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Colonization of Land by Conjugating Green Algae

Colonization of Land by Conjugating Green Algae

Andreas Holzinger (ORCID: 0000-0002-7745-3978)
  • Grant DOI 10.55776/I1951
  • Funding program Principal Investigator Projects International
  • Status ended
  • Start January 1, 2015
  • End December 31, 2019
  • Funding amount € 211,838
  • Project website

Bilaterale Ausschreibung: Tschechien

Disciplines

Biology (100%)

Keywords

    Stress Tolerance, Metabolomics, Green Algae, Cell Wall, Ultrastructure, Plant Physiology

Abstract Final report

Conjugating green algae (Zygnematophyceae) are considered to be closest algal relatives to land plants (Embryophyta). Several members of this group typically grow in an aeroterrestrial environment that allowed colonization of land. In Polar or high Alpine regions, some filamentous Zygnematophyceae often dominate and typically produce relatively large amounts of biomass. Therefore, they are ideal model organisms for studying stress tolerance mechanisms connected with transition to land. The central goal of the project is to understand strategies that allowed plants to colonize land. It is known that Zygnematophyceae have the ability to form particularly tolerant permanent stages, akinetes, derived from vegetative cells. Within this project naturally occurring stress scenarios (desiccation, freezing, UV irradiation) will be simulated under simplified but monitorable laboratory conditions. Members of the genera Zygnema, Zygnemopis and Zyogonium will serve as research objects. The Czech project partners will characterize strains suitable for the key stress scenarios, using methods of multi gene phylogeny and perform desiccation and freezing stress experiments. The Austrian project partners will perform UV stress experiments and investigate the biochemical composition by a metabolomics approach. Moreover, cell walls will be investigated by immunological methods, with a particular focus on polymers known to act as plasticizers of the cell walls, which is important for desiccation tolerance. For the first time the spectral properties of Zygnematophyceae will be investigated at the subcellular level by hyperspectral imaging, a technique that allows to map the spectral properties in the range from 250 -950 nm. This will further contribute to our understanding of UV tolerance and integrate the biochemical with the structural findings. The complimentary expertise of the Czech and Austrian project partners will gain an added value resulting from the bilateral research project. The gained results will bring new insight into survival strategies of Zygnematophyceae and will be analyzed in an evolutionary and global change context.

The bilateral project investigated conjugating green algae (Zygnematophyceae) currently believed to be closest algal relatives to land plants (Embryophyta). These filamentous algae grow at aeroterrestrial environments that allowed colonization of land. Zygnema sp. and near relatives from polar and high Alpine habitats were investigated to study their phylogenetic variability, their stress tolerance to various naturally occurring stress scenarios (desiccation, freezing, UV irradiation). The variability of Zygnema sp. from Svalbard was studied after a joint expedition of the Austrian and the Czech research partners. 12 different arctic genotpyes could be described according to molecular and morphological data. Zygospores resulting from sexual reproduction were rare, but vegetative filaments formed permeant stages, termed akinetes. These akinetes were tested for their metabolite composition, and a shift in fatty acids could be found during this transition process. Particularly oleic and linoleic acid were enriched in the aktines, whereas metabolites related to primary metabolic processes were reduced. When subjected to desiccation stress, transcriptomic changes were described, where a much higher transcript regulation was observed in young cultures when compared to akinetes, suggestion that an acclimation process was responsible for this change. When exposed to experimental UV irradiation in a sun-simulation system, particularly the young cells showed a flexible reaction to this stress. While young cells could not recover from freezing down to - 8 C, akinetes tolerated freezing down to - 26 C and could recover their physiological activity afterwards. In a combined transcriptomic and metabolite profiling of Zygnema sp. field samples, it was found that the upper layers of a mat, exposed to the environmental factors had a much higher transcript regulation than the protected lower layers of a mat. Stress related metabolites were up-accumulated in the upper layer, enabling their survival under exposed conditions. The complementary expertise of the Austrian and the Czech research partners allowed to study many different aspects of Zygnematophycean cell physiology and structure. Taken together, our observations lead to the conclusion that Zygnematophyceae are well prepared to withstand harsh environmental conditions that allowed them to conquer land and ultimately gave rise to all land plants.

