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. 2023 May 15;64(3):101–108. doi: 10.47371/mycosci.2023.04.001

Molecular phylogeny and morphology reveal a new wood-rotting fungal species, Sistotrema yunnanense sp. nov. from the Yunnan-Guizhou Plateau

Li-Qiong Cai a, Chang-Lin Zhao a,b,c,*
PMCID: PMC10308066  PMID: 37397608

Abstract

Wood-rotting fungi are important components of woody plant ecosystems and play an active role in the decomposition and turnover of nutrients from wood, and are among the major groups of Basidiomycota. In this study, a new species of wood-rotting fungus, Sistotrema yunnanense, was proposed based on morphological characteristics and molecular evidence. It is characterized by resupinate basidiomata, a monomitic hyphal system having generative hyphae with clamp connections, suburniform to urniform basidia, and short-cylindrical to oblong ellipsoid basidiospores (4.5-6.5 × 3-4 µm). Phylogenetic analyses performed using the large subunit nuc rDNA indicated that S. yunnanense was nested within the genus Sistotrema s.l. of the family Hydnaceae, within the order Cantharellales.

Keywords: Cantharellales, Hydnaceae, molecular systematics, taxonomy, Yunnan Province

In forest ecosystems, fungi play essential ecological roles by driving carbon cycling in forest soils, mediating mineral uptake by plants, and alleviating carbon limitations (Tedersoo et al., 2014). Wood-rotting fungi are a highly diverse cosmopolitan group that are associated with a range of plants growing in boreal, temperate, subtropical, and tropical regions (Gilbertson & Ryvarden, 1987; Núñez & Ryvarden, 2001; Bernicchia & Gorjón, 2010; Dai, 2012; Ryvarden & Melo, 2014; Dai et al., 2015; Wu et al., 2020; Dai et al., 2021). The wood-rotting fungal genus, Sistotrema Fr. (Hydnaceae, Cantharellales), typified by S. confluens Pers., is a comparatively large genus belonging to the phylum Basidiomycota, and is morphologically characterized by resupinate or pileate-stipitate, soft basidiomes, smooth, grandinioid, hydnoid, or poroid hymenophore with various characteristic textures (pellicular, membranaceous, or ceraceous), a monomitic hyphal system with oily inclusions, urniform basidia, and smooth, thin-walled, basidiospores containing cytoplasmic oil droplets (Eriksson, Hjortstam, & Ryvarden, 1984; Bernicchia & Gorjón, 2010). Based on the MycoBank database (http://www.mycobank.org, accessed Jun 20, 2022) and the Index Fungorum (http://www.indexfungorum.org, accessed Jun 20, 2022), the genus Sistotrema has 204 registered species and intraspecies names, however the actual number of the species is 60 (Eriksson et al., 1984; Bernicchia & Gorjón, 2010; Sugawara et al., 2022).

These pioneering phylogenetic studies reveal that the genus Sistotrema is highly polyphyletic (Nilsson, Larsson, Larsson, & Kõljalg, 2006; Larsson, 2007, Hibbett et al., 2014), and were conducted before the advent of molecular systematics (Kotiranta & Larsson, 2013; Cao, Hu, Yu, Wei, & Yuan, 2021; Sugawara et al., 2022). Kotiranta and Larsson (2013) conducted preliminary phylogenetic research on Sistotrema and proposed a new species, S. luteoviride Kotir. & K.H. Larss., which clustered with S. citriforme (M.P. Christ) K.H. Larss. & Hjortsam with high bootstrap support (98%), and was grouped together with S. pistilliferum Hauerslev, Membranomyces spurius (Bourdot) Jülich, and two Clavulina J. Schröt. species in a moderately supported clade (79%). The nuclear rDNA sequence analysis of the phylogenetic diversity of bulbil-forming lichenicolous fungi in Cantharellales by Lawrey et al. (2016) revealed that the type species, S. confluens, grouped closely with the genus Cantharellus Adans. ex Fr. A comprehensive phylogenetic analysis based on a multiple-marker dataset for the entire Hydnaceae sensu stricto indicated that Sistotrema along with its sister genus Hydnum L. forms a fully supported lineage that is closely related to the genera Craterellus Pers. and Cantharellus (Cao et al., 2021). Phylogenetic trees obtained using the fungal nuc rDNA ITS and LSU and rpb2 sequences showed that Sistotrema grouped with Hydnum; however, the generic boundary was unclear (Sugawara et al., 2022).

