Publications by authors named "Martin Grube"

109 Publications

The Lichens' Microbiota, Still a Mystery?

Front Microbiol 2021 30;12:623839. Epub 2021 Mar 30.

Institute of Microbiology, University Greifswald, Greifswald, Germany.

Lichens represent self-supporting symbioses, which occur in a wide range of terrestrial habitats and which contribute significantly to mineral cycling and energy flow at a global scale. Lichens usually grow much slower than higher plants. Nevertheless, lichens can contribute substantially to biomass production. This review focuses on the lichen symbiosis in general and especially on the model species L. Hoffm., which is a large foliose lichen that occurs worldwide on tree trunks in undisturbed forests with long ecological continuity. In comparison to many other lichens, . is less tolerant to desiccation and highly sensitive to air pollution. The name-giving mycobiont (belonging to the Ascomycota), provides a protective layer covering a layer of the green-algal photobiont () and interspersed cyanobacterial cell clusters ( spec.). Recently performed metaproteome analyses confirm the partition of functions in lichen partnerships. The ample functional diversity of the mycobiont contrasts the predominant function of the photobiont in production (and secretion) of energy-rich carbohydrates, and the cyanobiont's contribution by nitrogen fixation. In addition, high throughput and state-of-the-art metagenomics and community fingerprinting, metatranscriptomics, and MS-based metaproteomics identify the bacterial community present on as a surprisingly abundant and structurally integrated element of the lichen symbiosis. Comparative metaproteome analyses of lichens from different sampling sites suggest the presence of a relatively stable core microbiome and a sampling site-specific portion of the microbiome. Moreover, these studies indicate how the microbiota may contribute to the symbiotic system, to improve its health, growth and fitness.
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http://dx.doi.org/10.3389/fmicb.2021.623839DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8042158PMC
March 2021

Lichens - growing greenhouses .

Authors:
Martin Grube

Microb Cell 2021 Mar 1;8(3):65-68. Epub 2021 Mar 1.

Institute of Biology, University of Graz, Graz, Austria.

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http://dx.doi.org/10.15698/mic2021.03.743DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7919387PMC
March 2021

The beauty and the yeast: can the microalgae form a borderline lichen with ?

Symbiosis 2020 Nov 27;82(1):123-131. Epub 2020 Jul 27.

Department of Biology, Biotechnical Faculty, University of Ljubljana, Večnapot 111, 1000 Ljubljana, Slovenia.

Lichenized fungi usually develop complex, stratified morphologies through an intricately balanced living together with their algal partners, but several species are known to form only more or less loose associations with algae. These borderline lichens are still little explored although they could inform us about early stages of lichen evolution. We studied the association of the extremely halotolerant fungus with the alga , discovered in a cave in the Atacama Desert (Chile), and with . , common inhabitant of saltern brines. . forms small colonies, in which cells of . can be frequently observed, while such interaction has not been observed with . . As symbiotic interactions between and have not been reported, we performed a series of co-cultivation experiments to inspect whether these species could interact and develop more distinct lichen-like symbiotic structures. We set up co-cultures between axenic strains of (isolated both from Mediterranean salterns and from the Atacama cave) and isolates of . (from the Atacama cave) and . (isolated from Mediterranean salterns). Although we used different growth media and cultivation approaches, bright field and SEM microscopy analyses did not indicate any mutual effects in these experiments. We discuss the implications for fungal algal interactions along the transition from algal exploiters to lichen symbioses.
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http://dx.doi.org/10.1007/s13199-020-00697-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7116670PMC
November 2020

Antimicrobial-specific response from resistance gene carriers studied in a natural, highly diverse microbiome.

Microbiome 2021 01 27;9(1):29. Epub 2021 Jan 27.

Institute of Environmental Biotechnology, Graz University of Technology, Graz, Austria.

Background: Antimicrobial resistance (AMR) is a major threat to public health. Microorganisms equipped with AMR genes are suggested to have partially emerged from natural habitats; however, this hypothesis remains inconclusive so far. To understand the consequences of the introduction of exogenic antimicrobials into natural environments, we exposed lichen thalli of Peltigera polydactylon, which represent defined, highly diverse miniature ecosystems, to clinical (colistin, tetracycline), and non-clinical (glyphosate, alkylpyrazine) antimicrobials. We studied microbiome responses by analysing DNA- and RNA-based amplicon libraries and metagenomic datasets.

Results: The analyzed samples consisted of the thallus-forming fungus that is associated with cyanobacteria as well as other diverse and abundant bacterial communities (up to 10 16S rRNA gene copies ng DNA) dominated by Alphaproteobacteria and Bacteroidetes. Moreover, the natural resistome of this meta-community encompassed 728 AMR genes spanning 30 antimicrobial classes. Following 10 days of exposure to the selected antimicrobials at four different concentrations (full therapeutic dosage and a gradient of sub-therapeutic dosages), we observed statistically significant, antimicrobial-specific shifts in the structure and function but not in bacterial abundances within the microbiota. We observed a relatively lower response after the exposure to the non-clinical compared to the clinical antimicrobial compounds. Furthermore, we observed specific bacterial responders, e.g., Pseudomonas and Burkholderia to clinical antimicrobials. Interestingly, the main positive responders naturally occur in low proportions in the lichen holobiont. Moreover, metagenomic recovery of the responders' genomes suggested that they are all naturally equipped with specific genetic repertoires that allow them to thrive and bloom when exposed to antimicrobials. Of the responders, Sphingomonas, Pseudomonas, and Methylobacterium showed the highest potential.

