11 urn:lsid:arphahub.com:pub:C004A564-9D6A-5F9F-B058-6A3815DFE9C3 MycoKeys MC 1314-4057 1314-4049 Pensoft Publishers 10.3897/mycokeys.91.86257 86257 Research Article Hypocreales Sordariomycetes Taxonomy Asia Morphological characteristics and phylogenetic evidence reveal two new species of Acremonium (Hypocreales, Sordariomycetes) Li Xin https://orcid.org/0000-0001-7910-1469 1 Zhang Zhi-Yuan 1 Ren Yu-Lian https://orcid.org/0000-0003-2424-1266 1 Chen Wan-Hao https://orcid.org/0000-0001-7240-6841 2 Liang Jian-Dong https://orcid.org/0000-0002-3939-3900 2 Pan Ji-Mei 2 Huang Jian-Zhong 3 Liang Zong-Qi 1 Han Yan-Feng swallow1128@126.com 1 Institute of Fungus Resources, Department of Ecology, College of Life Sciences, Guizhou University, Guiyang 550025, Guizhou, China Guizhou University Guiyang China Basic Medical School, Guizhou University of Traditional Chinese Medicine, Guiyang 550025, Guizhou, China Guizhou University of Traditional Chinese Medicine Guiyang China Engineering Research Center of Industrial Microbiology, Ministry of Education, Fujian Normal University, Fuzhou 350108, Fujian, China Fujian Normal University Fuzhou China

Corresponding author: Yan-Feng Han (swallow1128@126.com)

Academic editor: Andrew Miller

 2022 15 07 2022 91 85 96 327E86F9-1CC6-5068-A060-A87D0E3B8C94 6848352 07 05 2022 04 07 2022 Xin Li, Zhi-Yuan Zhang, Yu-Lian Ren, Wan-Hao Chen, Jian-Dong Liang, Ji-Mei Pan, Jian-Zhong Huang, Zong-Qi Liang, Yan-Feng Han This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Using chicken feathers as bait, Acremonium globosisporumsp. nov. and Acremonium curvumsp. nov. were collected from the soil of Yuncheng East Garden Wildlife Zoo and Zhengzhou Zoo in China. They were identified by combining the morphological characteristics and the two-locus DNA sequence (LSU and ITS) analyses. In the phylogenetic tree, both new species clustered into separate subclades, respectively. They were different from their allied species in their morphology. The description, illustrations, and phylogenetic tree of the two new species were provided.

 Acremonium filamentous fungi phylogeny taxonomy Citation

Li X, Zhang Z-Y, Ren Y-L, Chen W-H, Liang J-D, Pan J-M, Huang J-Z, Liang Z-Q, Han Y-F (2022) Morphological characteristics and phylogenetic evidence reveal two new species of Acremonium (Hypocreales, Sordariomycetes). MycoKeys 91: 85–96. https://doi.org/10.3897/mycokeys.91.86257

 Introduction

The genus Acremonium Link, established in 1929, with A. alternatum Link as the type species, is one of the largest and most complex genera of asexually typified. The morphological characteristics consist of hyphae septate, mostly tapered and lateral phialides, produced singly or in small groups, and unicellular conidia produced in mucoid heads or unconnected chains (Summerbell et al. 2011). Nowadays, Acremonium has 217 records in the Index Fungorum (http://www.indexfungorum.org/Names/Names.asp, retrieval on 30 Jun. 2022). The traditionally circumscribed Acremonium is polyphyletic, which explains why many Acremonium species were transferred to other genera and families (Yang et al. 2019). Thus, there are still many unidentified, suspect or misidentified taxa that require taxonomic investigation.

Due to the poor differentiation of asexual forms of the genus Acremonium, it is difficult to identify species only by morphological differences. To address this issue, there are many unidentified and suspicious species that require further phylogenetic analysis. To date, many isolates of Acremonium spp. lack the gene loci such as SSU, TEF 1-α and RPB2 (Table 1), therefore, phylogenetic analyses of this genus are generally performed based on the single locus sequences, especially LSU (Hyde et al. 2020).

In the present study, two new species of Acremonium were identified in a survey of keratinolytic fungi from China, which were enriched by the baiting technique. We provided a description, illustrations, and phylogenetic tree for the two new species.