Research institution(s)
  • Universität Innsbruck - 100%
International project participants
  • David Rysanek, Charles University Prague - Czechia
  • Martina Pichrtová, Charles University Prague - Czechia
  • Yvonne Nemcova, Charles University Prague - Czechia
  • Dimitri Deheyn, University of California San Diego - USA

Research Output

  • 1585 Citations
  • 56 Publications
  • 8 Disseminations
  • 7 Scientific Awards
  • 2 Fundings
Publications
  • 2021
    Title Thorsmoerkia curvula gen. et spec. nov. (Trebouxiophyceae, Chlorophyta), a semi-terrestrial microalga from Iceland exhibits high levels of unsaturated fatty acids
    DOI 10.1007/s10811-021-02577-y
    Type Journal Article
    Author Nicoletti C
    Journal Journal of Applied Phycology
    Pages 3671-3682
    Link Publication
  • 2021
    Title Characterization of Two Zygnema Strains (Zygnema circumcarinatum SAG 698-1a and SAG 698-1b) and a Rapid Method to Estimate Nuclear Genome Size of Zygnematophycean Green Algae
    DOI 10.3389/fpls.2021.610381
    Type Journal Article
    Author Feng X
    Journal Frontiers in Plant Science
    Pages 610381
    Link Publication
  • 2021
    Title Ecophysiological, morphological, and biochemical traits of free-living Diplosphaera chodatii (Trebouxiophyceae) reveal adaptation to harsh environmental conditions
    DOI 10.1007/s00709-021-01620-6
    Type Journal Article
    Author Medwed C
    Journal Protoplasma
    Pages 1187-1199
    Link Publication
  • 2021
    Title Terrestrial Green Algae Show Higher Tolerance to Dehydration than Do Their Aquatic Sister-Species
    DOI 10.1007/s00248-020-01679-3
    Type Journal Article
    Author Terlova E
    Journal Microbial Ecology
    Pages 770-782
    Link Publication
  • 2021
    Title Cell wall characteristics during sexual reproduction of Mougeotia sp. (Zygnematophyceae) revealed by electron microscopy, glycan microarrays and RAMAN spectroscopy
    DOI 10.1007/s00709-021-01659-5
    Type Journal Article
    Author Permann C
    Journal Protoplasma
    Pages 1261-1275
    Link Publication
  • 2022
    Title Timaviella dunensis sp. nov. from sand dunes of the Baltic Sea, Germany, and emendation of Timaviella edaphica (Elenkin) O.M. Vynogr. & Mikhailyuk (Synechococcales, Cyanobacteria) based on an integrative approach.
    DOI 10.11646/phytotaxa.532.3.1
    Type Journal Article
    Author Mikhailyuk T
    Journal Phytotaxa
    Pages 192-208
    Link Publication
  • 2018
    Title Ecology, cytology and phylogeny of the snow alga Scotiella cryophila K-1 (Chlamydomonadales, Chlorophyta) from the Austrian Alps
    DOI 10.2216/18-45.1
    Type Journal Article
    Author Remias D
    Journal Phycologia
    Pages 581-592
    Link Publication
  • 2018
    Title Molecular and morphological diversity of Zygnema and Zygnemopsis (Zygnematophyceae, Streptophyta) from Svalbard (High Arctic)
    DOI 10.1080/09670262.2018.1476920
    Type Journal Article
    Author Pichrtová M
    Journal European Journal of Phycology
    Pages 492-508
    Link Publication
  • 2018
    Title New Taxa of Streptophyte Algae (Streptophyta) from Terrestrial Habitats Revealed Using an Integrative Approach
    DOI 10.1016/j.protis.2018.03.002
    Type Journal Article
    Author Mikhailyuk T
    Journal Protist
    Pages 406-431
    Link Publication
  • 2018
    Title Localisation and substrate specificities of transglycanases in charophyte algae relate to development and morphology
    DOI 10.1242/jcs.203208
    Type Journal Article
    Author Herburger K
    Journal Journal of Cell Science
    Link Publication
  • 2018
    Title Ecophysiological and morphological comparison of two populations of Chlainomonas sp. (Chlorophyta) causing red snow on ice-covered lakes in the High Tatras and Austrian Alps
    DOI 10.1080/09670262.2018.1426789
    Type Journal Article
    Author Procházková L
    Journal European Journal of Phycology
    Pages 230-243
    Link Publication
  • 2018
