Fungi: What Have We Learned from Omics?

A special issue of Journal of Fungi (ISSN 2309-608X). This special issue belongs to the section "Fungal Genomics, Genetics and Molecular Biology".

Deadline for manuscript submissions: closed (31 August 2022) | Viewed by 34828

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Guest Editor
CESAM and Department of Biology, University of Aveiro, Campus Universitário de Santiago, 3810-193 Aveiro, Portugal
Interests: marine fungi; microbial interactions; proteomics; microbial enzymes
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Special Issue Information

Dear Colleagues,

Fungi have been long referred to as an understudied and under-understood group of organisms. Fungi are also described as being excellent producers of compounds with activities that can be used in numerous industries, from the food industry to agriculture and health industries. Last but definitely not least, some species are pathogenic to humans (luckily not that many), other animals, plants, and virtually to all eukaryotes.

Characterizing a fungus is still a challenge: fungi are diverse in nature, in lifestyles, and in terms of many other characteristics. The advent of omics—from genomics to metabolomics—brought many promises of elucidating the molecular mechanisms that govern fungi physiology. This Special Issue aims to reveal how and what omics have contributed to unravel the fungi complexity. We welcome research and review manuscripts in which omics are used to understand (but are not restricted to): fungal interactions with the environment/hosts, infection or biocontrol mechanisms, and molecular networks that govern the adaptation to new environments or the production of new compounds.

Dr. Ana Cristina Esteves
Guest Editor

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Keywords

  • fungi
  • genomics
  • transcriptomics
  • proteomics
  • metabolomics

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Published Papers (11 papers)

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Editorial

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3 pages, 204 KiB  
Editorial
Special Issue: “Fungi: What Have We Learned from Omics?”
by Ana Cristina Esteves
J. Fungi 2022, 8(11), 1145; https://doi.org/10.3390/jof8111145 - 28 Oct 2022
Viewed by 1544
Abstract
Fungi are vast in terms of diversity, ecological roles, habitats they occupy, physiology, metabolism, and in many other characteristics [...] Full article
(This article belongs to the Special Issue Fungi: What Have We Learned from Omics?)

