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Funk, Christiane
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Publications (10 of 95) Show all publications
Chen, Q., Arents, J., Schuurmans, J. M., Ganapathy, S., de Grip, W. J., Cheregi, O., . . . Hellingwerf, K. J. (2019). Combining retinal-based and chlorophyll-based (oxygenic) photosynthesis: Proteorhodopsin expression increases growth rate and fitness of a Delta PSI strain of Synechocystis sp. PCC6803. Metabolic engineering, 52, 68-76
Open this publication in new window or tab >>Combining retinal-based and chlorophyll-based (oxygenic) photosynthesis: Proteorhodopsin expression increases growth rate and fitness of a Delta PSI strain of Synechocystis sp. PCC6803
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2019 (English)In: Metabolic engineering, ISSN 1096-7176, E-ISSN 1096-7184, Vol. 52, p. 68-76Article in journal (Refereed) Published
Abstract [en]

To fill the "green absorption gap", a green absorbing proteorhodopsin was expressed in a PSI-deletion strain (Delta PSI) of Synechocystis sp. PCC6803. Growth-rate measurements, competition experiments and physiological characterization of the proteorhodopsin-expressing strains, relative to the Delta PSI control strain, allow us to conclude that proteorhodopsin can enhance the rate of photoheterotrophic growth of Delta PSI Synechocystis strain. The physiological characterization included measurement of the amount of residual glucose in the spent medium and analysis of oxygen uptake- and production rates. To explore the use of solar radiation beyond the PAR region, a red-shifted variant Proteorhodopsin-D212N/F234S was expressed in a retinal-deficient PSI-deletion strain (Delta PSI/Delta SynACO). Via exogenous addition of retinal analogue an infrared absorbing pigment (maximally at 740 nm) was reconstituted in vivo. However, upon illumination with 746 nm light, it did not significantly stimulate the growth (rate) of this mutant. The inability of the proteorhodopsin-expressing Delta PSI strain to grow photoautotrophically is most likely due to a kinetic rather than a thermodynamic limitation of its NADPH-dehydrogenase in NADP(+)-reduction.

Place, publisher, year, edition, pages
Elsevier, 2019
Keywords
Retinal-based proton pump, PSI-deletion, Synechocystis, Oxygen evolution, Glucose consumption, Growth stimulation
National Category
Biochemistry and Molecular Biology
Identifiers
urn:nbn:se:umu:diva-162503 (URN)10.1016/j.ymben.2018.11.002 (DOI)000457633200007 ()30447329 (PubMedID)
Available from: 2019-08-21 Created: 2019-08-21 Last updated: 2019-08-21Bibliographically approved
Huber, C. V., Jakobs, B. D., Mishra, L. S., Niedermaier, S., Stift, M., Winter, G., . . . Funck, D. (2019). DEG10 contributes to mitochondrial proteostasis, root growth, and seed yield in Arabidopsis. Journal of Experimental Botany, 70(19), 5423-5436
Open this publication in new window or tab >>DEG10 contributes to mitochondrial proteostasis, root growth, and seed yield in Arabidopsis
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2019 (English)In: Journal of Experimental Botany, ISSN 0022-0957, E-ISSN 1460-2431, Vol. 70, no 19, p. 5423-5436Article in journal (Refereed) Published
Abstract [en]

Maintaining mitochondrial proteome integrity is especially important under stress conditions to ensure a continued ATP supply for protection and adaptation responses in plants. Deg/HtrA proteases are important factors in the cellular protein quality control system, but little is known about their function in mitochondria. Here we analyzed the expression pattern and physiological function of Arabidopsis thaliana DEG10, which has homologs in all photosynthetic eukaryotes. Both expression of DEG10:GFP fusion proteins and immunoblotting after cell fractionation showed an unambiguous subcellular localization exclusively in mitochondria. DEG10 promoter:GUS fusion constructs showed that DEG10 is expressed in trichomes but also in the vascular tissue of roots and aboveground organs. DEG10 loss-of-function mutants were impaired in root elongation, especially at elevated temperature. Quantitative proteome analysis revealed concomitant changes in the abundance of mitochondrial respiratory chain components and assembly factors, which partially appeared to depend on altered mitochondrial retrograde signaling. Under field conditions, lack of DEG10 caused a decrease in seed production. Taken together, our findings demonstrate that DEG10 affects mitochondrial proteostasis, is required for optimal root development and seed set under challenging environmental conditions, and thus contributes to stress tolerance of plants.