An undescribed fungal taxon was identified during investigations on wood-rotting fungi in southern China. The unknown taxon was placed in the genus Sistotrema based on analyses of the morphology and sequences of the large subunit (LSU) nuclear ribosomal RNA gene, and is proposed here as a new species, S. yunnanense.

The specimens studied were deposited at the herbarium of Southwest Forestry University (SWFC), Kunming, Yunnan Province, P.R. China. Macroscopic descriptions are based on field notes. Color terms followed Petersen (1996). All the materials were examined under a Nikon 80i microscope. Drawings were made with the aid of a drawing tube. The measurements and drawings were made from slide preparations stained with cotton blue (0.1 mg aniline blue dissolved in 60 g pure lactic acid), Melzer's reagent (1.5 g potassium iodide, 0.5 g crystalline iodine, 22 g chloral hydrate, aq. dest. 20) and 5% (5 g potassiumhydroxide, 100 mL water) potassiumhydroxide. Spores were measured from sections cut from the hymenial layer, in presenting spore size data, 5% of the measurements excluded from each end of the range are shown in parentheses, and spore measurements were made in Cotton Blue. The following abbreviations were used: KOH = 5% potassium hydroxide, CB = Cotton Blue, CB- = acyanophilous, IKI = Melzer's reagent, IKI- = both inamyloid and indextrinoid, L = mean spore length (arithmetic average for all spores), W = mean spore width (arithmetic average for all spores), Q = variation in the L/W ratios between the specimens studied, n (a/b) = number of spores (a) measured from given number (b) of specimens.

Cetyltrimethylammonium bromide (CTAB) rapid plant genome extraction kit-DN14 (Aidlab Biotechnologies Co., Ltd, Beijing) was used to obtain genomic DNA from dried specimens, according to the manufacturer's instructions with some modifications that a small piece of dried fungal specimen (about 30 mg) was ground to powder with liquid nitrogen. The powder was transferred to a 1.5 mL centrifuge tube, suspended in 0.4 mL of lysis buffer, and incubated at 65 °C in a water bath for 60 min. After that, 0.4 mL phenol-chloroform (24:1) was added to each tube and the suspension was shaken vigorously. After centrifugation at 13,000 rpm for 5 min, 0.3 mL of supernatant was transferred to a new tube and mixed with 0.45 mL of binding buffer. The mixture was then transferred to an adsorbing column (AC) for centrifugation at 13,000 rpm for 0.5 min. Then, 0.5 mL of inhibitor removal fluid was added in AC for a centrifugation at 12,000 rpm for 0.5 min. After washing twice with 0.5 mL of washing buffer, the AC was transferred to a clean centrifuge tube, and 100 mL elution buffer was added to the middle of adsorbed film to elute the genome DNA. The nuc rDNA ITS region was amplified with primer pair ITS5 and ITS4 (White, Bruns, Lee, & Taylor, 1990). The nuc rDNA LSU region was amplified with primer pair LR0R and LR7 (Rehner & Samuels, 1994; Vilgalys & Hester, 1990). The PCR procedure for ITS was as follows: initial denaturation at 95 °C for 3 min, followed by 35 cycles at 94 °C for 40 s, 58 °C for 45 s and 72 °C for 1 min, and a final extension at 72 °C for 10 min. The PCR procedure for LSU marked as follows: initial denaturation at 94 °C for 1 min, followed by 35 cycles at 94 °C for 30 s, 48 °C 1 min and 72 °C for 1.5 min, and a final extension at 72 °C for 10 min. The PCR products were purified and directly sequenced at Kunming Tsingke Biological Technology Limited Company. All newly generated sequences were deposited in GenBank (Table 1).

Table 1. List of species, specimens, and GenBank accession numbers of sequences used in this study.