Research

Jump to: Editorial, Review

26 pages, 2193 KiB  
Article
Unveiling the Secretome of the Fungal Plant Pathogen Neofusicoccum parvum Induced by In Vitro Host Mimicry
by Forough Nazar Pour, Bruna Pedrosa, Micaela Oliveira, Cátia Fidalgo, Bart Devreese, Gonzalez Van Driessche, Carina Félix, Nuno Rosa, Artur Alves, Ana Sofia Duarte and Ana Cristina Esteves
J. Fungi 2022, 8(9), 971; https://doi.org/10.3390/jof8090971 - 17 Sep 2022
Cited by 15 | Viewed by 3656
Abstract
Neofusicoccum parvum is a fungal plant pathogen of a wide range of hosts but knowledge about the virulence factors of N. parvum and host–pathogen interactions is rather limited. The molecules involved in the interaction between N. parvum and Eucalyptus are mostly unknown, so [...] Read more.
Neofusicoccum parvum is a fungal plant pathogen of a wide range of hosts but knowledge about the virulence factors of N. parvum and host–pathogen interactions is rather limited. The molecules involved in the interaction between N. parvum and Eucalyptus are mostly unknown, so we used a multi-omics approach to understand pathogen–host interactions. We present the first comprehensive characterization of the in vitro secretome of N. parvum and a prediction of protein–protein interactions using a dry-lab non-targeted interactomics strategy. We used LC-MS to identify N. parvum protein profiles, resulting in the identification of over 400 proteins, from which 117 had a different abundance in the presence of the Eucalyptus stem. Most of the more abundant proteins under host mimicry are involved in plant cell wall degradation (targeting pectin and hemicellulose) consistent with pathogen growth on a plant host. Other proteins identified are involved in adhesion to host tissues, penetration, pathogenesis, or reactive oxygen species generation, involving ribonuclease/ribotoxin domains, putative ricin B lectins, and necrosis elicitors. The overexpression of chitosan synthesis proteins during interaction with the Eucalyptus stem reinforces the hypothesis of an infection strategy involving pathogen masking to avoid host defenses. Neofusicoccum parvum has the molecular apparatus to colonize the host but also actively feed on its living cells and induce necrosis suggesting that this species has a hemibiotrophic lifestyle. Full article
(This article belongs to the Special Issue Fungi: What Have We Learned from Omics?)
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15 pages, 5269 KiB  
Article
Comparative Proteomics Study on the Postharvest Senescence of Volvariella volvacea
by Lei Zha, Mingjie Chen, Qian Guo, Zongjun Tong, Zhengpeng Li, Changxia Yu, Huanling Yang and Yan Zhao
J. Fungi 2022, 8(8), 819; https://doi.org/10.3390/jof8080819 - 4 Aug 2022
Cited by 6 | Viewed by 2114
Abstract
Volvariella volvacea is difficult to store after harvest, which restricts the production and circulation of V. volvacea fruiting bodies. Low-temperature storage is the traditional storage method used for most edible fungi. However, V. volvacea undergoes autolysis at low temperatures. When fruiting bodies are [...] Read more.
Volvariella volvacea is difficult to store after harvest, which restricts the production and circulation of V. volvacea fruiting bodies. Low-temperature storage is the traditional storage method used for most edible fungi. However, V. volvacea undergoes autolysis at low temperatures. When fruiting bodies are stored at 15 °C (suitable temperature), V. volvacea achieves the best fresh-keeping effect. However, the molecular mechanism underlying the postharvest senescence of V. volvacea remains unclear. Based on this information, we stored V. volvacea fruiting bodies at 15 °C after harvest and then analyzed the texture and phenotype combined with the results of previous physiological research. Four time points (0, 24, 60, and 96 h) were selected for the comparative proteomics study of V. volvacea during storage at 15 °C. A variety of proteins showed differential expressions in postharvest V. volvacea at 15 °C. Further comparison of the gene ontology (GO) enrichment analysis and KEGG pathways performed at different sampling points revealed proteins that were significantly enriched at several time points. At the same time, we also analyzed differentially expressed proteins (DEPs) related to the RNA transport, fatty acid biosynthesis and metabolism, and amino acid biosynthesis and metabolism pathways, and discussed the molecular functions of the PAB1, RPG1, ACC1, ADH3, ADH2, ALD5, and SDH2 proteins in postharvest V. volvacea senescence. Our results showed that many biological processes of the postharvest senescence of V. volvacea changed. Most importantly, we found that most RNA transport-related proteins were down-regulated, which may lead to a decrease in related gene regulation. Our results also showed that the expression of other important proteins, such as the fatty acid metabolism related proteins increased; and changes in fatty acid composition affected the cell membrane, which may accelerate the ripening and perception of V. volvacea fruiting bodies. Therefore, our research provides a reference for further studies on the aging mechanism of V. volvacea. Full article
(This article belongs to the Special Issue Fungi: What Have We Learned from Omics?)
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20 pages, 19098 KiB  
Article
AGC/AKT Protein Kinase SCH9 Is Critical to Pathogenic Development and Overwintering Survival in Magnaporthe oryzae