Place, publisher, year, edition, pages
Oxford University Press, 2019
Keywords
Arabidopsis, Deg proteases, mitochondria, proteome, root, seed yield, temperature stress, G10, which has homologs in all photosynthetic eukaryotes. Both pression of DEG10:GFP fusion proteins and immunoblotting after cell actionation showed an unambiguous subcellular localization exclusively mitochondria. DEG10 promoter:GUS fusion constructs showed that DEG10 expressed in trichomes but also in the vascular tissue of roots and oveground organs. DEG10 loss-of-function mutants were impaired in root ongation, especially at elevated temperature. Quantitative proteome alysis revealed concomitant changes in the abundance of mitochondrial spiratory chain components and assembly factors, which partially peared to depend on altered mitochondrial retrograde signaling. Under eld conditions, lack of DEG10 caused a decrease in seed production. ken together, our findings demonstrate that DEG10 affects tochondrial proteostasis, is required for optimal root development and ed set under challenging environmental conditions, and thus ntributes to stress tolerance of plants.
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-164890 (URN)10.1093/jxb/erz294 (DOI)000491240900029 ()31225599 (PubMedID)
Funder
Swedish Energy Agency, 2012-005889
Available from: 2019-11-06 Created: 2019-11-06 Last updated: 2019-11-07Bibliographically approved
Ferro, L., Colombo, M., Posadas, E., Funk, C. & Muñoz, R. (2019). Elucidating the symbiotic interactions between a locally isolated microalga Chlorella vulgaris and its co-occurring bacterium Rhizobium sp. in synthetic municipal wastewater. Journal of Applied Phycology, 31(4), 2299-2310
Open this publication in new window or tab >>Elucidating the symbiotic interactions between a locally isolated microalga Chlorella vulgaris and its co-occurring bacterium Rhizobium sp. in synthetic municipal wastewater
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2019 (English)In: Journal of Applied Phycology, ISSN 0921-8971, E-ISSN 1573-5176, Vol. 31, no 4, p. 2299-2310Article in journal (Refereed) Published
Abstract [en]

Co-cultivation of microalgae and bacteria during municipal wastewater treatment can boost carbon and nutrient recovery as a result of their synergistic interactions. The symbiotic relationships between the locally isolated microalga Chlorella vulgaris and the bacterium Rhizobium sp., co-isolated from municipal wastewater, were investigated batchwise under photoautotrophic, heterotrophic, and mixotrophic conditions in a synthetic municipal wastewater medium. During photoautotrophic growth in BG11 medium, photosynthetic algal oxygenation and organic carbon production supported bacterial activity but no significant beneficial effects on microalgal growth were observed. In synthetic wastewater, a twofold higher biomass concentration was achieved in the axenic algal culture compared with the co-culture under heterotrophic conditions, suggesting a competition for nutrients. A comparable carbon removal was observed in all cultures (83–79% TOC), but a faster nitrogen consumption (59% TN) and complete phosphate assimilation (100% TP) was only achieved in the co-culture. A positive synergistic relationship was found under mixotrophic conditions, clearly supported by an in situ O2/CO2 exchange between the microorganisms. This mutualism led to a threefold higher biomass production with a 13-fold higher fatty acid content compared with the axenic algal culture, as well as a superior wastewater treatment performance (+ 58% TOC, + 41% TN and + 44% TP). The co-cultivation of C. vulgaris and Rhizobium is therefore suggested as a potential microbial consortium for a cost-efficient biomass generation during municipal wastewater reclamation, especially under mixotrophic conditions.