 Materials and methods Fungal isolation and morphology

Soil samples were collected from Yuncheng East Garden Wildlife Zoo (35°6'26"N, 111°4'24"E) (three isolates), Yuncheng City, Shanxi Province and Zhengzhou Zoo (34°47'20"N, 113°40'41"E) (one isolate), Zhengzhou City, Henan Province, China by Yu-Lian Ren on July 2021. We collected 3–10 cm below the soil surface, placed the samples in sterile Ziploc plastic bags (Kaixin Biotechnology, Guizhou, China), and transported them to the laboratory (Zhang et al. 2019a, b). Then, they were treated and isolated according to the baiting method (using chicken feathers as bait: a method specifically designed for isolating keratinophilic microbes) of Zhang et al. (2020a, b; 2021). We washed the chicken feathers, sterilized them in an autoclave for 30 minutes at 121 °C, and dried them in an oven at 50 °C. The sterile and dried chicken feathers were mixed with soil samples and then wet with sterile distilled water and cultured at darkroom temperature for 1 month (Li et al. 2022).

Then, the 2 g samples were weighed in a conical flask with glass beads containing 20 mL sterile water and mixed evenly by eddy shock for 10 min. Next, 1 mL samples were mixed evenly in 9 mL sterile water in a sterile environment and diluted to 10-3. Then, 1 mL 10-3 samples were put into a sterile petri dish, and SDA medium containing 50 mg/L penicillin and 50 mg/L streptomycin was added and mixed. The target strains were isolated. The purified strains were transferred to PDA, OA, and MEA plates for dark culture at 25 °C for 7 days. Microscopic features were examined by making direct wet mounts with 25% lactic acid on PDA, with a light microscope.

The cultures were placed to slowly dry at 50 °C to produce the dried holotype. The dried holotype was deposited in the Mycological Herbarium of the Institute of Microbiology, Chinese Academy of Sciences, Beijing, China (HMAS), while ex-type living culture was stored in PDA test tubes which were deposited in the China General Microbiological Culture Collection Center (CGMCC), and the Institute of Fungus Resources, Guizhou University, Guiyang City, Guizhou, China (GZUIFR).

 DNA extraction, PCR amplification, and sequencing

We used a 5% chelex-100 solution for total genomic DNA extraction. ITS1/ITS4 (White et al. 1990), LROR/LR7 (Vilgalys and Hester 1990), EF1-983F/ EF1-2218R (Rehner and Buckley 2005), fRPB2-5f/ fRPB2-7cR (Liu et al. 1999), and NS1 and NS4 (White et al. 1990) primers were used for amplification of the internal transcribed spacers (ITS), the 28S nrRNA locus (LSU), translation elongation factor 1-alpha gene region (TEF 1-α), RNA polymerase II second largest subunit gene (RPB2), and small subunit rDNA (SSU), respectively. Purification and sequencing were performed by Quintarabio (Wuhan, China). The new sequences were submitted to GenBank (Table 1).

Strains included in the present study.

