Studies on domestication of two species of wild edible mushroom from BrazilAbstract
There are about 80 species of wild edible mushroom that certainly occur in Brazil and can be used as a natural source of food and medicine. This study aimed to evaluate the in vitro mycelial development in culture media at different temperatures and substrates for cultivation of the edible mushroom species Auricularia fuscosuccinea and Laetiporus gilbertsonii. Additionally, the cultivation and the nutritional composition of A. fuscosuccinea mushrooms were evaluated. The two best wild strains of each species were selected for the in vitro cultivation experiment in two different substrates. Furthermore, an axenic cultivation on sawdust was conduct and the basidiomata produced were evaluated on their nutritional composition. The temperatures that best favored the mycelial growth were 30 °C for A. fuscosuccinea and 25 °C and 30 °C for L. gilbertsonii. The mycelium of both species developed better in the sterile Eucalyptus sawdust substrate. Despite the success in cultivating the mycelium of L. gilbertsonii, it was not possible to obtain basidioma for this species. On the other hand, it was possible to produce basidiomata of the two tested wild strains of A. fuscosuccinea.
Key words
Atlantic Rainforest; Auricularia fuscosuccinea; Laetiporus gilbertsonii; mushroom cultivation; nutritional content
INTRODUCTION
Wild edible mushrooms are an important natural source of food, medicine, and income for communities in more than 90 countries (Li et al. 2021). There are about 2,000 species of wild edible mushrooms worldwide (Li et al. 2021), but only approximately 130 have been domesticated (Thawthong et al. 2014). Despite the diversity of edible species, five genera [Lentinula Earle, Pleurotus (Fr.) P. Kumm., Auricularia Bull., Agaricus L., and Flammulina P. Karst.] constitute about 85 % of the world production of edible mushrooms (Royse et al. 2017). Albertó (2017) summarized the steps for domestication of naturally occurring species in 14 points, from the strain isolation to the nutritional composition. Considering that all these steps are complex, a good starting point is to determine if the wild species to be domesticated can be cultivated using the techniques common for commercial species (Albertó 2017). Among the almost 80 species of wild edible mushroom that certainly occur in Brazil (Drewinski 2023), we focus this work to test few steps for the domestication of Brazilian wild strains of the edible mushrooms Auricularia fuscosuccinea (Mont.) Henn. and Laetiporus gilbertsonii Burds.
Auricularia fuscosuccinea (Basidiomycota: Auriculariaceae) was originally described from Cuba and occurs in tropical and subtropical regions of the Americas (Wu et al. 2021). Fidalgo & Hirata (1979) reported the use of this species as food by Txicão and Txucarramãe indigenous people from the Xingu National Park in Brazil. Additionally, the use of A. fuscosuccinea as food has been recorded by other communities in the Americas (Gamboa-Trujillo et al. 2019, Ruán-Soto et al. 2021). Auricularia fuscosuccinea is easily found both in forests and in urban areas, and it has already been recorded for 13 of the 26 Brazilian states: Acre, Amazonas, Mato Grosso, Goiás, Pará, Paraíba, Pernambuco, Paraná, Rio de Janeiro, Rondônia, Rio Grande do Sul, Santa Catarina, and São Paulo (Alvarenga et al. 2015, Drewinski 2023).
Laetiporus gilbertsonii (Basidiomycota: Laetiporaceae) was described based on collections from the Pacific coast of the United States of America (Burdsall Jr & Banik 2001) and has a wide distribution in the Americas, occurring from temperate to tropical and subtropical zones (Lindner & Banik 2008, Banik et al. 2012, Pires et al. 2016, Campi et al. 2022). Recently, Campi et al. (2022) studied the occurrence of the genus Laetiporus in South America and concluded that L. gilbertsonii is the correct name for the species growing in Southern South America (Campi et al. 2022). In Brazil, the species has been reported for the Southeastern region, in the states of São Paulo (Pires et al. 2016) and Espírito Santo (Drewinski 2023). The species is associated with brown rot mainly of Eucalyptus spp. and Quercus spp., occurring in both living trees and dead trunks and logs (Burdsall Jr & Banik 2001). As well as for another species of the genus, Laetiporus sulphureus (Bull.) Murrill, the species L. gilbertsonii is also known as “chicken of the woods” and present a pronounced flavor, excellent texture and is highly appreciated in gastronomy, although there are no studies on its cultivation. Tropical regions have a great potential to be a rich source of cultivatable fungal species (Thawthong et al. 2014), and Brazil is a good country for this kind of investigations.