Species name Sample no. GenBank accession no. References
ITS LSU
Bergerella atrofusca Berger 34240 MN902070 Lawrey et al. (2020)
Botryobasidium candicans GEL3083 AJ406440 unpublished
B. conspersum KHL11063 AY586657 Larsson et al. (2004)
B. subcoronatum FCUG1286 SWE AY647212 unpublished
Bryoclavula phycophila (Type) TNS-F-79667 LC508118 Masumoto & Degawa (2020)
Burgella lutea Etayo 27623 KC336075 Diederich et al. (2014)
Burgellopsis nivea (Type) ATCC MYA-4209 KC336077 Diederich et al. (2014)
Burgoa verzuoliana (Type) ATCC 24040 DQ915475 Lawrey et al. (2007)
Cantharellus alborufescens JLS880b KR677531 Olariaga et al. (2015)
C. ambohitantelyi (type) BB 08.336 KF294656 Buyck et al. (2014)
Ceratobasidium bulbillifaciens CBS 129339 KC336073 Diederich et al. (2014)
Clavulina cristata EL95_97 AY586648 Larsson et al. (2004)
C. livida MCCNNU140159 KT946799 He et al. (2016)
Hydnum albidum MB11-6024/2 AY293186 Binder et al. (2005)
H. crocidens PERTH08095981 KU612684 Feng et al. (2016)
H. elatum FRI62309 KU612691 Feng et al. (2016)
H. repandum KHL 8552 AF347095 Larsson et al. (2004)
Membranomyces delectabile KHL11147 AY586688 Larsson et al. (2004)
M. spurius Hjm 19169 KF218966 Kotiranta & Larsson (2013)
Minimedusa obcoronata F-082, 316 AY004068 Platas et al. (2001)
M. polyspora (Type) ATCC 24041 DQ915476 Lawrey et al. (2007)
Multiclavula corynoides Lutzoni 930804-2, DUKE U66440 Lutzoni (1997)
M. mucida AFTOL-ID 1130 AY885163 unpublished
Neoburgoa freyi isolate JL596-16 KX423755 Lawrey et al. (2016)
Platygloea disciformis AFTOL-ID 710 AY629314 unpublished
Rogersiomyces malaysianus LE-BIN 3507-10 KU820986 Psurtseva et al. (2016)
Sistotrema adnatum (Type) FCUG 700 DQ898699 Moncalvo et al. (2006)
S. alboluteum TAA167982 AY586713 Larsson et al. (2004)
S. alboluteum TAA 180259 AJ606042 Nilsson et al. (2006)
S. alboluteum MB6 KX358055 Stephenson et al. (2017)
S. albopallescens KHL11070 AM259210 Nilsson et al. (2006)
S. athelioides (Type) FCUG 701 DQ898700 Moncalvo et al. (2006)
S. biggsiae (Type) FCUG 782 DQ898697 Moncalvo et al. (2006)
S. brinkmannii FCUG 2198 DQ898705 Moncalvo et al. (2006)
S. brinkmannii FCUG 2055 DQ898706 Moncalvo et al. (2006)
S. brinkmannii FCUG 2217 DQ898709 Moncalvo et al. (2006)
S. brinkmannii aurim1111 JQ912675 Menkis et al. (2006)
S. chloroporum TUMH:64400 LC642058 Sugawara et al. (2022)
S. chloroporum TUMH:64396 LC642054 Sugawara et al. (2022)
S. citriforme KHL15898 KF218962 Kotiranta & Larsson (2013)
S. confluens PV174 AY586712 Larsson et al. (2004)
S. confluens FCUG 298 DQ898711 Moncalvo et al. (2006)
S. coroniferum KH Larsson s.n. KF218968 Kotiranta & Larsson (2013)
S. coroniferum Herbarium GB-BN-2 AM259215 Nilsson et al. (2006)
S. coronilla NH7598 AF506475 Larsson et al. (2004)
S. coronilla AFTOL-ID 618 DQ457641 Matheny et al. (2006)
S. farinaceum (Type) FCUG 659 DQ898707 Moncalvo et al. (2006)
S. flavorhizomorphae TUMH:64401 LC642059 Sugawara et al. (2022)
S. flavorhizomorphae TUMH:64402 LC642060 Sugawara et al. (2022)
S. hypogaeum CBS:393.63 MH869925 Vu et al. (2019)
S. hypogaeum (Type) CBS:394.63 MH869926 Vu et al. (2019)
S. luteoviride (Type) HK23176 KF218963 Kotiranta & Larsson (2013)
S. muscicola KHL8791 AF506474 Larsson & Larsson (2003)
S. muscicola KHL 11721 AJ606040 Nilsson et al. (2006)
S. oblongisporum KHL 14077 KF218970 Kotiranta & Larsson (2013)
S. oblongisporum KHL 11189 GQ162819 Kotiranta et al. (2011)
S. oblongisporum GEL2125 DQ898728 Moncalvo et al. (2006)
S. oblongisporum FCUG 1490 DQ898702 Moncalvo et al. (2006)
S. oblongisporum KHL 14077 KF218970 Kotiranta & Larsson (2013)
S. octosporum FCUG 2822 DQ898698 Moncalvo et al. (2006)
S. octosporum CBS:126038 MH875510 Vu et al. (2019)
S. pistilliferum EL 28/10 KF218964 Kotiranta & Larsson (2013)
S. raduloides LR 44004 KF218969 Kotiranta & Larsson (2013)
S. raduloides FCUG 1695 DQ898710 Moncalvo et al. (2006)
S. resinicystidium FCUG 2188 DQ898708 Moncalvo et al. (2006)
S. sernanderi CBS 926.70 AF518650 Hibbett & Binder (2002)
S. sernanderi FCUG1049 SWE AY647215 unpublished
S. subconfluens Dai 12578 JX076811 Zhou & Qin (2013)
S. subconfluens (Type) Dai 12577 JX076810 Zhou & Qin (2013)
S. yunnanense CLZhao 7341 (SWFC007341) ON817192 ON810360 Present study
S. yunnanense CLZhao 7355 (SWFC007355) ON817193 ON810361 Present study
S. yunnanense CLZhao 7395 (SWFC007395) ON817195 ON810363 Present study
S. yunnanense (Type) CLZhao 7357 (SWFC007357) ON817194 ON810362 Present study
Sistotremella perpusilla CBS:126048 MH875516 Vu et al. (2019)
Thanatephorus cucumeris AG8 AF354068 Gonzalez et al. (2001)
T. theobromae Sulawesi-10 HQ424242 Samuels et al. (2012)
Tilletiaria anomala AFTOL-ID 865 AY745715 unpublished
Tulasnella cystidiophora KW 2871 AY585831 Shefferson et al. (2005)
T. eremophila 13062MD KJ701189 Crous et al. (2015)
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DNA sequences were aligned in MAFFT 7 (https://mafft.cbrc.jp/alignment/server/) using the “G-INS-I” strategy for LSU, and manually adjusted in BioEdit (Hall, 1999). Tilletiaria anomala Bandoni & B.N. Johri and Platygloea disciformis (Fr.) Neuhoff were selected as an outgroup for LSU analysis based on previous study (Sugawara et al., 2022) (Fig. 1). The sequence alignment was deposited in TreeBASE (submission ID 29714).