Species Strains LSU ITS SSU TEF 1-α RPB2
Acremonium alcalophilum CBS 114.92T JX158443 DQ825967 JX158486 JX158399 JX158465
Acremonium alternatum CBS 407.66T HQ231988 HE798150
Acremonium alternatum CBS 831.97 HQ231989
Acremonium arthrinii MFLU 18-1225T MN036334 MN036335 MN038169
Acremonium behniae CBS 146824T MW175400 MW175360
Acremonium biseptum CBS 750.69T HQ231998
Acremonium blochii CBS 993.69 HQ232002 HE608636
Acremonium borodinense CBS 101148T HQ232003 HE608635
Acremonium brachypenium CBS 866.73T HQ232004 AB540570
Acremonium camptosporum CBS 756.69T HQ232008 HQ232186
Acremonium cavaraeanum CBS 101149T HF680202 HF680220
Acremonium cavaraeanum CBS 111656 HF680203 HF680221
Acremonium cavaraeanum CBS 758.69 HQ232012 HF680222
Acremonium cerealis CBS 207.65 HQ232013
Acremonium cerealis CBS 215.69 HQ232014
Acremonium chiangraiense MFLUCC 14-0397T MN648329 MN648324
Acremonium chrysogenum CBS 144.62T HQ232017 HQ232187
Acremonium chrysogenum CBS 401.65 MH870276 MH858636
Acremonium citrinum CBS 384.96T HF680217 HF680236
Acremonium dimorphosporum CBS 139050T LN810506 LN810515
Acremonium exiguum CBS 587.73T HQ232035
Acremonium exuviarum UAMH 9995T HQ232036 AY882946
Acremonium felinum CBS 147.81T AB540488 AB540562
Acremonium flavum CBS 596.70T HQ232037 HQ232191
Acremonium flavum CBS 316.72 MH872204 MH860487
Acremonium fuci CBS 112868T AY632653
Acremonium fuci CBS 113889 AY632652
Acremonium fusidioides CBS 109069 HF680204 HF680223
Acremonium fusidioides CBS 991.69 HF680211 HF680230
Acremonium fusidioides CBS 840.68T HQ232039 FN706542
Acremonium hansfordii CBS 390.73 HQ232043 AB540578
Acremonium hennebertii CBS 768.69T HQ232044 HF680238
Acremonium inflatum CBS 212.69T HQ232050
Acremonium mali ACCC 39305T MF993114 MF987658
Acremonium moniliforme CBS 139051T LN810507 LN810516
Acremonium moniliforme FMR 10363 LN810508 LN810517
Acremonium parvum CBS 381.70A HQ231986 HF680219
Acremonium persicinum CBS 310.59T HQ232077
Acremonium persicinum CBS 101694 HQ232085
Acremonium pinkertoniae CBS 157.70T HQ232089 HQ232202
Acremonium polychroma CBS 181.27T HQ232091 AB540567
Acremonium potronii CBS 189.70 HQ232094
Acremonium pseudozeylanicum CBS 560.73T HQ232101
Acremonium pteridii CBS 782.69T HQ232102
Acremonium pteridii CBS 784.69 HQ232103
Acremonium sclerotigenum CBS 124.42T HQ232126 FN706552 HQ232209
Acremonium sclerotigenum A101 KC987215 KC987139 KC987177 KC998961
Acremonium sclerotigenum A130 KC987242 KC987166 KC987204 KC998988
Acremonium sp. E102 KC987248 KC987172 KC987210 KC998994 KC999030
Acremonium spinosum CBS 136.33T HQ232137 HE608637 HQ232210
Acremonium stroudii CBS 138820T KM225291
Acremonium tumulicola CBS 127532T AB540478 AB540552
Acremonium variecolor CBS 130360T HE608651 HE608647
Acremonium variecolor CBS 130361 HE608652 HE608648
Acremonium verruculosum CBS 989.69T HQ232150
Acrophialophora hechuanensis GZUIFR-H08-1T MK926789 DQ185070 EU053286
Brunneomyces brunnescens CBS 559.73T HQ231966 LN810520 HQ232184 LN810534
Brunneomyces hominis UTHSC 06-415T LN810509 KP131517 LN810535
Bryocentria brongniartii M139 EU940105 EU940052
Bryocentria brongniartii M190 EU940125 EU940052
Bryocentria metzgeriae M140 EU940106
Bulbithecium hyalosporum CBS 318.91T AF096187 HE608634
Cephalosporium purpurascens CBS 149.62T HQ232071
Cosmospora lavitskiae CBS 530.68T HQ231997
Emericellopsis alkalina CBS 127350T KC987247 KC987171 KC987209 KC998993 KC999029
Emericellopsis terricola CBS 120.40T U57082 U57676 U44112
Gliomastix roseogrisea CBS 134.56T HQ232121
Hapsidospora irregularis ATCC 22087T AF096192 AF096177
Kiflimonium curvulum CBS 430.66T HQ232026 HE608638 HQ232188
Lanatonectria flavolanata CBS 230.31 HQ232157
Leucosphaerina arxii CBS 737.84T HE608662 HE608640
Nigrosabulum globosum ATCC 22102T AF096195
Paracremonium contagium CBS 110348T HQ232118 KM231831 KM231966
Parasarocladium breve CBS 150.62T HQ232005
Parasarocladium radiatum CBS 142.62T HQ232104 HQ232205
Pestalotiopsis hawaiiensis CBS 114491T KM116239 KM199339 KM199514
Pestalotiopsis spathulata CBS 356.86T KM116236 KM199338 KM199513
Phialemonium atrogriseum CBS 604.67T HQ231981 HE610367 FJ176825
Pseudoacremonium sacchari CBS 137990T KJ869201 KJ869144
Sarcopodium vanillae CBS 100582 HQ232174 KM231780 KM231911
Sarocladium bacillisporum CBS 425.67T HQ231992 HE608639 HQ232179
Sarocladium bactrocephalum CBS 749.69T HQ231994 HG965006 HQ232180
Sarocladium strictum CBS 346.70T HQ232141 AY214439 HQ232211
Sarocladium terricola CBS 243.59T HQ232046 HQ232196
Selinia pulchra AR 2812 GQ505992 HM484859 HM484841
Trichothecium crotocinigenum CBS 129.64T HQ232018 AJ621773
Trichothecium indicum CBS 123.78T AF096194 AF096179
Trichothecium roseum DAOM 208997 U69891 U69892
Trichothecium sympodiale ATCC 36477 U69889 U69890
Acremonium curvum CGMCC 3.20954 = GZUIFR 22.035T ON041050 ON041034 ON876754 ON494579 ON494583
Acremonium globosisporum CGMCC 3.20955 = GZUIFR 22.036T ON041051 ON041035 ON876755 ON494580 ON494584
Acremonium globosisporum GZUIFR 22.037 ON041052 ON041036 ON876756 ON494581 ON494585
Acremonium globosisporum GZUIFR 22.038 ON041053 ON041037 ON876757 ON494582 ON494586