    Title Light and Dehydration but Not Temperature Drive Photosynthetic Adaptations of Basal Streptophytes (Hormidiella, Streptosarcina and Streptofilum) Living in Terrestrial Habitats
    DOI 10.1007/s00248-018-1225-x
    Type Journal Article
    Author Pierangelini M
    Journal Microbial Ecology
    Pages 380-393
    Link Publication
  • 2021
    Title The red alga Tsunamia transpacifica (Stylonematophyceae) from plastic drift shows adaptation to its uncommon habitat in ultrastructure and soluble low molecular weight carbohydrate composition
    DOI 10.1007/s00709-021-01674-6
    Type Journal Article
    Author Holzinger A
    Journal Protoplasma
    Pages 1307-1321
    Link Publication
  • 2020
    Title Desiccation tolerance in streptophyte algae and the algae to land plant transition: evolution of LEA and MIP protein families within the Viridiplantae
    DOI 10.1093/jxb/eraa105
    Type Journal Article
    Author Becker B
    Journal Journal of Experimental Botany
    Pages 3270-3278
    Link Publication
  • 2020
    Title Ecophysiological changes and spore formation: two strategies in response to low-temperature and high-light stress in Klebsormidium cf. flaccidum (Klebsormidiophyceae, Streptophyta)1
    DOI 10.1111/jpy.12971
    Type Journal Article
    Author Míguez F
    Journal Journal of Phycology
    Pages 649-661
    Link Publication
  • 2018
    Title Arctic, Antarctic, and temperate green algae Zygnema spp. under UV-B stress: vegetative cells perform better than pre-akinetes
    DOI 10.1007/s00709-018-1225-1
    Type Journal Article
    Author Holzinger A
    Journal Protoplasma
    Pages 1239-1252
    Link Publication
  • 2017
    Title The terrestrial green macroalga Prasiola calophylla (Trebouxiophyceae, Chlorophyta): ecophysiological performance under water-limiting conditions
    DOI 10.1007/s00709-016-1068-6
    Type Journal Article
    Author Holzinger A
    Journal Protoplasma
    Pages 1755-1767
    Link Publication
  • 2020
    Title Klebsormidin A and B, Two New UV-Sunscreen Compounds in Green Microalgal Interfilum and Klebsormidium Species (Streptophyta) From Terrestrial Habitats
    DOI 10.3389/fmicb.2020.00499
    Type Journal Article
    Author Hartmann A
    Journal Frontiers in Microbiology
    Pages 499
    Link Publication
  • 2019
    Title The conjugating green alga Zygnema sp. (Zygnematophyceae) from the Arctic shows high frost tolerance in mature cells (pre-akinetes)
    DOI 10.1007/s00709-019-01404-z
    Type Journal Article
    Author Trumhová K
    Journal Protoplasma
    Pages 1681-1694
    Link Publication
  • 2019
    Title Metatranscriptomic and metabolite profiling reveals vertical heterogeneity within a Zygnema green algal mat from Svalbard (High Arctic)
    DOI 10.1111/1462-2920.14788
    Type Journal Article
    Author Rippin M
    Journal Environmental Microbiology
    Pages 4283-4299
    Link Publication
  • 2016
    Title Influence of substrate and pH on the diversity of the aeroterrestrial alga Klebsormidium (Klebsormidiales, Streptophyta): a potentially important factor for sympatric speciation
    DOI 10.2216/15-110.1
    Type Journal Article
    Author Ryšánek D
    Journal Phycologia
    Pages 347-358
    Link Publication
  • 2016
    Title Hyperspectral imaging of snow algae and green algae from aeroterrestrial habitats
    DOI 10.1016/j.jphotobiol.2016.07.001
    Type Journal Article
    Author Holzinger A
    Journal Journal of Photochemistry and Photobiology B: Biology
    Pages 412-420
    Link Publication
  • 2016
    Title Abiotic Stress Tolerance of Charophyte Green Algae: New Challenges for Omics Techniques
    DOI 10.3389/fpls.2016.00678
    Type Journal Article
    Author Holzinger A
    Journal Frontiers in Plant Science
    Pages 678
    Link Publication
  • 2016
    Title The green alga Zygogonium ericetorum (Zygnematophyceae, Charophyta) shows high iron and aluminium tolerance: protection mechanisms and photosynthetic performance
    DOI 10.1093/femsec/fiw103
    Type Journal Article
    Author Herburger K
    Journal FEMS Microbiology Ecology