Fig. 1 - Maximum Parsimony strict consensus tree showing the phylogeny of a new Sistotrema species and related species in Hydnaceae s.l. based on nuc rDNA LSU sequences. Branches are labelled with maximum likelihood bootstrap > 70%, parsimony bootstrap proportions > 50% and Bayesian posterior probabilities > 0.95, respectively.

Fig. 1 - Maximum Parsimony strict consensus tree showing the phylogeny of a new Sistotrema species and related species in Hydnaceae s.l. based on nuc rDNA LSU sequences. Branches are labelled with maximum likelihood bootstrap > 70%, parsimony bootstrap proportions > 50% and Bayesian posterior probabilities > 0.95, respectively.

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Maximum parsimony (MP) analyses were applied to the LSU dataset sequences. Approaches to phylogenetic analysis followed Zhao and Wu (2017), and the tree construction procedure was performed in PAUP* version 4.0b10 (Swofford, 2002). All characters were equally weighted and gaps were treated as missing data. Trees were inferred using the heuristic search option with TBR branch swapping and 1,000 random sequence additions. Max-trees were set to 5,000, branches of zero length were collapsed and all parsimonious trees were saved. Clade robustness was assessed using a bootstrap (BT) analysis with 1,000 replicates (Felsenstein, 1985). Descriptive tree statistics tree length (TL), consistency index (CI), retention index (RI), rescaled consistency index (RC), and homoplasy index (HI) were calculated for each MP tree generated. Datamatrix was also analyzed using Maximum Likelihood (ML) approach with RAxML-HPC2 through the Cipres Science Gateway (www.phylo.org; Miller et al., 2009). Branch support (BS) for ML analysis was determined by 1,000 bootstrap replicates.