Notes: “T” stands for Ex-type strains.

 Phylogenetic analyses

The ITS and LSU sequences of Acremonium were downloaded from GenBank (Table 1). Two strains of Pestalotiopsis spathulata (CBS 356.86) and P. hawaiiensis (CBS 114491) were chosen as the outgroup taxa. The TBtools were used for name simplification and renaming (Chen et al. 2020). Sequences were aligned by MAFFT v7.037 (Katoh and Standley 2013). Multi-locus was concatenated by PhyloSuite v1.16 (Zhang et al. 2020a).

Bayesian inference (BI) and maximum likelihood (ML) methods were used in the analysis. For BI analysis was conducted with MrBayes v3.2 (Ronquist et al. 2012) and Markov chain Monte Carlo (MCMC) simulations; ML analysis was performed using IQ-TREE v1.6.11 (Nguyen et al. 2015), as outlined in Li et al (2022). All analyses were performed in PhyloSuite V1.16 (Zhang et al. 2020b).

 Results Phylogeny

Based on a BLAST search (https://blast.ncbi.nlm.nih.gov/Blast.cgi) using the LSU sequences, our isolates were identified as belonging to the genus Acremonium. To further determine the phylogenetic position of these strains, we performed a multi-locus phylogenetic analysis. The dataset was composed of LSU (1–430 bp) and ITS (431–1005 bp) gene, comprising a total of 1005 characters (including gaps). The best-fit partition model for ML analysis and BI analysis is shown in Table 2. The results showed that the CGMCC 3.20955, GZUIFR 22.037, and GZUIFR 22.038 are still grouped in the Pinkertoniae-clade (Fig. 1). The CGMCC 3.20954 is still grouped in the Chrysogenum-clade (Fig. 1).

The best-fit substitution models are used in multi-locus phylogenetic construction.

LSU ITS
ML analysis TN+F+R5 GTR+F+R4
BI analysis GTR+F+I+G4 GTR+F+I+G4
10.3897/mycokeys.91.86257.figure1 6F9E390F-A124-5792-94DB-E3FC7DD1AFCF

Phylogenetic tree of the genus Acremonium constructed from LSU and ITS. Bayesian posterior probability (≥ 0.95) and ML bootstrap values (≥ 70%) are indicated along branches (BPP/ML).

https://binary.pensoft.net/fig/715606 Taxonomy Fungi Hypocreales Bionectriaceae 35BF27DA-FC43-57D8-989A-49581DCE8C51 Acremonium globosisporum 843765 Xin Li, Y.F. Han & Z.Q. Liang sp. nov. Fig. 2 Type.