Place, publisher, year, edition, pages
Springer, 2019
Keywords
Chlorella vulgaris, Rhizobium, Symbiosis, Mixotrophy, Heterotrophy, Wastewater treatment
National Category
Microbiology Oceanography, Hydrology and Water Resources
Identifiers
urn:nbn:se:umu:diva-156463 (URN)10.1007/s10811-019-1741-1 (DOI)000479057200012 ()
Funder
Swedish Energy Agency, 476 38239-1Swedish Research Council Formas, 942-2015-92
Available from: 2019-02-15 Created: 2019-02-15 Last updated: 2019-08-30Bibliographically approved
Klemenčič, M. & Funk, C. (2019). Evolution and structural diversity of metacaspases. Journal of Experimental Botany, 70(7), 2039-2047
Open this publication in new window or tab >>Evolution and structural diversity of metacaspases
2019 (English)In: Journal of Experimental Botany, ISSN 0022-0957, E-ISSN 1460-2431, Vol. 70, no 7, p. 2039-2047Article, review/survey (Refereed) Published
Abstract [en]

Caspases are metazoan proteases, best known for their involvement in programmed cell death in animals. In higher plants genetically controlled mechanisms leading to the selective death of individual cells also involve the regulated interplay of various types of proteases. Some of these enzymes are structurally homologous to caspases and have therefore been termed metacaspases. In addition to the two well-studied metacaspase variants found in higher plants, type I and type II, biochemical data have recently become available for metacaspases of type III and metacaspase-like proteases, which are present only in certain algae. Although increasing in vitro and in vivo data suggest the existence of further sub-types, a lack of structural information hampers the interpretation of their distinct functional properties. However, the identification of key amino acid residues involved in the proteolytic mechanism of metacaspases, as well as the increased availability of plant genomic and transcriptomic data, is increasingly enabling in-depth analysis of all metacaspase types found in plastid-containing organisms. Here, we review the structural distribution and diversification of metacaspases and in doing so try to provide comprehensive guidelines for further analyses of this versatile family of proteases in organisms ranging from simple unicellular species to flowering plants.

Place, publisher, year, edition, pages
Oxford University Press, 2019
Keywords
Caspase, cystein protease, metacaspase, orthocaspase, plant protease, programmed cell death, proteolysis
National Category
Plant Biotechnology
Identifiers
urn:nbn:se:umu:diva-159630 (URN)10.1093/jxb/erz082 (DOI)000467901600006 ()30921456 (PubMedID)
Available from: 2019-06-13 Created: 2019-06-13 Last updated: 2019-06-13Bibliographically approved
Gomez, F. M., Carrion, C. A., Costa, M. L., Desel, C., Kieselbach, T., Funk, C., . . . Guiamet, J. (2019). Extra-plastidial degradation of chlorophyll and photosystem I in tobacco leaves involving 'senescence-associated vacuoles'. The Plant Journal, 99(3), 465-477
Open this publication in new window or tab >>Extra-plastidial degradation of chlorophyll and photosystem I in tobacco leaves involving 'senescence-associated vacuoles'
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2019 (English)In: The Plant Journal, ISSN 0960-7412, E-ISSN 1365-313X, Vol. 99, no 3, p. 465-477Article in journal (Refereed) Published
Abstract [en]

Chlorophyll (Chl) loss is the main visible symptom of senescence in leaves. The initial steps of Chl degradation operate within the chloroplast, but the observation that ‘senescence‐associated vacuoles’ (SAVs) contain Chl raises the question of whether SAVs might also contribute to Chl breakdown. Previous confocal microscope observations (Martínez et al., 2008) showed many SAVs containing Chl. Isolated SAVs contained Chl a and b (with a Chl a/b ratio close to 5) and lower levels of chlorophyllide a. Pheophytin a and pheophorbide a were formed after the incubation of SAVs at 30°C in darkness, suggesting the presence of Chl‐degrading activities in SAVs. Chl in SAVs was bound to a number of ‘green bands’. In the most abundant green band of SAVs, Western blot analysis showed the presence of photosystem I (PSI) Chl‐binding proteins, including the PsaA protein of the PSI reaction center and the apoproteins of the light‐harvesting complexes (Lhca 1–4). This was confirmed by: (i) measurements of 77‐K fluorescence emission spectra showing a single emission peak at around 730 nm in SAVs; (ii) mass spectrometry of the most prominent green band with the slowest electrophoretic mobility; and (iii) immunofluorescence detection of PsaA in SAVs observed through confocal microscopy. Incubation of SAVs at 30°C in darkness caused a steady decrease in PsaA levels. Overall, these results indicate that SAVs may be involved in the degradation of PSI proteins and their associated chlorophylls during the senescence of leaves.