    Link Publication
  • 2016
    Title Photosynthetic Strategies of Desiccation-Tolerant Organisms; In: Handbook of Photosynthesis, Third Edition
    DOI 10.1201/b19498-49
    Type Book Chapter
    Publisher CRC Press
  • 2016
    Title Formation of lipid bodies and changes in fatty acid composition upon pre-akinete formation in Arctic and Antarctic Zygnema (Zygnematophyceae, Streptophyta) strains
    DOI 10.1093/femsec/fiw096
    Type Journal Article
    Author Pichrtová M
    Journal FEMS Microbiology Ecology
    Link Publication
  • 2016
    Title A new microscopic method to analyse desiccation-induced volume changes in aeroterrestrial green algae
    DOI 10.1111/jmi.12409
    Type Journal Article
    Author Lajos K
    Journal Journal of Microscopy
    Pages 192-199
    Link Publication
  • 2015
    Title Entransia and Hormidiella, sister lineages of Klebsormidium (Streptophyta), respond differently to light, temperature, and desiccation stress
    DOI 10.1007/s00709-015-0889-z
    Type Journal Article
    Author Herburger K
    Journal Protoplasma
    Pages 1309-1323
    Link Publication
  • 2017
    Title F-actin reorganization upon de- and rehydration in the aeroterrestrial green alga Klebsormidium crenulatum
    DOI 10.1016/j.micron.2017.03.012
    Type Journal Article
    Author Blaas K
    Journal Micron
    Pages 34-38
    Link Publication
  • 2016
    Title Ecophysiology, secondary pigments and ultrastructure of Chlainomonas sp. (Chlorophyta) from the European Alps compared with Chlamydomonas nivalis forming red snow
    DOI 10.1093/femsec/fiw030
    Type Journal Article
    Author Remias D
    Journal FEMS Microbiology Ecology
    Link Publication
  • 2015
    Title Desiccation tolerance in the streptophyte green alga Klebsormidium: The role of phytohormones
    DOI 10.1080/19420889.2015.1059978
    Type Journal Article
    Author Holzinger A
    Journal Communicative & Integrative Biology
    Link Publication
  • 2015
    Title Conjugation morphology of Zygogonium ericetorum (Zygnematophyceae, Charophyta) from a high alpine habitat
    DOI 10.1111/jpy.12363
    Type Journal Article
    Author Stancheva R
    Journal Journal of Phycology
    Pages 131-134
    Link Publication
  • 2015
    Title Localization and Quantification of Callose in the Streptophyte Green Algae Zygnema and Klebsormidium: Correlation with Desiccation Tolerance
    DOI 10.1093/pcp/pcv139
    Type Journal Article
    Author Herburger K
    Journal Plant and Cell Physiology
    Pages 2259-2270
    Link Publication
  • 2015
    Title Biodiversity of Klebsormidium (Streptophyta) from alpine biological soil crusts (Alps, Tyrol, Austria, and Italy)
    DOI 10.1111/jpy.12316
    Type Journal Article
    Author Mikhailyuk T
    Journal Journal of Phycology
    Pages 750-767
    Link Publication
  • 2015
    Title Desiccation tolerance in the chlorophyte green alga Ulva compressa: does cell wall architecture contribute to ecological success?
    DOI 10.1007/s00425-015-2292-6
    Type Journal Article
    Author Holzinger A
    Journal Planta
    Pages 477-492
    Link Publication
  • 2017
    Title Epilithic Chamaesiphon (Synechococcales, Cyanobacteria) species in mountain streams of the Alps—interspecific differences in photo-physiological traits
    DOI 10.1007/s10811-017-1328-7
    Type Journal Article
    Author Aigner S
    Journal Journal of Applied Phycology
    Pages 1125-1134
    Link Publication
  • 2017
    Title New species of Oculatella (Synechococcales, Cyanobacteria) from terrestrial habitats of Ukraine
    DOI 10.15407/ukrbotj74.06.509
    Type Journal Article
    Author Vinogradova O
    Journal Ukrainian Botanical Journal
    Pages 509-520
    Link Publication
  • 2017
    Title Terrestrial adaptation of green algae Klebsormidium and Zygnema (Charophyta) involves diversity in photosynthetic traits but not in CO2 acquisition
    DOI 10.1007/s00425-017-2741-5
    Type Journal Article
    Author Pierangelini M
    Journal Planta
    Pages 971-986