Yuncheng East Garden Wildlife Zoo, Yuncheng City, Shanxi Province, China N35°6'26", E111°4'24", isolated from green belt soil, July 2021, Yu-Lian Ren (dried holotype culture HMAS 351939, ex-holotype culture CGMCC 3.20955 = GZUIFR 22.036). ITS sequences, GenBank ON041035; LSU sequences, GenBank ON041051; SSU sequences, GenBank ON876755; TEF 1-α sequences, GenBank ON494580; RPB2 sequences, GenBank ON494584.

10.3897/mycokeys.91.86257.figure2 C68BBD33-589C-56BD-90F4-CC764D080EE4

Morphology of Acremonium globosisporum sp. nov. a–f colony on PDA, OA and MEA after 7 d at 25 °C (upper surface and lower surface) g–j conidia are borne on the phialides k–l winding hyphae and inflate hyphae. Scale bars: 4 mm (a–f); 10 μm (g–l).

https://binary.pensoft.net/fig/715607 Description.

Colonies on PDA and OA at 25 °C attaining 11–13 mm and 9–11 mm diam respectively after 7 d, white, flat or raised, velvety to slightly cottony. On MEA at 25 °C, reaching 8–10 mm after 7 d, white to yellowish white, raised, slimy. Hyphae hyaline, septate, sometimes winding and inflate, 1.5–11.0 µm wide. Sporulation abundant. Phialides are mostly borne singly, hyaline, erect to slightly curved, sometimes forming a collarette, 9.0–22.0 µm long, tapering from 1.5–3.5 µm near the base to 0.5–1.5 µm. Conidia cohering in long chains, with minutely truncate ends, up to 27.5 µm long, globose or subglobose, 2.5–4.5 × 2.5–4.5 µm (x– ± SD = 3.4 ± 0.77 × 3.6 ± 0.52, n = 50) diam. Chlamydospores and teleomorph stage were not observed.

 Etymology.

globosisporum. A reference to the global conidia.

 Additional specimens examined.

Yuncheng East Garden Wildlife Zoo, Yuncheng City, Shanxi Province, China N35°6'26", E111°4'24", isolated from green belt soil, July 2021, Yu-Lian Ren, GZUIFR 22.037, ITS, LSU, SSU, TEF 1-α, RPB2 sequences GenBank ON041036, ON041052, ON876756, ON494581, ON494585; GZUIFR 22.038, ITS, LSU, SSU, TEF 1-α, RPB2 sequences GenBank ON041037, ON041053, ON876757, ON494582, ON494586.

 Known distribution.

Yuncheng City, Shanxi Province, China.

 Notes.

The phylogeny results showed that the CGMCC 3.20955, GZUIFR 22.037 and GZUIFR 22.038 still nested in the Pinkertoniae-clade. The morphological characteristics of Acremonium globosisporum were similar to other species of the Pinkertoniae-clade in that phialides were erect on the hyphae; sporulation was abundant, and conidia were subglobose (Ito et al. 2000). However, Acremonium globosisporum hyphae were sometimes winding and inflated, with conidia cohering in long chains, unlike other species.

 Fungi Hypocreales Bionectriaceae 7DC71370-B32D-59C2-B927-D407C2A66239 Acremonium curvum 843766 Xin Li, Y.F. Han & Z.Q. Liang sp. nov. Fig. 3 Type.

Zhengzhou Zoo, Zhengzhou City, Henan Province, China N34°47'20", E113°40'41", isolated from green belt soil, July 2021, Yu-Lian Ren (dried holotype culture HMAS 351938, ex-holotype culture CGMCC 3.20954 = GZUIFR 22.035). ITS sequences, GenBank ON041034, LSU sequences, GenBank ON041050; SSU sequences, GenBank ON876754; TEF 1-α sequences, GenBank ON494579; RPB2 sequences, GenBank ON494583.

10.3897/mycokeys.91.86257.figure3 AA4457C3-2005-5D36-89A4-C00B00AD3A3A

Morphology of Acremonium curvum sp. nov. a–f colony on PDA, OA and MEA after 7 d at 25 °C (upper surface and lower surface) g, I, j conidia are borne on the phialides h Winding hyphae. Scale bars: 4 mm (a–f); 10 μm (g–j).

https://binary.pensoft.net/fig/715608 Description.