by Wajjiha Batool, Chang Liu, Xiaoning Fan, Penghui Zhang, Yan Hu, Yi Wei and Shi-Hong Zhang
J. Fungi 2022, 8(8), 810; https://doi.org/10.3390/jof8080810 - 31 Jul 2022
Cited by 6 | Viewed by 2400
Abstract
Primary inoculum that survives overwintering is one of the key factors that determine the outbreak of plant disease. Pathogenic resting structures, such as chlamydospores, are an ideal inoculum for plant disease. Puzzlingly, Magnaporthe oryzae, a devastating fungal pathogen responsible for blast disease [...] Read more.
Primary inoculum that survives overwintering is one of the key factors that determine the outbreak of plant disease. Pathogenic resting structures, such as chlamydospores, are an ideal inoculum for plant disease. Puzzlingly, Magnaporthe oryzae, a devastating fungal pathogen responsible for blast disease in rice, hardly form any morphologically changed resting structures, and we hypothesize that M. oryzae mainly relies on its physiological alteration to survive overwintering or other harsh environments. However, little progress on research into regulatory genes that facilitate the overwintering of rice blast pathogens has been made so far. Serine threonine protein kinase AGC/AKT, MoSch9, plays an important role in the spore-mediated pathogenesis of M. oryzae. Building on this finding, we discovered that in genetic and biological terms, MoSch9 plays a critical role in conidiophore stalk formation, hyphal-mediated pathogenesis, cold stress tolerance, and overwintering survival of M. oryzae. We discovered that the formation of conidiophore stalks and disease propagation using spores was severely compromised in the mutant strains, whereas hyphal-mediated pathogenesis and the root infection capability of M. oryzae were completely eradicated due to MoSch9 deleted mutants’ inability to form an appressorium-like structure. Most importantly, the functional and transcriptomic study of wild-type and MoSch9 mutant strains showed that MoSch9 plays a regulatory role in cold stress tolerance of M. oryzae through the transcription regulation of secondary metabolite synthesis, ATP hydrolyzing, and cell wall integrity proteins during osmotic stress and cold temperatures. From these results, we conclude that MoSch9 is essential for fungal infection-related morphogenesis and overwintering of M. oryzae. Full article
(This article belongs to the Special Issue Fungi: What Have We Learned from Omics?)
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20 pages, 2799 KiB  
Article
Unveiling the Core Effector Proteins of Oil Palm Pathogen Ganoderma boninense via Pan-Secretome Analysis
by Mohamad Hazwan Fikri Khairi, Nor Azlan Nor Muhammad, Hamidun Bunawan, Abdul Munir Abdul Murad and Ahmad Bazli Ramzi
J. Fungi 2022, 8(8), 793; https://doi.org/10.3390/jof8080793 - 29 Jul 2022
Cited by 7 | Viewed by 2658
Abstract
Ganoderma boninense is the major causal agent of basal stem rot (BSR) disease in oil palm, causing the progressive rot of the basal part of the stem. Despite its prominence, the key pathogenicity determinants for the aggressive nature of hemibiotrophic infection remain unknown. [...] Read more.
Ganoderma boninense is the major causal agent of basal stem rot (BSR) disease in oil palm, causing the progressive rot of the basal part of the stem. Despite its prominence, the key pathogenicity determinants for the aggressive nature of hemibiotrophic infection remain unknown. In this study, genome sequencing and the annotation of G. boninense T10 were carried out using the Illumina sequencing platform, and comparative genome analysis was performed with previously reported G. boninense strains (NJ3 and G3). The pan-secretome of G. boninense was constructed and comprised 937 core orthogroups, 243 accessory orthogroups, and 84 strain-specific orthogroups. In total, 320 core orthogroups were enriched with candidate effector proteins (CEPs) that could be classified as carbohydrate-active enzymes, hydrolases, and non-catalytic proteins. Differential expression analysis revealed an upregulation of five CEP genes that was linked to the suppression of PTI signaling cascade, while the downregulation of four CEP genes was linked to the inhibition of PTI by preventing host defense elicitation. Genome architecture analysis revealed the one-speed architecture of the G. boninense genome and the lack of preferential association of CEP genes to transposable elements. The findings obtained from this study aid in the characterization of pathogenicity determinants and molecular biomarkers of BSR disease. Full article
(This article belongs to the Special Issue Fungi: What Have We Learned from Omics?)
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17 pages, 1369 KiB  
Article
Metabolomics Analysis and Antioxidant Potential of Endophytic Diaporthe fraxini ED2 Grown in Different Culture Media
by Wen-Nee Tan, Kashvintha Nagarajan, Vuanghao Lim, Juzaili Azizi, Kooi-Yeong Khaw, Woei-Yenn Tong, Chean-Ring Leong and Nelson Jeng-Yeou Chear
J. Fungi 2022, 8(5), 519; https://doi.org/10.3390/jof8050519 - 18 May 2022
Cited by 13 | Viewed by 2787
Abstract
Endophytic fungi are a promising source of bioactive metabolites with a wide range of pharmacological activities. In the present study, MS-based metabolomics was conducted to study the metabolomes variations of endophytic Diaporthe fraxini ED2 grown in different culture media. Total phenolic content (TPC), [...] Read more.