    Link Publication
  • 2017
    Title Enhanced Desiccation Tolerance in Mature Cultures of the Streptophytic Green Alga Zygnema circumcarinatum Revealed by Transcriptomics
    DOI 10.1093/pcp/pcx136
    Type Journal Article
    Author Rippin M
    Journal Plant and Cell Physiology
    Pages 2067-2084
    Link Publication
  • 2017
    Title Single colony genetic analysis of epilithic stream algae of the genus Chamaesiphon spp.
    DOI 10.1007/s10750-017-3295-z
    Type Journal Article
    Author Kurmayer R
    Journal Hydrobiologia
    Pages 61-75
    Link Publication
  • 2017
    Title The freshwater red alga Batrachospermum turfosum (Florideophyceae) can acclimate to a wide range of light and temperature conditions
    DOI 10.1080/09670262.2016.1274430
    Type Journal Article
    Author Aigner S
    Journal European Journal of Phycology
    Pages 238-249
    Link Publication
  • 2017
    Title Photosynthetic plasticity in the green algal species Klebsormidium flaccidum (Streptophyta) from a terrestrial and a freshwater habitat
    DOI 10.2216/16-85.1
    Type Journal Article
    Author Karsten U
    Journal Phycologia
    Pages 213-220
    Link Publication
  • 2019
    Title Arabinogalactan Proteins and the Extracellular Matrix of Charophytes: A Sticky Business
    DOI 10.3389/fpls.2019.00447
    Type Journal Article
    Author Palacio-López K
    Journal Frontiers in Plant Science
    Pages 447
    Link Publication
  • 2019
    Title Homogalacturonan Accumulation in Cell Walls of the Green Alga Zygnema sp. (Charophyta) Increases Desiccation Resistance
    DOI 10.3389/fpls.2019.00540
    Type Journal Article
    Author Herburger K
    Journal Frontiers in Plant Science
    Pages 540
    Link Publication
  • 2019
    Title New record of the rare genus Crinalium Crow (Oscillatoriales, Cyanobacteria) from sand dunes of the Baltic Sea, Germany: epitypification and emendation of Crinalium magnum Fritsch et John based on an integrative approach
    DOI 10.11646/phytotaxa.400.3.4
    Type Journal Article
    Author Mikhailyuk T
    Journal Phytotaxa
    Pages 165-179
    Link Publication
  • 2015
    Title Living in biological soil crust communities of African deserts—Physiological traits of green algal Klebsormidium species (Streptophyta) to cope with desiccation, light and temperature gradients
    DOI 10.1016/j.jplph.2015.09.002
    Type Journal Article
    Author Karsten U
    Journal Journal of Plant Physiology
    Pages 2-12
    Link Publication
  • 2014
    Title Photosynthetic efficiency, desiccation tolerance and ultrastructure in two phylogenetically distinct strains of alpine Zygnema sp. (Zygnematophyceae, Streptophyta): role of pre-akinete formation
    DOI 10.1007/s00709-014-0703-3
    Type Journal Article
    Author Herburger K
    Journal Protoplasma
    Pages 571-589
    Link Publication
  • 2017
    Title Localisation and substrate specificities of transglycanases in charophyte algae relate to development and morphology
    DOI 10.13025/27591
    Type Journal Article
    Author Herburger K
    Link Publication
  • 2015
    Title Prasiolin, a new UV-sunscreen compound in the terrestrial green macroalga Prasiola calophylla (Carmichael ex Greville) Kützing (Trebouxiophyceae, Chlorophyta)
    DOI 10.1007/s00425-015-2396-z
    Type Journal Article
    Author Hartmann A
    Journal Planta
    Pages 161-169
    Link Publication
  • 2020
    Title Dictyosphaerium-like morphotype in terrestrial algae: what is Xerochlorella (Trebouxiophyceae, Chlorophyta)?1
    DOI 10.1111/jpy.12974
    Type Journal Article
    Author Mikhailyuk T
    Journal Journal of Phycology
    Pages 671-686
    Link Publication
  • 2020
    Title Pre-akinete formation in Zygnema sp. from polar habitats is associated with metabolite re-arrangement
    DOI 10.1093/jxb/eraa123
    Type Journal Article
    Author Arc E
    Journal Journal of Experimental Botany
    Pages 3314-3322
    Link Publication
  • 2020