Colonies on PDA and OA at 25 °C attaining 11–14 mm and 7–9 mm diam respectively after 7 d, white, flat, radially folded or rugose. On MEA at 25 °C, reaching 6–8 mm after 7 d, white to yellowish-white, slimy. Hyphae hyaline, septate, sometimes winding, 1.5–2.5 µm wide. Sporulation abundant. Phialides are mostly borne singly, curved, slightly inflated at the base, tapered at the tip, up to 38.0 µm long. tapering from 1.5–3.5 µm near the base to 0.5–1.5 µm. Conidia cohering together on the top of phialides, one-celled, solitary, or several fascicled, ovoid or subglobose, 3.0–7.0 × 2.5–3.5 µm (x– ± SD = 4.1 ± 1.18 ×3.2 ± 0.77, n = 50) diam. Chlamydospores and teleomorph stage were not observed.

 Etymology.

curvum. Referring to the curved Phialides.

 Known distribution.

Henan Province, China.

 Notes.

Based on the multi-locus analysis we found that Acremonium curvum had close phylogenetic affinities to other taxa of the Chrysogenum-clade. Morphologically, A. curvum was similar to other taxa of the Chrysogenum-clade in having simple or rarely branched conidiophores, slightly inflated at the base and tapered at tip phialides, and ovoid to subglobose conidia (Yang et al. 2019). Conidia of Hapsidospora irregularis and A. curvum had several fascicled at the tips of the conidiophores (Malloch and Cain 1970). However, A. curvum was differentiated by having mostly curved phialides and the conidia were several fascicled at the tips of the phialides.

 Discussion

In the present study, four strains of Acremonium fungi were isolated from soil in the Shanxi and Henan Province, China. Two-locus (LSU and ITS) phylogenetic analyses in combination with morphological characteristics were used for identification. As a result, two new species of A. curvum (one isolate) and A. globosisporum (three isolates) were proposed.

With the development of biotechnology, a growing number of studies have combined morphological and phylogenetic features to distinguish between species. This provides the basis for more precise species naming. Generally, the fungal ITS marker includes considerably more sequence variability, and consequently provides high interspecific resolution, and also some degree of intraspecific variability (Nilsson et al. 2008). Therefore, ITS has been widely used in studies of fungal inter- and intraspecific relationships (Dai et al. 2020; Szczepańska et al. 2021). There are numerous ITS sequences stored in public databases, which are incomparable to other molecular markers (Zhang et al. 2022). In addition, according to Vu et al. (2019), combining ITS and LSU can improve the accuracy of fungal species discrimination with high generality. They think that fungi commonly present in clinical, environmental, or economically relevant communities can often be identified to species level by their ITS and LSU barcodes (Vu et al. 2019).

Although, Yang et al. (2019) used a multi-locus phylogenetic analysis in introducing the new species Acremonium arthrinii, lacking loci such as SSU, TEF 1-α and RPB2 (Table 1) in the isolates of Acremonium spp. were relatively serious, so it is not difficult to find that the strains with SSU and TEF 1-α in this analysis were not yet 50% or even 30% of the total number of strains. Therefore, although we sequenced these above loci in the new isolates, they were not included in the phylogenetic analysis. In the future, the phylogeny relationships of Acremonium members will undoubtedly vary and become clearer with the increase of the number and type of molecular used.

In recent years, Acremonium spp. has been reported to cause immunocompetent and immunocompromised individual diseases, such as brain abscess (Anis et al. 2021), fungal keratitis (Liu et al. 2021), fungal osteomyelitis (Jalan et al. 2021), and fungal maxillary sinusitis (Durbec et al. 2011). In the present study, all strains were isolated by a method specifically designed for the isolation of keratinophilic microbes. Therefore, more studies are necessary to confirm whether A. curvum and A. globosisporum are opportunistic infectious pathogens that infect the skin and cause skin infection, as well as their potential application in the degradation of keratin-rich matrices.

 Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (no. 32060011, 32160007, 31860002), “Hundred” Talent Projects of Guizhou Province (Qian Ke He [2020] 6005), and the Key Areas of Research and Development Program of Guangdong Province (no. 2018B020205003), and Construction Program of Biology First-class Discipline in Guizhou (GNYL [2017] 009). We appreciate MDPI for the English-language editing of the whole manuscript.

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