Place, publisher, year, edition, pages
John Wiley & Sons, 2019
Keywords
senescence-associated vacuoles, photosystem I, chlorophyll degradation, tobacco, Nicotiana tabacum
National Category
Biochemistry and Molecular Biology
Identifiers
urn:nbn:se:umu:diva-162399 (URN)10.1111/tpj.14337 (DOI)000477680000007 ()30985038 (PubMedID)2-s2.0-85066909992 (Scopus ID)
Available from: 2019-08-19 Created: 2019-08-19 Last updated: 2019-08-19Bibliographically approved
Gomez, F. M., Carrion, C. A., Costa, M. L., Desel, C., Kieselbach, T., Funk, C., . . . Guiamet, J. (2019). Extra-plastidial degradation of chlorophyll and photosystem I in tobacco leaves involving 'senescence-associated vacuoles'. The Plant Journal, 99(3), 465-477
Open this publication in new window or tab >>Extra-plastidial degradation of chlorophyll and photosystem I in tobacco leaves involving 'senescence-associated vacuoles'
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2019 (English)In: The Plant Journal, ISSN 0960-7412, E-ISSN 1365-313X, Vol. 99, no 3, p. 465-477Article in journal (Refereed) Published
Abstract [en]

Chlorophyll (Chl) loss is the main visible symptom of senescence in leaves. The initial steps of Chl degradation operate within the chloroplast, but the observation that 'senescence-associated vacuoles' (SAVs) contain Chl raises the question of whether SAVs might also contribute to Chl breakdown. Previous confocal microscope observations (Martinez et al., 2008) showed many SAVs containing Chl. Isolated SAVs contained Chl a and b (with a Chl a/b ratio close to 5) and lower levels of chlorophyllide a. Pheophytin a and pheophorbide a were formed after the incubation of SAVs at 30 degrees C in darkness, suggesting the presence of Chl-degrading activities in SAVs. Chl in SAVs was bound to a number of 'green bands'. In the most abundant green band of SAVs, Western blot analysis showed the presence of photosystem I (PSI) Chl-binding proteins, including the PsaA protein of the PSI reaction center and the apoproteins of the light-harvesting complexes (Lhca 1-4). This was confirmed by: (i) measurements of 77-K fluorescence emission spectra showing a single emission peak at around 730 nm in SAVs; (ii) mass spectrometry of the most prominent green band with the slowest electrophoretic mobility; and (iii) immunofluorescence detection of PsaA in SAVs observed through confocal microscopy. Incubation of SAVs at 30 degrees C in darkness caused a steady decrease in PsaA levels. Overall, these results indicate that SAVs may be involved in the degradation of PSI proteins and their associated chlorophylls during the senescence of leaves.

Place, publisher, year, edition, pages
WILEY, 2019
Keywords
senescence-associated vacuoles, photosystem I, chlorophyll degradation, tobacco, Nicotiana tabacum
National Category
Plant Biotechnology
Identifiers
urn:nbn:se:umu:diva-162317 (URN)10.1111/tpj.14337 (DOI)000477680000007 ()30985038 (PubMedID)
Available from: 2019-09-03 Created: 2019-09-03 Last updated: 2019-09-03Bibliographically approved
Chen, Q., Arents, J., Schuurmans, J. M., Ganapathy, S., de Grip, W. J., Cheregi, O., . . . Hellingwerf, K. J. (2019). Functional Expression of Gloeobacter Rhodopsin in PSI-Less Synechocystis sp. PCC6803. Frontiers in Bioengineering and Biotechnology, 7, Article ID 67.
Open this publication in new window or tab >>Functional Expression of Gloeobacter Rhodopsin in PSI-Less Synechocystis sp. PCC6803
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2019 (English)In: Frontiers in Bioengineering and Biotechnology, E-ISSN 2296-4185, Vol. 7, article id 67Article in journal (Refereed) Published
Abstract [en]