Conclusions: Antimicrobial exposure resulted in a microbial dysbiosis due to a bloom of naturally low abundant taxa (positive responders) with specific AMR features. Overall, this study provides mechanistic insights into community-level responses of a native microbiota to antimicrobials and suggests novel strategies for AMR prediction and management. Video Abstract.
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http://dx.doi.org/10.1186/s40168-020-00982-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7841911PMC
January 2021

The Bacterial Community of the Foliose Macro-lichen Peltigera frigida Is More than a Mere Extension of the Microbiota of the Subjacent Substrate.

Microb Ecol 2021 May 6;81(4):965-976. Epub 2021 Jan 6.

Faculty of Sciences, Department of Ecological Sciences, Universidad de Chile, Santiago, Chile.

Lichens host highly diverse microbial communities, with bacteria being one of the most explored groups in terms of their diversity and functioning. These bacteria could partly originate from symbiotic propagules developed by many lichens and, perhaps more commonly and depending on environmental conditions, from different sources of the surroundings. Using the narrowly distributed species Peltigera frigida as an object of study, we propose that bacterial communities in these lichens are different from those in their subjacent substrates, even if some taxa might be shared. Ten terricolous P. frigida lichens and their substrates were sampled from forested sites in the Coyhaique National Reserve, located in an understudied region in Chile. The mycobiont identity was confirmed using partial 28S and ITS sequences. Besides, 16S fragments revealed that mycobionts were associated with the same cyanobacterial haplotype. From both lichens and substrates, Illumina 16S amplicon sequencing was performed using primers that exclude cyanobacteria. In lichens, Proteobacteria was the most abundant phylum (37%), whereas soil substrates were dominated by Acidobacteriota (39%). At lower taxonomic levels, several bacterial groups differed in relative abundance among P. frigida lichens and their substrates, some of them being highly abundant in lichens but almost absent in substrates, like Sphingomonas (8% vs 0.2%), and others enriched in lichens, as an unassigned genus of Chitinophagaceae (10% vs 2%). These results reinforce the idea that lichens would carry some components of their microbiome when propagating, but they also could acquire part of their bacterial community from the substrates.
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http://dx.doi.org/10.1007/s00248-020-01662-yDOI Listing
May 2021

Shed Light in the DaRk LineagES of the Fungal Tree of Life-STRES.

Life (Basel) 2020 Dec 19;10(12). Epub 2020 Dec 19.

Institute of Natural Sciences and Technology in the Arts, Academy of Fine Arts Vienna, Vienna 22180, Austria.

The polyphyletic group of black fungi within the Ascomycota (Arthoniomycetes, Dothideomycetes, and Eurotiomycetes) is ubiquitous in natural and anthropogenic habitats. Partly because of their dark, melanin-based pigmentation, black fungi are resistant to stresses including UV- and ionizing-radiation, heat and desiccation, toxic metals, and organic pollutants. Consequently, they are amongst the most stunning extremophiles and poly-extreme-tolerant organisms on Earth. Even though ca. 60 black fungal genomes have been sequenced to date, [mostly in the family Herpotrichiellaceae (Eurotiomycetes)], the class Dothideomycetes that hosts the largest majority of extremophiles has only been sparsely sampled. By sequencing up to 92 species that will become reference genomes, the "Shed light in The daRk lineagES of the fungal tree of life" (STRES) project will cover a broad collection of black fungal diversity spread throughout the Fungal Tree of Life. Interestingly, the STRES project will focus on mostly unsampled genera that display different ecologies and life-styles (e.g., ant- and lichen-associated fungi, rock-inhabiting fungi, etc.). With a resequencing strategy of 10- to 15-fold depth coverage of up to ~550 strains, numerous new reference genomes will be established. To identify metabolites and functional processes, these new genomic resources will be enriched with metabolomics analyses coupled with transcriptomics experiments on selected species under various stress conditions (salinity, dryness, UV radiation, oligotrophy). The data acquired will serve as a reference and foundation for establishing an encyclopedic database for fungal metagenomics as well as the biology, evolution, and ecology of the fungi in extreme environments.
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http://dx.doi.org/10.3390/life10120362DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7767062PMC
December 2020

Contrasting Environmental Drivers Determine Biodiversity Patterns in Epiphytic Lichen Communities along a European Gradient.

Microorganisms 2020 Dec 1;8(12). Epub 2020 Dec 1.

Área de Biodiversidad y Conservación, ESCET, Universidad Rey Juan Carlos, c/Tulipán s/n, 28933 Móstoles, Spain.

Assessing the ecological impacts of environmental change on biological communities requires knowledge of the factors driving the spatial patterns of the three diversity facets along extensive environmental gradients. We quantified the taxonomic (TD), functional (FD), and phylogenetic diversity (PD) of lichen epiphytic communities in 23 beech forests along Europe to examine their response to environmental variation (climate, habitat quality, spatial predictors) at a continental geographic scale. We selected six traits related to the climatic conditions in forest ecosystems, the water-use strategy and the nutrient uptake, and we built a phylogenetic tree based on four molecular markers. FD and climate determined TD and PD, with spatial variables also affecting PD. The three diversity facets were primarily shaped by distinct critical predictors, with the temperature diurnal range affecting FD and PD, and precipitation of the wettest month determining TD. Our results emphasize the value of FD for explaining part of TD and PD variation in lichen communities at a broad geographic scale, while highlighting that these diversity facets provide complementary information about the communities' response under changing environmental conditions. Furthermore, traits such as growth form, photobiont type, and reproductive strategy mediated the response of lichen communities to abiotic factors emerging as useful indicators of macroclimatic variations.
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http://dx.doi.org/10.3390/microorganisms8121913DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7760525PMC
December 2020

Assembly of Bacterial Genomes from the Metagenomes of Three Lichen Species.