Endophytic fungi are a promising source of bioactive metabolites with a wide range of pharmacological activities. In the present study, MS-based metabolomics was conducted to study the metabolomes variations of endophytic Diaporthe fraxini ED2 grown in different culture media. Total phenolic content (TPC), total flavonoid content (TFC), 2,2-diphenyl-1-picrylhydrazyl (DPPH) radical scavenging, 2,2-azinobis(3-ethylbenzothiazoline-6-sulfonic acid (ABTS), and ferric reducing antioxidant power (FRAP) assays were conducted to assess the antioxidant potential of the fungal extracts. Multivariate data analysis (MVDA) was employed in data analysis and interpretation to elucidate the complex metabolite profile. The supplemented culture medium of D. fraxini fungal extract stimulated the production of metabolites not occurring in the normal culture medium. Antioxidant activity studies revealed the potential of supplemented cultured fungal extract of D. fraxini as a source of antioxidants. The present findings highlight that fungal culture medium supplementation is an effective approach to unravelling the hidden metabolome in plant-associated fungal diversity. Full article
(This article belongs to the Special Issue Fungi: What Have We Learned from Omics?)
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11 pages, 1099 KiB  
Communication
Differential Gene Expression of Mucor lusitanicus under Aerobic and Anaerobic Conditions
by Mónika Homa, Sandugash Ibragimova, Csilla Szebenyi, Gábor Nagy, Nóra Zsindely, László Bodai, Csaba Vágvölgyi, Gábor Nagy and Tamás Papp
J. Fungi 2022, 8(4), 404; https://doi.org/10.3390/jof8040404 - 15 Apr 2022
Cited by 5 | Viewed by 2628
Abstract
Mucor lusitanicus and some other members of the fungal order Mucorales display the phenomenon of morphological dimorphism. This means that these fungi aerobically produce filamentous hyphae, developing a coenocytic mycelium, but they grow in a multipolar yeast-like form under anaerobiosis. Revealing the molecular [...] Read more.
Mucor lusitanicus and some other members of the fungal order Mucorales display the phenomenon of morphological dimorphism. This means that these fungi aerobically produce filamentous hyphae, developing a coenocytic mycelium, but they grow in a multipolar yeast-like form under anaerobiosis. Revealing the molecular mechanism of the reversible yeast-hyphal transition can be interesting for both the biotechnological application and in the understanding of the pathomechanism of mucormycosis. In the present study, transcriptomic analyses were carried out after cultivating the fungus either aerobically or anaerobically revealing significant changes in gene expression under the two conditions. In total, 539 differentially expressed genes (FDR < 0.05, |log2FC| ≥ 3) were identified, including 190 upregulated and 349 downregulated transcripts. Within the metabolism-related genes, carbohydrate metabolism was proven to be especially affected. Anaerobiosis also affected the transcription of transporters: among the 14 up- and 42 downregulated transporters, several putative sugar transporters were detected. Moreover, a considerable number of transcripts related to amino acid transport and metabolism, lipid transport and metabolism, and energy production and conversion were proven to be downregulated when the culture had been transferred into an anaerobic atmosphere. Full article
(This article belongs to the Special Issue Fungi: What Have We Learned from Omics?)
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25 pages, 4995 KiB  
Article
A Comprehensive Assessment of the Secretome Responsible for Host Adaptation of the Legume Root Pathogen Aphanomyces euteiches
by Andrei Kiselev, Hélène San Clemente, Laurent Camborde, Bernard Dumas and Elodie Gaulin
J. Fungi 2022, 8(1), 88; https://doi.org/10.3390/jof8010088 - 17 Jan 2022
Cited by 5 | Viewed by 3972
Abstract
The soil-borne oomycete pathogen Aphanomyces euteiches causes devastating root rot diseases in legumes such as pea and alfalfa. The different pathotypes of A. euteiches have been shown to exhibit differential quantitative virulence, but the molecular basis of host adaptation has not yet been [...] Read more.
The soil-borne oomycete pathogen Aphanomyces euteiches causes devastating root rot diseases in legumes such as pea and alfalfa. The different pathotypes of A. euteiches have been shown to exhibit differential quantitative virulence, but the molecular basis of host adaptation has not yet been clarified. Here, we re-sequenced a pea field reference strain of A. euteiches ATCC201684 with PacBio long-reads and took advantage of the technology to generate the mitochondrial genome. We identified that the secretome of A. euteiches is characterized by a large portfolio of secreted proteases and carbohydrate-active enzymes (CAZymes). We performed Illumina sequencing of four strains of A. euteiches with contrasted specificity to pea or alfalfa and found in different geographical areas. Comparative analysis showed that the core secretome is largely represented by CAZymes and proteases. The specific secretome is mainly composed of a large set of small, secreted proteins (SSP) without any predicted functional domain, suggesting that the legume preference of the pathogen is probably associated with unknown functions. This study forms the basis for further investigations into the mechanisms of interaction of A. euteiches with legumes. Full article
(This article belongs to the Special Issue Fungi: What Have We Learned from Omics?)
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Graphical abstract