The approach of providing an oxygenic photosynthetic organism with a cyclic electron transfer system, i.e., a far-red light-driven proton pump, is widely proposed to maximize photosynthetic efficiency via expanding the absorption spectrum of photosynthetically active radiation. As a first step in this approach, Gloeobacter rhodopsin was expressed in a PSI-deletion strain of Synechocystis sp. PCC6803. Functional expression of Gloeobacter rhodopsin, in contrast to Proteorhodopsin, did not stimulate the rate of photoheterotrophic growth of this Synechocystis strain, analyzed with growth rate measurements and competition experiments. Nevertheless, analysis of oxygen uptake and-production rates of the Gloeobacter rhodopsin-expressing strains, relative to the 1 PSI control strain, confirm that the proton-pumping Gloeobacter rhodopsin provides the cells with additional capacity to generate proton motive force. Significantly, expression of the Gloeobacter rhodopsin did modulate levels of pigment formation in the transgenic strain.

Place, publisher, year, edition, pages
Frontiers Media S.A., 2019
Keywords
retinal-based proton pump, PSI-deletion Synechocystis, growth stimulation, carotenoid metabolism, oxygen evolution
National Category
Biochemistry and Molecular Biology
Identifiers
urn:nbn:se:umu:diva-158747 (URN)10.3389/fbioe.2019.00067 (DOI)000463016900002 ()30984754 (PubMedID)
Available from: 2019-05-15 Created: 2019-05-15 Last updated: 2019-05-15Bibliographically approved
Karan, H., Funk, C., Grabert, M., Oey, M. & Hankamer, B. (2019). Green Bioplastics as Part of a Circular Bioeconomy. Trends in Plant Science, 24(3), 237-249
Open this publication in new window or tab >>Green Bioplastics as Part of a Circular Bioeconomy
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2019 (English)In: Trends in Plant Science, ISSN 1360-1385, E-ISSN 1878-4372, Vol. 24, no 3, p. 237-249Article, review/survey (Refereed) Published
Abstract [en]

The rapid accumulation of plastic waste is driving international demand for renewable plastics with superior qualities (e.g., full biodegradability to CO2 without harmful byproducts), as part of an expanding circular bioeconomy. Higher plants, microalgae, and cyanobacteria can drive solar-driven processes for the production of feedstocks that can be used to produce a wide variety of biodegradable plastics, as well as bioplastic-based infrastructure that can act as a long-term carbon sink. The plastic types produced, their chemical synthesis, scaled-up biorefinery concepts (e.g., plant-based methane-to-bioplastic production and co-product streams), bioplastic properties, and uses are summarized, together with the current regulatory framework and the key barriers and opportunities.

Place, publisher, year, edition, pages
Elsevier, 2019
Keywords
bioplastic, cyanobacteria, microalgae, photosynthesis, plants, plastic
National Category
Plant Biotechnology
Identifiers
urn:nbn:se:umu:diva-157578 (URN)10.1016/j.tplants.2018.11.010 (DOI)000459897200008 ()30612789 (PubMedID)
Available from: 2019-04-01 Created: 2019-04-01 Last updated: 2019-04-01Bibliographically approved
Lage, S., Kudahettige, N. P., Ferro, L., Matsakas, L., Funk, C., Rova, U. & Gentili, F. G. (2019). Microalgae Cultivation for the Biotransformation of Birch Wood Hydrolysate and Dairy Effluent. Catalysts, 9(2), Article ID 150.
Open this publication in new window or tab >>Microalgae Cultivation for the Biotransformation of Birch Wood Hydrolysate and Dairy Effluent
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2019 (English)In: Catalysts, E-ISSN 2073-4344, Vol. 9, no 2, article id 150Article in journal (Refereed) Published
Abstract [en]