Microbiol Resour Announc 2020 Sep 17;9(38). Epub 2020 Sep 17.

Institute of Environmental Biotechnology, Graz University of Technology, Graz, Austria.

Bacteria have recently emerged as important constituents of lichen holobionts. Here, 29 bacterial metagenome-assembled genome (MAG) sequences were reconstructed from lichen metagenomes and taxonomically classified in four phyla. These results provide a pivotal resource for further exploration of the ecological roles played by bacterial symbionts in lichen holobionts.
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http://dx.doi.org/10.1128/MRA.00622-20DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7498425PMC
September 2020

Lichens redefined as complex ecosystems.

New Phytol 2020 09 2;227(5):1281-1283. Epub 2020 Jun 2.

Institute of Biology, University of Graz, Holteigasse 6, 8010, Graz, Austria.

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http://dx.doi.org/10.1111/nph.16630DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7497170PMC
September 2020

Integrative taxonomy confirms three species of (Arthoniaceae) in Norway.

MycoKeys 2020 23;62:27-51. Epub 2020 Jan 23.

NTNU University Museum, Norwegian University of Science and Technology, 7491 Trondheim, Norway.

We have studied the highly oceanic genus in Norway. Our aim has been to delimit species of in Norway based on an integrative taxonomic approach. The material studied comprises 120 specimens of , obtained through recent collecting efforts (2017 and 2018) or received from major fungaria in Denmark, Finland, Norway and Sweden, as well as from private collectors. We have assessed (1) species delimitations and relationships based on Bayesian and maximum likelihood phylogenetic analyses of three genetic markers (mtSSU, nucITS and ), (2) morphology and anatomy using standard light microscopy, and (3) secondary lichen chemistry using high-performance thin-layer chromatography. The results show three genetically distinct lineages of , representing , and comb. nov. The latter was originally described as Arthonia cinnabarina f. cuspidans and is herein raised to species level. All three species are supported by morphological, anatomical and chemical data.
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http://dx.doi.org/10.3897/mycokeys.62.48480DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6992689PMC
January 2020

Phylogenetic relationships of rock-inhabiting black fungi belonging to the widespread genera Lichenothelia and Saxomyces.

Mycologia 2019 Jan-Feb;111(1):127-160. Epub 2019 Feb 6.

a Department of Life Sciences , University of Trieste , via Giorgieri 10, 34127 Trieste , Italy.

Rock-inhabiting fungi (RIF) are adapted to thrive in oligotrophic environments and to survive under conditions of abiotic stress. Under these circumstances, they form biocoenoses with other tolerant organisms, such as lichens, or with less specific phototrophic consortia of aerial algae or cyanobacteria. RIF are phylogenetically diverse, and their plastic morphological characters hamper the straightforward species delimitation of many taxa. Here, we present a phylogenetic study of two RIF genera, Lichenothelia and Saxomyces. Representatives of both genera inhabit rather similar niches on rocks, but their phylogenetic relationships are unknown so far. The cosmopolitan genus Lichenothelia is recognized by characters of fertile ascomata and includes species with different life strategies. In contrast, Saxomyces species were described exclusively by mycelial characters found in cultured isolates from rock samples collected at high alpine elevations. Here, we use an extended taxon sampling of Dothideomycetes to study the phylogenetic relationships of both Lichenothelia and Saxomyces. We consider environmental samples, type species, and cultured isolates of both genera and demonstrate their paraphyly, as well as the occurrence of teleomorphs in Saxomyces. We applied three species delimitation methods to improve species recognition based on molecular data. We show the distinctiveness of the two main lineages of Lichenothelia (Lichenotheliales s. str.) and Saxomyces and discuss differences in species delimitation depending on molecular markers or methods. We revise the taxonomy of the two genera and describe three new taxa, Lichenothelia papilliformis, L. muriformis, and Saxomyces americanus, and the teleomorph of S. penninicus.
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http://dx.doi.org/10.1080/00275514.2018.1543510DOI Listing
May 2019

Enterobacteriaceae dominate the core microbiome and contribute to the resistome of arugula (Eruca sativa Mill.).

Microbiome 2019 01 29;7(1):13. Epub 2019 Jan 29.

Institute of Environmental Biotechnology, Graz University of Technology, Petersgasse 12, 8010, Graz, Austria.

Background: Arugula is a traditional medicinal plant and popular leafy green today. It is mainly consumed raw in the Western cuisine and known to contain various bioactive secondary metabolites. However, arugula has been also associated with high-profile outbreaks causing severe food-borne human diseases. A multiphasic approach integrating data from metagenomics, amplicon sequencing, and arugula-derived bacterial cultures was employed to understand the specificity of the indigenous microbiome and resistome of the edible plant parts.

Results: Our results indicate that arugula is colonized by a diverse, plant habitat-specific microbiota. The indigenous phyllosphere bacterial community was shown to be dominated by Enterobacteriaceae, which are well-equipped with various antibiotic resistances. Unexpectedly, the prevalence of specific resistance mechanisms targeting therapeutic antibiotics (fluoroquinolone, chloramphenicol, phenicol, macrolide, aminocoumarin) was only surpassed by efflux pump assignments.