MrModeltest 2.3 (Nylander, 2004) was used to determine the best-fit evolution model for each data set for Bayesian inference (BI). BI was calculated with MrBayes 3.1.2 with a general time reversible (GTR+I+G) model of DNA substitution and a gamma distribution rate variation across sites (Ronquist & Huelsenbeck, 2003). Four Markov chains were run for 2 runs from random starting trees for 640 thousand generations for LSU (Fig. 1), and trees were sampled every 100 generations. The first one-fourth generations were discarded as burn-in. A majority rule consensus tree of all remaining trees was calculated. Branches were considered as significantly supported if they received the maximum likelihood bootstrap (BS) >70%, the maximum parsimony bootstrap (BT) >50%, or Bayesian posterior probabilities (BPP) >0.95.

The LSU dataset included sequences from 75 fungal specimens representing 59 taxa. The dataset had an aligned length of 1,622 characters in the dataset, of which 689 characters were constant, 463 were variable and parsimony-uninformative, and 470 were parsimony-informative. MP analysis yielded one equally parsimonious tree (TL = 2,903, CI = 0.471, HI = 0.528, RI = 0.611, RC = 0.288). The best model for LSU estimated and applied in Bayesian analysis had the following characteristics: GTR+I+G, lset nst = 6, rates = invgamma; prset statefreqpr = dirichlet (1,1,1,1). Bayesian analysis resulted in a similar topology with an average standard deviation of split frequencies (BI). The effective sample size (ESS) across the two runs was twice that of the average ESS (avg ESS) = 255. The phylogeny (Fig. 1) inferred from the LSU sequences showed that S. yunnanense nested in the family Hydnaceae.

Sistotrema yunnanense L.Q. Cai & C.L. Zhao, sp. nov. Figs. 2, 3.

MycoBank no.: MB 844701.

Fig. 2 - Macroscopic features of Sistotrema yunnanense (SWFC 007357, holotype): basidiomata. Bars: A 1 cm; B 1 mm.

Fig. 2 - Macroscopic features of Sistotrema yunnanense (SWFC 007357, holotype): basidiomata. Bars: A 1 cm; B 1 mm.

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Fig. 3 - Microscopic features of Sistotrema yunnanense (SWFC 007357, holotype). A: Basidiospores. B: Basidia and basidioles. C: A part of the hymenial layer and subiculum. Bars: A 5 µm; B, C 10 µm.

Fig. 3 - Microscopic features of Sistotrema yunnanense (SWFC 007357, holotype). A: Basidiospores. B: Basidia and basidioles. C: A part of the hymenial layer and subiculum. Bars: A 5 µm; B, C 10 µm.

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Holotype: CHINA, Yunnan Province, Chuxiong, Zixishan National Forestry Park, E 101°24′, N 25°0′, alt. 1,950 m, on fallen branch of angiosperm, 2 Jul 2018, CLZhao 7357 (SWFC 007357). GenBank: LSU = ON810362, ITS = ON817194.

Etymology: Yunnanense (Lat.): referring to the province name of the type locality.

Basidiomata annual, resupinate, farinaceous to pruinose when fresh, becoming membranaceous upon drying, up to 11 cm long and 2 cm wide, 100-200 µm thick. Hymenial surface smooth, white when fresh, turning to pale cream upon drying, cracking with age. Margin narrow, slightly cream, fragile. Hyphal system monomitic; generative hyphae with clamp connections, colorless, thin- to slight thick-walled, branched, 2.5-5 µm in diam, frequently with oily contents, IKI-, CB-, tissues unchanged in KOH. Cystidia and cystidioles absent. Basidia suburniform to urniform, thin-walled, with four sterigmata and a basal clamp connection, with oily contents, 13.5-24 × 2.5-5.5 µm; basidioles abundant, in shape similar to basidia, but slightly smaller. Basidiospores subcylindrical to oblong ellipsoid, colorless, thin-walled, smooth, with oily contents, IKI-, CB-, (4-)4.5-6.5(-7) × (2.5-)3-4(-4.5) µm, L = 5.45 µm, W = 3.67 µm, Q = 1.43-1.51 (n = 120/4).