In order to investigate environmentally sustainable sources of organic carbon and nutrients, four Nordic green microalgal strains, Chlorella sorokiniana, Chlorella saccharophila, Chlorella vulgaris, and Coelastrella sp., were grown on a wood (Silver birch, Betula pendula) hydrolysate and dairy effluent mixture. The biomass and lipid production were analysed under mixotrophic, as well as two-stage mixotrophic/heterotrophic regimes. Of all of the species, Coelastrella sp. produced the most total lipids per dry weight (~40%) in the mixture of birch hydrolysate and dairy effluent without requiring nutrient (nitrogen, phosphorus, and potassium—NPK) supplementation. Overall, in the absence of NPK, the two-stage mixotrophic/heterotrophic cultivation enhanced the lipid concentration, but reduced the amount of biomass. Culturing microalgae in integrated waste streams under mixotrophic growth regimes is a promising approach for sustainable biofuel production, especially in regions with large seasonal variation in daylight, like northern Sweden. To the best of our knowledge, this is the first report of using a mixture of wood hydrolysate and dairy effluent for the growth and lipid production of microalgae in the literature.

Place, publisher, year, edition, pages
MDPI, 2019
Keywords
mixotrophic, heterotrophic, lipids, fatty acid methyl esters, dairy wastewater, birch hydrolysate, green algae, Coelastrella, Chlorella
National Category
Bioenergy
Identifiers
urn:nbn:se:umu:diva-157784 (URN)10.3390/catal9020150 (DOI)000460702200044 ()2-s2.0-85062564536 (Scopus ID)
Projects
Bio4Energy
Available from: 2019-04-03 Created: 2019-04-03 Last updated: 2019-09-06Bibliographically approved
Gojkovic, Z., Lindberg, R., Tysklind, M. & Funk, C. (2019). Northern green algae have the capacity to remove active pharmaceutical ingredients. Ecotoxicology and Environmental Safety, 170, 644-656
Open this publication in new window or tab >>Northern green algae have the capacity to remove active pharmaceutical ingredients
2019 (English)In: Ecotoxicology and Environmental Safety, ISSN 0147-6513, E-ISSN 1090-2414, Vol. 170, p. 644-656Article in journal (Refereed) Published
Abstract [en]

Eight recently isolated microalgal species from Northern Sweden and the culture collection strain Scenedesmus obliquus RISE (UTEX 417) were tested for their ability to remove 19 pharmaceuticals from growth medium upon cultivation in short light path, flat panel photobioreactors. While the growth of one algal species, Chlorellasorokiniana B1-1, was completely inhibited by the addition of pharmaceuticals, and the one of Scenedesmus sp. B2-2 was strongly inhibited, the other algal strains grew well and produced biomass.

In general, lipophilic compounds were removed highly efficient from the culture medium by the microalgae (>70% in average within 2 days). The most lipophilic compounds Biperiden, Trihexyphenidyl, Clomipramine and Amitriptyline significantly accumulated in the biomass of most algal species, with a positive correlation between accumulation and their total biomass content. More persistent in the growth medium were hydrophilic compounds like Caffeine, Fluconazole, Trimetoprim, Codeine, Carbamazepin, Oxazepam and Tramadol, which were detected in amounts of above 60% in average after algal treatment.

While Coelastrella sp. 3–4 and Coelastrum astroideum RW10 were most efficient to accumulate certain compounds in their biomass, two algae species, Chlorella vulgaris13-1 and Chlorella saccharophila RNY, were not only highly efficient in removing all 19 pharmaceuticals from the growth medium within 12 days, at the same time only small amounts of these compounds accumulated in their biomass allowing its further use. Chlorella vulgaris 13-1 was able to remove most compounds within 6 days of growth, while Chlorella saccharophila RNY needed 8–10 days.”Wild” Nordic microalgae therefore are able to remove active pharmaceutical ingredients, equally or more efficient than the investigated culture collection strain, thereby demonstrating their possible use in sustainable wastewater reclamation in Nordic conditions.

Place, publisher, year, edition, pages
Elsevier, 2019
Keywords
Pharmaceuticals, Green microalgae, Photodegradation, Removal efficiency
National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-156578 (URN)10.1016/j.ecoenv.2018.12.032 (DOI)000456890700078 ()30579165 (PubMedID)
Funder
Swedish Energy Agency, 2013-006259Swedish Energy Agency, 38239-1Swedish Research Council Formas, 942-2015-92Swedish Research Council Formas, 213-2014-1504VINNOVA, 2017-03301
Available from: 2019-02-22 Created: 2019-02-22 Last updated: 2019-02-22Bibliographically approved
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