Conclusions: Enterobacteria, being core microbiome members of arugula, have a substantial implication in the overall resistome. Detailed insights into the natural occurrence of antibiotic resistances in arugula-associated microorganisms showed that the plant is a hotspot for distinctive defense mechanisms. The specific functioning of microorganisms in this unusual ecosystem provides a unique model to study antibiotic resistances in an ecological context.
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http://dx.doi.org/10.1186/s40168-019-0624-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6352427PMC
January 2019

Bacterial communities in an optional lichen symbiosis are determined by substrate, not algal photobionts.

FEMS Microbiol Ecol 2019 03;95(3)

Department of Botany, Swedish Museum of Natural History, PO Box 50007, SE-10405 Stockholm, Sweden.

Borderline lichens are simple mutualistic symbioses between fungi and algae, where the fungi form loose mycelia interweaving algal cells, instead of forming a lichen thallus. Schizoxylon albescens shows two nutritional modes: it can either live as a borderline lichen on Populus tremula bark or as a saprotroph on Populus wood. This enables us to investigate the microbiota diversity in simple fungal-algal associations and to study the impact of lichenization on the structure of bacterial communities. We sampled three areas in Sweden covering the distribution of Schizoxylon, and using high-throughput sequencing of the 16S rRNA gene and fluorescence in situ hybridization we characterized the associated microbiota. Bacterial communities in lichenized and saprotrophic Schizoxylon were clearly distinct, but when comparing the microbiota with the respective substrates, only the fruiting bodies show clear differences in composition and abundance from the communities in the substrates. The colonization by either lichenized or saprotrophic mycelia of Schizoxylon did not significantly influence the microbiota in the substrate. This suggests that in a morphologically simple form of lichenization, as represented by the Schizoxylon-Coccomyxa system, algal-fungal interactions do not significantly influence bacterial communities, but a more complex structure of the lichen thallus is likely required for hosting specific microbiota.
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http://dx.doi.org/10.1093/femsec/fiz012DOI Listing
March 2019

Adaptions of Lichen Microbiota Functioning Under Persistent Exposure to Arsenic Contamination.

Front Microbiol 2018 30;9:2959. Epub 2018 Nov 30.

Institute of Environmental Biotechnology, Graz University of Technology, Graz, Austria.

Host-associated microbiota play an important role in the health and persistence of more complex organisms. In this study, metagenomic analyses were used to reveal microbial community adaptations in three lichen samples as a response to different arsenic concentrations at the sampling sites. Elevated arsenic concentrations at a former mining site expanded the spectrum and number of relevant functions in the lichen-associated microorganisms. Apparent changes affected the abundance of numerous detoxification-related genes, they were substantially enhanced in arsenic-polluted samples. Complementary quantifications of the arsenite S-adenosylmethionine methyltransferase () gene showed that its abundance is not strictly responding to the environmental arsenic concentrations. The analyzed samples contained rather low numbers of the gene with a maximum of 202 gene copies μl in total community DNA extracts. In addition, bacterial isolates were screened for the presence of . Positive isolates were exposed to different As(III) and As(V) concentrations and tolerated up to 30 mM inorganic arsenic in fluid media, while no substantial biotransformations were observed. Obtained data deepens our understanding related to adaptions of whole microbial communities to adverse environmental conditions. Moreover, this study provides the first evidence that the integrity of bacteria in the lichen holobiont is maintained by acquisition of specific resistances.
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http://dx.doi.org/10.3389/fmicb.2018.02959DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6283889PMC
November 2018

Leaves of Indoor Ornamentals Are Biodiversity and Functional Hotspots for Fungi.

Front Microbiol 2018 1;9:2343. Epub 2018 Oct 1.

Institute of Environmental Biotechnology, Graz University of Technology, Graz, Austria.

Leaf-inhabiting fungi are an important, but often overlooked component of molecular biodiversity studies. To understand their diversity and function in relation to plant species and climate, the phyllospheres of 14 phylogenetically diverse ornamental plant species were analyzed under different controlled greenhouse conditions. We found unexpectedly high fungal diversity (H' = 2.8-6.5), OTU numbers (449-1050) and abundances (10-10 CFU cm leaf surface) associated with all plants studied indoors. Despite experimental limitations, the composition of fungal communities were inclined toward a plant species-dependent pattern compared to the ambient climatic variables. Most detected fungi were patho- and saprotrophs showing a yeast-like growth morphology and were associated to the groups of endophytes and potential plant pathogens in a plant species-specific manner. A representative strain collection showed that 1/3 of the tested fungi (mainly , and .) were able to inhibit mycelial growth and 2/3 inhibit sporulation of the plant pathogen by the production of antifungal volatile organic compounds (VOCs) completely. This study indicates that plant leaves harbor a stable phyllosphere fungal diversity in diverse microclimates and enrich distinctive functional guilds.
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http://dx.doi.org/10.3389/fmicb.2018.02343DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6174238PMC
October 2018

Plasticity of a holobiont: desiccation induces fasting-like metabolism within the lichen microbiota.

ISME J 2019 02 11;13(2):547-556. Epub 2018 Oct 11.

Institute of Environmental Biotechnology, Graz University of Technology, Petersgasse 12, 8010, Graz, Austria.