    Title Abundance and Extracellular Release of Phytohormones in Aero-terrestrial Microalgae (Trebouxiophyceae, Chlorophyta) As a Potential Chemical Signaling Source1
    DOI 10.1111/jpy.13032
    Type Journal Article
    Author Pichler G
    Journal Journal of Phycology
    Pages 1295-1307
    Link Publication
  • 2020
    Title Phytohormone release by three isolated lichen mycobionts and the effects of indole-3-acetic acid on their compatible photobionts
    DOI 10.1007/s13199-020-00721-9
    Type Journal Article
    Author Pichler G
    Journal Symbiosis
    Pages 95-108
    Link Publication
  • 2020
    Title Adaptation to Aquatic and Terrestrial Environments in Chlorella vulgaris (Chlorophyta)
    DOI 10.3389/fmicb.2020.585836
    Type Journal Article
    Author Aigner S
    Journal Frontiers in Microbiology
    Pages 585836
    Link Publication
  • 2020
    Title Cell Wall Reinforcements Accompany Chilling and Freezing Stress in the Streptophyte Green Alga Klebsormidium crenulatum
    DOI 10.3389/fpls.2020.00873
    Type Journal Article
    Author Steiner P
    Journal Frontiers in Plant Science
    Pages 873
    Link Publication
  • 2016
    Title Aniline blue and Calcofluor white staining of callose and cellulose in the streptophyte green algae Zygnema and Klebsormidium.
    DOI 10.21769/bioprotoc.1969
    Type Journal Article
    Author Herburger K
    Journal Bio-protocol
    Link Publication
Disseminations
  • 2017
    Title Newspaper contribution
    Type A magazine, newsletter or online publication
  • 2018 Link
    Title Youtube VIDEO
    Type A broadcast e.g. TV/radio/film/podcast (other than news/press)
    Link Link
  • 2015 Link
    Title Media contribution
    Type A magazine, newsletter or online publication
    Link Link
  • 2019 Link
    Title Media contribution
    Type A magazine, newsletter or online publication
    Link Link
  • 2017 Link
    Title Media Contribution
    Type A magazine, newsletter or online publication
    Link Link
  • 2016
    Title Newsletter of the Phycological Section of the German Botanical Society
    Type A magazine, newsletter or online publication
  • 2018 Link
    Title Media contribution
    Type A magazine, newsletter or online publication
    Link Link
  • 2018 Link
    Title Alga of the year 2018
    Type A press release, press conference or response to a media enquiry/interview
    Link Link
Scientific Awards
  • 2019
    Title European Phycological Congress (EPC 7)
    Type Personally asked as a key note speaker to a conference
    Level of Recognition Continental/International
  • 2019
    Title Journal of Experimental Botany - Special issue
    Type Appointed as the editor/advisor to a journal or book series
    Level of Recognition Continental/International
  • 2019
    Title Visiting Researcher (PostDoc)
    Type Attracted visiting staff or user to your research group
    Level of Recognition Continental/International
  • 2018
    Title Visiting Researcher (PostDoc)
    Type Attracted visiting staff or user to your research group
    Level of Recognition Continental/International
  • 2017
    Title Guest Professor Ulf Karsten, University of Rostock
    Type Attracted visiting staff or user to your research group
    Level of Recognition Continental/International
  • 2017
    Title OeAD-GsmbH (Österreichische Austauschdienst) - Austrian Agency for International Cooperation in Education and Research
    Type Attracted visiting staff or user to your research group
    Level of Recognition Continental/International
  • 2016
    Title 57th Meeting of the Czech Phycological Society
    Type Personally asked as a key note speaker to a conference
    Level of Recognition Continental/International
Fundings
  • 2018
    Title Fulbright Visiting Scholar Program
    Type Fellowship
    Start of Funding 2018
    Funder US-UK Fulbright Commission
  • 2017
    Title Metabolomics and Biodiversity of Snow and Ice Phototrophs
    Type Other
    Start of Funding 2017
    Funder Austrian Science Fund (FWF)

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