MATERIALS AND METHODS
Sampling
Collections were carried out in the Atlantic Rainforest domain, in the Brazilian states of Espírito Santo, Paraná, Rio de Janeiro, and São Paulo (Table I). From the fresh wild basidiomata, a pure mycelium culture was obtained through the inoculation of fragments of the pileus context into Petri dishes containing sterile PDA (Potato Dextrose Agar) medium. The dried vouchers are deposited at the herbarium SP (at the ‘Instituto de Pesquisas Ambientais’) and at the fungarium FIFUNGI (IFungiLab, at the ‘Instituto Federal de Educação, Ciência e Tecnologia de São Paulo’), and the live cultures are at the ‘Coleção de Culturas de Algas, Fungos e Cianobactérias – CCIBt’ (at the ‘Instituto de Pesquisas Ambientais’). This study is according to the Brazilian legislation on access to biodiversity and is registered in the ‘Sistema Nacional de Gestão do Patrimônio Genético e do Conhecimento Tradicional Associado’ (SisGen # A4A9200).
Data on the Brazilian wild strains of Auricularia fuscosuccinea and Laetiporus gilbertsonii evaluated in this research.
Species identity
The identification of the collected specimens was made through morphological and molecular characteristics, following specific bibliographies (Lowy 1952, Burdsall Jr. & Banik 2001, Looney et al. 2013, Pires et al. 2016, Wu et al. 2021). For molecular studies, DNA extraction was performed from mycelium obtained in liquid culture following a modified CTAB extraction method. The intergenic ribosomal region (nrITS1-5.8S-ITS2) was amplified by polymerase chain reactions (PCR) with the primers ITS1-F and ITS4 (White et al. 1990). The amplified products were purified with QIAquick PCR Purification Kit and sequenced at MacroGen (South Korea) using the same primer pair. The generated sequences were manually checked and edited with Geneious v.8.1 (Kearse et al. 2012). We used the Basic Local Alignment Search Tool (BLAST) to find similar sequences to build the matrices. Sequences were aligned using MAFFT online (Katoh et al. 2019) and were manually optimized using AliView (Larsson 2014). The ITS region was partitioned into ITS1, 5.8S and ITS2, and the evolution model was estimated for each partition using the BIC (Bayesian Information Criterion) criterion in jModelTest v.2.0 (Darriba et al. 2012). The Bayesian inference (BI) analysis was performed with Mr.Bayes v3.2.7a (Ronquist et al. 2012), with two independent runs, four simultaneous independent chains and 20,000,000 generations with a sample frequency every 1,000 generation. The phylogenetic trees are available as Supplementary Material (Figures S1 and S2).
Mycelial growth and dry mycelial biomass at different temperatures
Twelve wild strains of A. fuscosuccinea and three of L. gilbertsonii were evaluated for mycelial growth and dry biomass production in PDA culture medium at different temperatures. After the preparation and solidification of the culture medium (30 mL) in Petri dishes (90 mm diam), a 9.6 mm fragment of the pure culture matrix was inoculated in the center of the plate for each wild strain. The plates were incubated at temperatures of 20 °C, 25 °C, 30 °C and 35 °C in a BOD (Bio-Oxygen Demand) incubator (Vargas-Isla & Ishikawa 2008). The experiment was carried out in 15 replicates per temperature per strain. The diameter of the mycelial growth was measured on the day that one of the replicates of each evaluated wild strain completed the growth on the plate. To evaluate the dry mycelial biomass, the plates were placed in the microwave and heated for 20 seconds to melt the culture medium, then the mycelium was filtered and washed with distilled water and the biomass was dehydrated until constant weight (Vargas-Isla & Ishikawa 2008).