The role of host-associated microbiota in enduring dehydration and drought is largely unknown. We have used lichens to study this increasingly important problem because they are the organisms that are optimally adapted to reoccurring hydration/dehydration cycles, and they host a defined and persistent bacterial community. The analysis of metatranscriptomic datasets from bacterial communities of the lung lichen (Lobaria pulmonaria (L.) Hoffm.), sampled under representative hydration stages, revealed significant structural shifts and functional specialization to host conditions. The hydrated samples showed upregulated transcription of transport systems, tRNA modification and various porins (Omp2b by Rhizobiales), whereas the desiccated samples showed different functions related to stress adaption prominently. Carbohydrate metabolism was activated under both conditions. Under dry conditions, upregulation of a specialized ketone metabolism indicated a switch to lipid-based nutrition. Several bacterial lineages were involved in a functional transition that was reminiscent of a 'fasting metaorganism'. Similar functional adaptions were assigned to taxonomically unrelated groups, indicating hydration-related specialization of the microbiota. We were able to show that host-associated bacterial communities are well adapted to dehydration by stress protection and changes of the metabolism. Moreover, our results indicate an intense interplay in holobiont functioning under drought stress.
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http://dx.doi.org/10.1038/s41396-018-0286-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6331575PMC
February 2019

Marine cyanolichens from different littoral zones are associated with distinct bacterial communities.

PeerJ 2018 17;6:e5208. Epub 2018 Jul 17.

Laboratoire de Biodiversité et Biotechnologies Microbiennes (LBBM), Sorbonne Université, CNRS, Banyuls sur mer, France.

The microbial diversity and function of terrestrial lichens have been well studied, but knowledge about the non-photosynthetic bacteria associated with marine lichens is still scarce. 16S rRNA gene Illumina sequencing was used to assess the culture-independent bacterial diversity in the strictly marine cyanolichen species and , and the maritime chlorolichen species which occupy different areas on the littoral zone. Inland terrestrial cyanolichens from Austria were also analysed as for the marine lichens to examine further the impact of habitat/lichen species on the associated bacterial communities. The and communities were significantly different from those of the maritime lichen found higher up on the littoral zone and these latter communities were more similar to those of the inland terrestrial lichens. The strictly marine lichens were dominated by the Bacteroidetes phylum accounting for 50% of the sequences, whereas Alphaproteobacteria, notably , dominated the maritime and the inland terrestrial lichens. Bacterial communities associated with the two species were significantly different sharing only 33 core OTUs, half of which were affiliated to the Bacteroidetes genera , and , suggesting an important role of these species in the marine lichen symbiosis. Marine cyanolichens showed a higher abundance of OTUs likely affiliated to moderately thermophilic and/or radiation resistant bacteria belonging to the Phyla Chloroflexi, Thermi, and the families Rhodothermaceae and Rubrobacteraceae when compared to those of inland terrestrial lichens. This most likely reflects the exposed and highly variable conditions to which they are subjected daily.
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http://dx.doi.org/10.7717/peerj.5208DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6054067PMC
July 2018

Considerations and consequences of allowing DNA sequence data as types of fungal taxa.

IMA Fungus 2018 Jun 24;9(1):167-175. Epub 2018 May 24.

Museum of Evolution, Uppsala University, Norbyvägen 16, 75236 Uppsala, Sweden.

Nomenclatural type definitions are one of the most important concepts in biological nomenclature. Being physical objects that can be re-studied by other researchers, types permanently link taxonomy (an artificial agreement to classify biological diversity) with nomenclature (an artificial agreement to name biological diversity). Two proposals to amend the International Code of Nomenclature for algae, fungi, and plants (ICN), allowing DNA sequences alone (of any region and extent) to serve as types of taxon names for voucherless fungi (mainly putative taxa from environmental DNA sequences), have been submitted to be voted on at the 11 International Mycological Congress (Puerto Rico, July 2018). We consider various genetic processes affecting the distribution of alleles among taxa and find that alleles may not consistently and uniquely represent the species within which they are contained. Should the proposals be accepted, the meaning of nomenclatural types would change in a fundamental way from physical objects as sources of data to the data themselves. Such changes are conducive to irreproducible science, the potential typification on artefactual data, and massive creation of names with low information content, ultimately causing nomenclatural instability and unnecessary work for future researchers that would stall future explorations of fungal diversity. We conclude that the acceptance of DNA sequences alone as types of names of taxa, under the terms used in the current proposals, is unnecessary and would not solve the problem of naming putative taxa known only from DNA sequences in a scientifically defensible way. As an alternative, we highlight the use of formulas for naming putative taxa (candidate taxa) that do not require any modification of the ICN.
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http://dx.doi.org/10.5598/imafungus.2018.09.01.10DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6048565PMC
June 2018

Fungal Diversity in Lichens: From Extremotolerance to Interactions with Algae.

Life (Basel) 2018 May 22;8(2). Epub 2018 May 22.

Institute of Biology, Karl-Franzens University of Graz, Holteigasse 6, 8010 Graz, Austria.

Lichen symbioses develop long-living thallus structures even in the harshest environments on Earth. These structures are also habitats for many other microscopic organisms, including other fungi, which vary in their specificity and interaction with the whole symbiotic system. This contribution reviews the recent progress regarding the understanding of the lichen-inhabiting fungi that are achieved by multiphasic approaches (culturing, microscopy, and sequencing). The lichen mycobiome comprises a more or less specific pool of species that can develop symptoms on their hosts, a generalist environmental pool, and a pool of transient species. Typically, the fungal classes Dothideomycetes, Eurotiomycetes, Leotiomycetes, Sordariomycetes, and Tremellomycetes predominate the associated fungal communities. While symptomatic lichenicolous fungi belong to lichen-forming lineages, many of the other fungi that are found have close relatives that are known from different ecological niches, including both plant and animal pathogens, and rock colonizers. A significant fraction of yet unnamed melanized ('black') fungi belong to the classes Chaethothyriomycetes and Dothideomycetes. These lineages tolerate the stressful conditions and harsh environments that affect their hosts, and therefore are interpreted as extremotolerant fungi. Some of these taxa can also form lichen-like associations with the algae of the lichen system when they are enforced to symbiosis by co-culturing assays.
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http://dx.doi.org/10.3390/life8020015DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6027233PMC
May 2018

Enforced fungal-algal symbioses in alginate spheres.

