, Scotland); this alga is described as P. glacialis sp. nov. The molecular data demonstrated the presence of P. crispa in Maritime and Continental Antarctica. P. antarctica was recorded from the Antarctic Peninsula and Shetland Islands, and P. glacialis from the Southern Ocean islands and coast. Such unexpected cryptic diversity highlights the need for a taxonomic reassessment of many published Antarctic records of P. crispa. The results also indicate that marine species of Prasiola form a well-supported monophyletic group, whereas the phylogenetic diversity of freshwater species is higher than previously suspected (at least three separate lineages within the genus include species living in this type of environments).