Mycelial development on different substrates
From the results of the mycelial biomass and growth tests at different temperatures, two wild strains of each species were selected for the experiment of mycelial development on two substrates: i) autoclaved, based on eucalyptus sawdust; ii) pasteurized, based on sugarcane bagasse and grass (Brachiaria sp.). The sawdust-based substrate was donated by the company Yuri Cogumelos (Sorocaba, São Paulo state, Brazil), which sells blocks for the shiitake production, and is composed of 80 % eucalyptus sawdust and 20 % grass bran, with a moisture content of 68 %. The substrate was distributed in glass jars (600 mL), closed with a metal lid with a cotton filter, and then sterilized in an autoclave at 121 °C for two hours. The substrate JunCao (Jun = mushroom and Cao = grass), based on sugarcane bagasse and grass (Brachiaria sp.), was donated by a producer of Pleurotus ostreatus from Bragança Paulista city (São Paulo state, Brazil), and is composed of 60 % sugarcane bagasse, 35 % Brachiaria sp., and 5 % wheat bran. The substrate was pasteurized with fluent steam for seven days and distributed in sterile glass jars (600 mL). The substrates were inoculated with 1 % of spawn (myceliated wheat grains), which was divided into three fractions and inoculated in three portions on the surface of substrates. The jars were maintained in BOD incubator at 30 °C and the daily growth was measured from the three inoculation points with a pachymeter. The experiment was carried out with 15 replicates per substrate per strain.
Axenic cultivation experiment
The substrate based on eucalyptus sawdust was used for the cultivation in blocks. The substrate (2.5 kg) was packed in polypropylene bags with filters, which were sterilized in an industrial autoclave for 3h and 40min at 121 °C. After sterilization and cooling of the substrate, the packages were inoculated with 2 % of spawn. The packages were incubated in the dark, in a culture chamber, with the temperature set to 30 °C. After complete mycelial growth, the packages were submitted to a rustic cultivation environment, without temperature control, with average temperature of 24 °C (ranging from 7.4 °C to 35.5 °C), average humidity of 64 % (ranging from 34 % to 99 %), and average CO2 concentration of 659 ppm (ranging from 585 ppm to 745 ppm). To induce primordia, the packages of A. fuscosuccinea were cut at the top. For the cultivation of L. gilbertsonii, four forms of induction of primordia were tested, following Pleszczyńska et al. (2013): i) incubation of the blocks in a refrigerator (7–8 °C) for 24 hours and transfer to the grow environment without opening the package; ii) injection of 300 mL of cold sterile distilled water through the package filter; iii) incubation of the blocks in a refrigerator (7–8 °C) for 24 hours, cutting on the surface of the package and removal of mycelium from the surface of grow block (scratching technique); and iv) cutting on the package surface and scratching technique. The A. fuscosuccinea experiment was carried out with 12 replicates and the L. gilbertsonii experiment was carried out with eight replicates per treatment. The blocks were monitored for 60 days after primordia induction.
Bromotalogical analyses of A. fuscosuccinea
The basidiomata obtained were analyzed for moisture content, ash, crude protein, crude fat, and crude fiber (Zenebon et al. 2008). The bromatological analyzes were carried out at the Bromatology Laboratory of the Animal Production Department at ‘Universidade Estadual Paulista Júlio de Mesquita Filho - UNESP’, in Dracena, São Paulo, Brazil. The crude protein content was determined indirectly from the total nitrogen value using Kjeldahl method (Zenebon et al. 2008), using the conversion factor of 4.38 (Crisan & Sands 1978). All analyzes were performed in triplicate and the results express the arithmetic mean.
Statistical analyses
For statistical evaluation, the data obtained were submitted to the Shapiro-Wilk normality test and then analyzed using Two-way ANOVA test. The averages were compared by the Tukey test, using level of significance of 0.05 (Vieira 1980). Statistical analyzes were performed using the software GraphPad Prism version 9 (http://www.graphpad.com).
RESULTS
Auricularia fuscosuccinea
The effects of different temperatures on 12 wild strains of A. fuscosuccinea growth in PDA are shown in Figure 1. The mycelial growth and dry mycelial biomass were higher at 30 °C (p ≤ 0.05) with the first wild strains completing the Petri dish colonization in seven days (Figure 3a-d). Comparing the mycelial growth diameter among all wild strains at 30 °C, there was no difference (p > 0.05) between the wild strains CCIBt2381, CCIBt2959, CCIBt4747, CCIBt4748, CCIBt4751, CCIBt4753, CCIBt4756, and CCIBt4758 (Figure 1a). However, in relation to dry mycelial biomass (Figure 1b), on the seventh day of colonization at 30 °C, the wild strain CCIBt2381 had the highest biomass production (171.20 mg ± 10.01 mg), followed by the wild strain CCIBt4753 (151.11 mg ± 6.77 mg). Based on these results, the wild strains CCIBt2381 and CCIBt4753 were selected for the substrates experiments.