FEMS Microbiol Lett 2018 07;365(14)

Institut of Plant Sciences, University of Graz, Holteigasse 6, 8010 Graz, Austria.

The thallus structure of the lichen symbiosis provides a fungal shelter for the growth of algal partners. The long-living thallus also provides a habitat for other fungi, but experimental studies, which could inform us about the details of their interactions have hardly been conducted. We present a new approach by embedding axenically cultured strains of fungi together with algae in alginate spheres, which allows easy transfer of co-cultures on solid media. As the growth rates of the organisms are differentially triggered by the underlying medium, alginate embedding can help to adjust optimal parameters for stable culture of the combined symbionts. In our experiments, direct contacts between hyphae and algae and the formation of layered structures were observed in a fungus that is living as a commensal in the host lichen without visible symbiotic structures. The growth of primary lichen symbionts cannot be accelerated by alginate embedding so far, but our approach could artificially enforce symbiotic interactions that are not normally observed in nature.
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http://dx.doi.org/10.1093/femsle/fny115DOI Listing
July 2018

Photoautotrophic organisms control microbial abundance, diversity, and physiology in different types of biological soil crusts.

ISME J 2018 04 14;12(4):1032-1046. Epub 2018 Feb 14.

Max Planck Institute for Chemistry, Multiphase Chemistry, Mainz, Germany.

Biological soil crusts (biocrusts) cover about 12% of the Earth's land masses, thereby providing ecosystem services and affecting biogeochemical fluxes on a global scale. They comprise photoautotrophic cyanobacteria, algae, lichens and mosses, which grow together with heterotrophic microorganisms, forming a model system to study facilitative interactions and assembly principles in natural communities. Biocrusts can be classified into cyanobacteria-, lichen-, and bryophyte-dominated types, which reflect stages of ecological succession. In this study, we examined whether these categories include a shift in heterotrophic communities and whether this may be linked to altered physiological properties. We analyzed the microbial community composition by means of qPCR and high-throughput amplicon sequencing and utilized flux measurements to investigate their physiological properties. Our results revealed that once 16S and 18S rRNA gene copy numbers increase, fungi become more predominant and alpha diversity increases with progressing succession. Bacterial communities differed significantly between biocrust types with a shift from more generalized to specialized organisms along succession. CO gas exchange measurements revealed large respiration rates of late successional crusts being significantly higher than those of initial biocrusts, and different successional stages showed distinct NO and HONO emission patterns. Thus, our study suggests that the photoautotrophic organisms facilitate specific microbial communities, which themselves strongly influence the overall physiological properties of biocrusts and hence local to global nutrient cycles.
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http://dx.doi.org/10.1038/s41396-018-0062-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5864206PMC
April 2018

Chemical analysis of the Alphaproteobacterium strain MOLA1416 associated with the marine lichen Lichina pygmaea.

Phytochemistry 2018 Jan 5;145:57-67. Epub 2017 Nov 5.

UMR CNRS 6226, Institut des Sciences Chimiques de Rennes, Equipe CORINT "Chimie Organique et Interfaces", UFR Sciences Pharmaceutiques et Biologiques, Univ. Rennes 1, Université Bretagne Loire, 2 Avenue du Pr. Léon Bernard, F-35043, Rennes, France. Electronic address:

Alphaproteobacterium strain MOLA1416, related to Mycoplana ramosa DSM 7292 and Chelativorans intermedius CC-MHSW-5 (93.6% 16S rRNA sequence identity) was isolated from the marine lichen, Lichina pygmaea and its chemical composition was characterized by a metabolomic network analysis using LC-MS/MS data. Twenty-five putative different compounds were revealed using a dereplication workflow based on MS/MS signatures available through GNPS (https://gnps.ucsd.edu/). In total, ten chemical families were highlighted including isocoumarins, macrolactones, erythrinan alkaloids, prodiginines, isoflavones, cyclohexane-diones, sterols, diketopiperazines, amino-acids and most likely glucocorticoids. Among those compounds, two known metabolites (13 and 26) were isolated and structurally identified and metabolite 26 showed a high cytotoxic activity against B16 melanoma cell lines with an IC 0.6 ± 0.07 μg/mL.
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http://dx.doi.org/10.1016/j.phytochem.2017.10.005DOI Listing
January 2018

ITS1 metabarcoding highlights low specificity of lichen mycobiomes at a local scale.

Mol Ecol 2017 Sep 24;26(18):4811-4830. Epub 2017 Aug 24.

Department of Life Sciences, University of Trieste, Trieste, Italy.