Type of rot: White rot.

Additional specimens examined (paratypes): CHINA, Yunnan Province, Chuxiong, Zixishan Forestry Park, E 101°24′, N 25°0′, alt. 1,950 m, on fallen branch of angiosperm, 2 Jul 2018, CLZhao 7355 (SWFC 007355), CLZhao 7341 (SWFC 007341), CLZhao 7395 (SWFC 007395).

In this study, a new species, Sistotrema yunnanense was described based on phylogenetic analyses and morphological characteristics.

The nuc rDNA LSU analysis showed that S. yunnanense belongs to Hydnaceae (Fig. 1) but not to Sistotrema s.s. clade (Sugawara et al., 2022), i.e., mycorrhizal lineage.

Morphologically, Sistotrema brinkmannii (Bres.) J. Erikss. differs from S. yunnanense by its rough, white to whitish gray hymenial surface having small aculei, and smaller basidiospores (3.4-4.6 × 1.9-3.0 µm; Dhingra, Priyanka, & Singh, 2009).

Sistotrema yunnanense is similar to S. diademiferum (Bourdot & Galzin) Donk and S. porulosum Hallenb in having farinaceous to pruinose hymenophores. However, S. diademiferum differs from S. yunnanense by its brownish-gray hymenial surface, thin-walled generative hyphae, and ellipsoid to ovoid, smaller basidiospores (3-5 × 2-3 µm; Kaur, Kaur, Singh, & Dhingra, 2018); S. porulosum differs in its smooth to porulose hymenophore with the grayish-white hymenial surface, basidia with 6-8 sterigmata, and narrowly ellipsoid to allantoid, smaller basidiospores (4-5 × 1.9-2.4 µm; Kaur et al., 2018).

Sistotrema yunnanense is similar to S. confluens Pers. and S. subconfluens L.W. Zhou in having similar morphological characteristics, namely, subcylindrical to oblong ellipsoid basidiospores. However, S. confluens differs from S. yunnanense by having brittle, tomentose hymenophore with the whitish to cream hymenial surface and narrower basidiospores (5-6 × 2-3 µm; Piątek & Cabała, 2002); S. subconfluens differs from S. yunnanense by having pileate basidiomata with buff to cinnamon buff hymenial surface and smaller basidiospores (3.9-4.2 × 2-2.3 µm; Zhou & Qin, 2013). Both species belongs to other linage “Sistotrema s.s.”.

Wood-rotting fungi are an extensively studied group of Basidiomycota (Núñez & Ryvarden, 2001; Dai, 2012; Ryvarden & Melo, 2014; Dai et al., 2015; Wu et al., 2020; Cao et al., 2021; Luo, Chen, & Zhao, 2022; Qu, Wang, & Zhao, 2022); however, the diversity of wood-rotting fungi in East Asia is remains poorly understood, especially in subtropical and tropical regions. Recently, many described taxa in this ecological group were recorded from these areas (Dai, 2012; Chen, Korhonen, Li, & Dai, 2014; Bian & Dai, 2015; Cui et al., 2019; Shen et al., 2019; Zhu, Song, Zhou, Si, & Cui, 2019; Sugawara et al., 2022), and our newly described taxon increases the number of corticioid fungal species in East Asia.

Disclosure

The authors declare no conflict of interest. All the experiments undertaken in this study comply with the current laws of the People's Republic of China.

Acknowledgements

The research was supported by the the National Natural Science Foundation of China (Project No. 32170004, U2102220), Yunnan Fundamental Research Project (Grant No. 202001AS070043), the High-level Talents Program of Yunnan Province (YNQR-QNRC-2018-111), the Science Foundation of Education Department of Yunnan Province (2023Y0724), and the Research Project of Key Laboratory of Forest Disaster Warning and Control in Universities of Yunnan Province (ZKJS-S-202208).

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