Effects of different temperatures on growth of 12 Brazilian wild strains of Auricularia fuscosuccinea on the seventh day. (a) Mycelium diameter (mm); (b) Dry mycelial biomass (mg). Capital letters compare the means of all wild strains at different temperatures. The asterisk indicates statistical significance by Tukey’s test at 0.05 probability of the best values obtained by the wild strain at the best temperature.
Cultivation of Brazilian wild strains of Auricularia fuscosuccinea. (a-d) Mycelial growth of the wild strain CCIBt4753 in PDA medium on the seventh day; (a) Temperature at 20 °C; (b) Temperature at 25 °C; (c) Temperature at 30 °C; (d) Temperature at 35 °C; (e) Primordia of the wild strain CCIBt4753; (f) Beginning of the basidiomata development of the wild strain CCIBt4753; (g) Basidiomata of the wild strain CCIBt4753 at harvest point; (h) Basidiomata of the wild strain CCIBt2381 at harvest point. Scale bars = 3cm. Photos by M.P. Drewinski.
The wild strains CCIBt4753 and CCIBt2381 completed the colonization of the eucalyptus sawdust substrate in 21 and 22 days, respectively (Figure 2). The wild strain CCIBt4753, although it took longer to start growing in the sawdust (sixth day), completed the substrate colonization before the other wild strain (CCIBt2381) and presented an average daily growth of 5.21 mm ± 2.99 mm, against 4.88 mm ± 0.96 mm of the wild strain CCIBt2381. In the JunCao substrate, the wild strain CCIBt2381 showed a good development at the beginning of the experiment (only until the tenth day), with an average daily growth of 1.00 mm ± 1.45 mm, but without surpassing the development in sawdust. The wild strain CCIBt4753 developed little in the JunCao substrate, showing an average growth of 0.26 mm ± 0.36 mm. For both wild strains, the substrate based on eucalyptus sawdust showed better mycelial growth results (p ≤ 0.05).
Cumulative mycelial growth of two Brazilian wild strains of Auricularia fuscosuccinea in substrates JunCao and based on eucalyptus sawdust. The asterisk indicates statistical significance by Tukey’s test at 0.05 probability.
The wild strain CCIBt2381 took 25 to 27 days to fully colonize the 2.5 kg sawdust substrate block, while the wild strain CCIBt4753 took 28 to 34 days. However, in the blocks with CCIBt4753, primordia were observed from 14 to 17 days after induction, not on the surface but in the lower half of the blocks (Figure 3e-f), and the harvest were performed 35 days after induction of primordia. The primordia of CCIBt2381 developed 21 days after induction, and the first harvest was performed 45 days after primordia induction (Figure 3g-h). Nutritional composition of basidiomata produced is shown in Table II.
Nutritional composition of two Brazilian wild strains of Auricularia fuscosuccinea produced on sawdust-based substrate.
Laetiporus gilbertsonii
For the three wild strains of L. gilbertsonii evaluated, the temperature that best favored the growth of the mycelium was at 30 °C (p ≤ 0.05), with all the wild strains completing the mycelial growth in the Petri dish in seven days (Figures 4a and 6a-d). However, in relation to dry mycelial biomass (Figure 4b), the values were higher at both 25 °C and 30 °C (p ≤ 0.05). The wild strain CCIBt4710, despite not showing differences in growth diameter against the other two wild strains evaluated, was the one that obtained the best values (p ≤ 0.05) of dry mycelial biomass, both at 25 °C (78.71 mg ± 5.10 mg) and 30 °C (78.00 mg ± 4.56 mg).
Effects of different temperatures on growth of three Brazilian wild strains of Laetiporus gilbertsonii on the seventh day. (a) Mycelium diameter (mm); (b) Dry mycelial biomass (mg). Capital letters compare the means of all wild strains at different temperatures. The asterisk indicates statistical significance by Tukey’s test at 0.05 probability of the best values obtained by the wild strains at each temperature.