As self-supporting and long-living symbiotic structures, lichens provide a habitat for many other organisms beside the traditionally considered lichen symbionts-the myco- and the photobionts. The lichen-inhabiting fungi either develop diagnostic phenotypes or occur asymptomatically. Because the degree of specificity towards the lichen host is poorly known, we studied the diversity of these fungi among neighbouring lichens on rocks in an alpine habitat. Using a sequencing metabarcoding approach, we show that lichen mycobiomes clearly reflect the overlap of multiple ecological sets of taxa, which differ in their trophic association with lichen thalli. The lack of specificity to the lichen mycobiome is further supported by the lack of community structure observed using clustering and ordination methods. The communities encountered across samples largely result from the subsampling of a shared species pool, in which we identify three major ecological components: (i) a generalist environmental pool, (ii) a lichenicolous/endolichenic pool and (iii) a pool of transient species. These taxa majorly belong to the fungal classes Dothideomycetes, Eurotiomycetes and Tremellomycetes with close relatives in adjacent ecological niches. We found no significant evidence that the phenotypically recognized lichenicolous fungi influence the occurrence of the other asymptomatic fungi in the host thalli. We claim that lichens work as suboptimal habitats or as a complex spore and mycelium bank, which modulate and allow the regeneration of local fungal communities. By performing an approach that minimizes ambiguities in the taxonomic assignments of fungi, we present how lichen mycobiomes are also suitable targets for improving bioinformatic analyses of fungal metabarcoding.
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http://dx.doi.org/10.1111/mec.14244DOI Listing
September 2017

Deciphering functional diversification within the lichen microbiota by meta-omics.

Microbiome 2017 07 19;5(1):82. Epub 2017 Jul 19.

Institute of Environmental Biotechnology, Graz University of Technology, Petersgasse 12, 8010, Graz, Austria.

Background: Recent evidence of specific bacterial communities extended the traditional concept of fungal-algal lichen symbioses by a further organismal kingdom. Although functional roles were already assigned to dominant members of the highly diversified microbiota, a substantial fraction of the ubiquitous colonizers remained unexplored. We employed a multi-omics approach to further characterize functional guilds in an unconventional model system.

Results: The general community structure of the lichen-associated microbiota was shown to be highly similar irrespective of the employed omics approach. Five highly abundant bacterial orders-Sphingomonadales, Rhodospirillales, Myxococcales, Chthoniobacterales, and Sphingobacteriales-harbor functions that are of substantial importance for the holobiome. Identified functions range from the provision of vitamins and cofactors to the degradation of phenolic compounds like phenylpropanoid, xylenols, and cresols.

Conclusions: Functions that facilitate the persistence of Lobaria pulmonaria under unfavorable conditions were present in previously overlooked fractions of the microbiota. So far, unrecognized groups like Chthoniobacterales (Verrucomicrobia) emerged as functional protectors in the lichen microbiome. By combining multi-omics and imaging techniques, we highlight previously overlooked participants in the complex microenvironment of the lichens.
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http://dx.doi.org/10.1186/s40168-017-0303-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5518139PMC
July 2017

Effects of Growth Media on the Diversity of Culturable Fungi from Lichens.

Molecules 2017 May 17;22(5). Epub 2017 May 17.

Institute of Plant Science, Karl-Franzens University of Graz, Holteigasse 6, 8010 Graz, Austria.

Microscopic and molecular studies suggest that lichen symbioses contain a plethora of associated fungi. These are potential producers of novel bioactive compounds, but strains isolated on standard media usually represent only a minor subset of these fungi. By using various in vitro growth conditions we are able to modulate and extend the fraction of culturable lichen-associated fungi. We observed that the presence of iron, glucose, magnesium and potassium in growth media is essential for the successful isolation of members from different taxonomic groups. According to sequence data, most isolates besides the lichen mycobionts belong to the classes Dothideomycetes and Eurotiomycetes. With our approach we can further explore the hidden fungal diversity in lichens to assist in the search of novel compounds.
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http://dx.doi.org/10.3390/molecules22050824DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6154544PMC
May 2017

Symbiotic Interplay of Fungi, Algae, and Bacteria within the Lung Lichen Lobaria pulmonaria L. Hoffm. as Assessed by State-of-the-Art Metaproteomics.

J Proteome Res 2017 06 4;16(6):2160-2173. Epub 2017 May 4.

Institute of Microbiology, Ernst-Moritz-Arndt-University Greifswald , DE-17487 Greifswald, Germany.

Lichens are recognized by macroscopic structures formed by a heterotrophic fungus, the mycobiont, which hosts internal autotrophic photosynthetic algal and/or cyanobacterial partners, referred to as the photobiont. We analyzed the structure and functionality of the entire lung lichen Lobaria pulmonaria L. Hoffm. collected from two different sites by state-of-the-art metaproteomics. In addition to the green algae and the ascomycetous fungus, a lichenicolous fungus as well as a complex prokaryotic community (different from the cyanobacteria) was found, the latter dominated by methanotrophic Rhizobiales. Various partner-specific proteins could be assigned to the different lichen symbionts, for example, fungal proteins involved in vesicle transport, algal proteins functioning in photosynthesis, cyanobacterial nitrogenase and GOGAT involved in nitrogen fixation, and bacterial enzymes responsible for methanol/C1-compound metabolism as well as CO-detoxification. Structural and functional information on proteins expressed by the lichen community complemented and extended our recent symbiosis model depicting the functional multiplayer network of single holobiont partners.1 Our new metaproteome analysis strongly supports the hypothesis (i) that interactions within the self-supporting association are multifaceted and (ii) that the strategy of functional diversification within the single lichen partners may support the longevity of L. pulmonaria under certain ecological conditions.
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http://dx.doi.org/10.1021/acs.jproteome.6b00974DOI Listing
June 2017

Differential sharing and distinct co-occurrence networks among spatially close bacterial microbiota of bark, mosses and lichens‬‬.

Mol Ecol 2017 May 13;26(10):2826-2838. Epub 2017 Mar 13.

Institute of Plant Sciences, University of Graz, Holteigasse 6, 8010, Graz, Austria.

Knowledge of bacterial community host-specificity has increased greatly in recent years. However, the intermicrobiome relationships of unrelated but spatially close organisms remain little understood. Trunks of trees covered by epiphytes represent complex habitats with a mosaic of ecological niches. In this context, we investigated the structure, diversity and interactions of microbiota associated with lichens, mosses and the bare tree bark. Comparative analysis revealed significant differences in the habitat-associated community structures. Corresponding co-occurrence analysis indicated that the lichen microbial network is less complex and less densely interconnected than the moss- and bark-associated networks. Several potential generalists and specialists were identified for the selected habitats. Generalists belonged mainly to Proteobacteria, with Sphingomonas as the most abundant genus. The generalists comprise microorganisms with generally beneficial features, such as nitrogen fixation or other supporting functions, according to a metagenomic analysis. We argue that beneficial strains shared among hosts contribute to ecological stability of the host biocoenoses.
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http://dx.doi.org/10.1111/mec.14070DOI Listing
May 2017

Lichenized Fungi and the Evolution of Symbiotic Organization.

Microbiol Spectr 2016 12;4(6)

Department of Botany, Swedish Museum of Natural History, 104 05 Stockholm, Sweden.

Lichen symbioses comprise a fascinating relationship between algae and fungi. The lichen symbiotic lifestyle evolved early in the evolution of ascomycetes and is also known from a few basidiomycetes. The ascomycete lineages have diversified in the lichenized stage to give rise to a tremendous variety of morphologies. Their thalli are often internally complex and stratified for optimized integration of algal and fungal metabolisms. Thalli are frequently colonized by specific nonlichenized fungi and occasionally also by other lichens. Microscopy has revealed various ways these fungi interact with their hosts. Besides the morphologically recognizable diversity of the lichen mycobionts and lichenicolous (lichen-inhabiting) fungi, many other microorganisms including other fungi and bacterial communities are now detected in lichens by culture-dependent and culture-independent approaches. The application of multi-omics approaches, refined microscopic techniques, and physiological studies has added to our knowledge of lichens, not only about the taxa involved in the lichen interactions, but also about their functions.
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http://dx.doi.org/10.1128/microbiolspec.FUNK-0011-2016DOI Listing
December 2016

Arthonia parietinaria - A common but frequently misunderstood lichenicolous fungus on species of the Xanthoria parietina-group.

Fungal Biol 2016 11;120(11):1341-1353

Institut für Pflanzenwissenschaften, NaWi Graz, Karl-Franzens-Universität, Holteigasse 6, 8010 Graz, Austria.

Arthonia parietinaria is described as new to science. Host of the type and at the same time the only confirmed host species is the foliose macrolichen Xanthoria parietina. Sequence data of nucLSU rRNA genes reveal a close relationship to Arthonia molendoi. A. parietinaria is recorded for many countries in Europe, western Asia, and northern Africa.
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http://dx.doi.org/10.1016/j.funbio.2016.06.009DOI Listing
November 2016

From Mouth to Model: Combining and Oral Biofilm Growth.

Front Microbiol 2016 21;7:1448. Epub 2016 Sep 21.

Institute of Plant Sciences, University of Graz Graz, Austria.

Oral biofilm studies based on simplified experimental setups are difficult to interpret. Models are limited mostly by the number of bacterial species observed and the insufficiency of artificial media. Few studies have attempted to overcome these limitations and to cultivate native oral biofilm. This study aimed to grow oral biofilm before transfer to a biofilm reactor for incubation. The survival of this oral biofilm and the changes in bacterial composition over time were observed. Six human enamel-dentin slabs embedded buccally in dental splints were used as biofilm carriers. Fitted individually to the upper jaw of 25 non-smoking male volunteers, the splints were worn continuously for 48 h. During this time, tooth-brushing and alcohol-consumption were not permitted. The biofilm was then transferred on slabs into a biofilm reactor and incubated there for 48 h while being nourished in BHI medium. Live/dead staining and confocal laser scanning microscopy were used to observe bacterial survival over four points in time: directly after removal (T0) and after 1 (T1), 24 (T2), and 48 h (T3) of incubation. Bacterial diversity at T0 and T3 was compared with 454-pyrosequencing. Fluorescence hybridization (FISH) was performed to show specific taxa. Survival curves were calculated with a specially designed MATLAB script. Acacia and QIIME 1.9.1 were used to process pyrosequencing data. SPSS 21.0 and R 3.3.1 were used for statistical analysis. After initial fluctuations at T1, survival curves mostly showed approximation of the bacterial numbers to the initial level at T3. Pyrosequencing analysis resulted in 117 OTUs common to all samples. The genera and (both ) dominated at T0 and T3. They make up two thirds of the biofilm. Genera with lower relative abundance had grown significantly at T3. FISH analysis confirmed the pyrosequencing results, i.e., the predominant staining of . We demonstrate the survival of native primary oral biofilm in its natural complexity over 48 h. Our results offer a baseline for cultivation studies of native oral biofilms in (phyto-) pharmacological and dental materials research. Further investigations and validation of culturing conditions could also facilitate the study of biofilm-induced diseases.
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http://dx.doi.org/10.3389/fmicb.2016.01448DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5030783PMC
September 2016
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