Cultivation of Brazilian wild strains of Laetiporus gilbertsonii. (a-d) Mycelial growth of the wild strain CCIBt4710 in PDA medium on the seventh day; (a) Temperature at 20 °C; (b) Temperature at 25 °C; (c) Temperature at 30 °C; (d) Temperature at 35 °C; (e) Specimen MPD306 (= CCIBt4710) in the field; (f) Fully colonized block CCIBt4710; (g) Fully colonized block CCIBt4718; (h-k) Mycelial growth out of the filter of a block of the wild strain CCIBt4710. Scale bars = 3cm. Photos by M.P. Drewinski.
The wild strains CCIBt4710 and CCIBt4718 were evaluated in the substrates experiment and completed the colonization of the sawdust-based substrate in 11 and 12 days, respectively (Figure 5). The mycelium of L. gilbertsonii is very aerial, fragile, and powdered, but it grew fast in the substrate based on eucalyptus sawdust after the second day from the inoculation. The average daily growth in this substrate was 9.60 mm ± 2.85 mm for the wild strain CCIBt4710 and 9.39 mm ± 2.88 mm for the wild strain CCIBt4718. On the JunCao substrate, the mycelium started to grow on the fourth day after inoculation, and it developed little, with an average daily growth of 0.27 mm ± 0.36 mm for the wild strain CCIBt4710 and 0.16 mm ± 0.24 mm for the wild strain CCIBt4718. The substrate based on eucalyptus sawdust was better for the mycelial development (p ≤ 0.05) of both wild strains of L. gilbertsonii when compared to the JunCao substrate.
Cumulative mycelial growth of two Brazilian wild strains of Laetiporus gilbertsonii in substrates JunCao and based on eucalyptus sawdust. The asterisk indicates statistical significance by Tukey’s test at 0.05 probability.
The wild strains CCIBt4710 and CCIBt4718 were evaluated in the experiment of cultivation in blocks (2.5 kg) with substrate based on eucalyptus sawdust. The wild strains colonized the block quickly (Figure 6f), taking from 9 to 10 days (CCIBt4710) and from 10 to 11 days (CCIBt4718) to complete the blocks (Figure 6g). After 30 days of inoculation, the blocks were induced to form primordia. In the blocks in which the bag was opened and/or the surface layer of the mycelium was removed from substrate, there was new mycelial growth with an intensification of the orange color of the mycelium, but without the formation of primordia. In the blocks where the bag was not opened, it was possible to observe the mycelium growing out of the filter (Figure 6h-k) in: four bags of the wild strain CCIBt4710 incubated in the refrigerator; one bag of the wild strain CCIBt4710 that was injected cold water through the filter; and one bag of the wild strain CCIBt4718 that was incubated in the refrigerator. Despite the formation of this external mycelial mass, over time other contaminating fungi began to grow on the surface of the mycelium of L. gilbertsonii and it was not possible to obtain basidiomata for this species.
DISCUSSION
The growth experiments on PDA culture medium at different temperatures showed a better mycelial development of the A. fuscosuccinea wild strains at 30 °C. Coniglio et al. (2021) studied five wild strains of A. fuscosuccinea from Argentinian Paranaense Rainforest and also indicates 30 °C as the optimal temperature for mycelial development in PDA medium. The evaluated wild strains of L. gilbertsonii developed well at both 25 °C and 30 °C. Hitherto, there are no studies on cultivation of L. gilbertsonii, only a few studies on another species of the genus, L. sulphureus, for which the suitable temperatures for mycelial growth also ranged between 25 °C and 30 °C (Okamura et al. 2000, Luangharn et al. 2014). Normally, tropical mushroom species grow rapidly at 25 °C or higher temperatures, and thus they can be produced in tropical areas more quickly than species from temperate climate areas (Klomklung et al. 2012).
Most studies on the domestication of A. fuscosuccinea were published by researchers from Mexico (Castillejos-Puón et al. 1996, Calvo-Bado et al. 1996, Carreño-Ruiz et al. 2014, Morales & Sánchez 2017), although there are studies with specimens from other locations, such as the United States of America, Brazil, Peru, Colombia, and Ecuador (Wong 1993, Vargas et al. 2015, Niño et al. 2017, Rodríguez et al. 2018). Wong (1993) studied two strains of A. fuscosuccinea from Brazil with success on the basidiomata production, although the authors did not describe in detail the substrate used neither the cultivation conditions. Here,A we demonstrate that it is possible to use eucalyptus sawdust as substrate to produce wild strains of A. fuscosuccinea. The use of substrates based on eucalyptus sawdust has already been reported to produce other wild mushrooms such as A. auricula-judae (Chen et al. 2013), Oudemansiella canarii (Jungh.) Höhn. (Ruegger et al. 2001), and Gymnopilus pampeanus (Speg.) Singer (Colavolpe & Albertó 2014).
Regarding the composition of A. fuscosuccinea produced in this study, the crude protein values found (10.73–12.11 %) were higher than those obtained by Mau et al. (1998) but lower than those obtained by Sánchez et al. (2018), which found 8.62 % and 13.5 % of crude protein, respectively. For crude fiber, the values obtained here (3.73–3.85 %) were higher than those found by Sánchez et al. (2018) but lower than those recorded by Mau et al. (1998), which found 5.8 % and 11.69 % of crude fiber, respectively. The value of the crude fat in the samples studied here (0.82–0.91 %) was much lower than that found by Mau et al. (1998) and Sánchez et al. (2018) for A. fuscosuccinea, which were 4.48 % and 13.5 %, respectively.
This is the first study on cultivation of L. gilbertsonii. Regarding on the evaluated substrates, it was possible to observe a fast colonization of the mycelium of L. gilbertsonii in the substrate based on eucalyptus sawdust. This result was already expected because the species occurs naturally in Eucalyptus spp. wood (Burdsall Jr. & Banik 2001). Unlike other commercially produced mushroom species, L. gilbertsonii is a brown rot fungus and does not produce lignin-degrading enzymes (Burdsall Jr. & Banik 2001). Pleszczyńska et al. 2013 were the first to report the successful initiation and development of a Laetiporus species mushrooms in large scale experiments. They studied the development of twelve wild strains of L. sulphureus from Poland in a substrate based on a mixture of sawdust. Among the twelve studied strains, only two produced basidiomata. It was found that shocking the fungus mycelium with cold water or at low temperature was the most suitable method for forcing L. sulphureus basidioma to grow (Pleszczyńska et al. 2013). In this study, we tested the same induction methods used by Pleszczyńska et al. 2013 for L. gilbertsonii, but we were not successful in obtaining primordia and neither producing basidiomata, unfortunately.
Besides the mushrooms, mycelia and the culture media used in the fungi cultivation also have been explored as potential sources of food and bioactive compounds (Cheung 1996, Gan et al. 2012, Ma et al. 2016, Souilem et al. 2017, Stoffel 2019). Compared to mushrooms production, mycelium cultivation has potential advantages for higher production of biomass in a more-compact space over a shorter incubation time (Gan et al. 2012).
CONCLUSIONS
We obtained twelve wild strains of A. fuscosuccinea and three wild strains of L. gilbertsonii from the Brazilian Atlantic Rainforest. The temperature that best favored the mycelial growth of A. fuscosuccinea was 30 °C. For L. gilbertsonii, the temperatures of 25 °C and 30 °C were suitable for the mycelium development. Mycelia of both species better developed in the sterile sawdust substrate, in which it was possible to produce basidiomata of the two wild strains of A. fuscosuccinea evaluated. The nutritional values of A. fuscosuccinea studied here are similar to those described for other species of the genus. This is the first study on cultivation of L. gilbertsonii. Although the mycelia of the two evaluated wild strains of L. gilbertsonii colonized the eucalyptus-based substrate quickly, they do not produced primordia neither basidiomata. However, it was possible to observe the mycelium of L. gilbertsonii growing out of the filter in some bags in which methods based on low temperature induction were performed. There is a huge potential associated to the collecting, identification, and maintenance of mushroom strains and further studies are needed for domestication and optimization of wild species production.
ACKNOWLEDGMENTS
The authors are grateful for the financial support received from the ‘Fundação de Amparo à Pesquisa do Estado de São Paulo – FAPESP’ (grants #2017/25754-9 and #2018/15677-0). MPD thanks Jorge Arruda Neto for donating the pasteurized substrate. NMJ thanks the ‘Conselho Nacional de Desenvolvimento Científico e Tecnológico–CNPq’ (Research Productivity grant 314236/2021-0).
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