20 pages, 1765 KiB  
Article
Genomic and Metabolomic Analyses of the Marine Fungus Emericellopsis cladophorae: Insights into Saltwater Adaptability Mechanisms and Its Biosynthetic Potential
by Micael F. M. Gonçalves, Sandra Hilário, Yves Van de Peer, Ana C. Esteves and Artur Alves
J. Fungi 2022, 8(1), 31; https://doi.org/10.3390/jof8010031 - 30 Dec 2021
Cited by 21 | Viewed by 4270
Abstract
The genus Emericellopsis is found in terrestrial, but mainly in marine, environments with a worldwide distribution. Although Emericellopsis has been recognized as an important source of bioactive compounds, the range of metabolites expressed by the species of this genus, as well as the [...] Read more.
The genus Emericellopsis is found in terrestrial, but mainly in marine, environments with a worldwide distribution. Although Emericellopsis has been recognized as an important source of bioactive compounds, the range of metabolites expressed by the species of this genus, as well as the genes involved in their production are still poorly known. Untargeted metabolomics, using UPLC- QToF–MS/MS, and genome sequencing (Illumina HiSeq) was performed to unlock E. cladophorae MUM 19.33 chemical diversity. The genome of E. cladophorae is 26.9 Mb and encodes 8572 genes. A large set of genes encoding carbohydrate-active enzymes (CAZymes), secreted proteins, transporters, and secondary metabolite biosynthetic gene clusters were identified. Our analysis also revealed genomic signatures that may reflect a certain fungal adaptability to the marine environment, such as genes encoding for (1) the high-osmolarity glycerol pathway; (2) osmolytes’ biosynthetic processes; (3) ion transport systems, and (4) CAZymes classes allowing the utilization of marine polysaccharides. The fungal crude extract library constructed revealed a promising source of antifungal (e.g., 9,12,13-Trihydroxyoctadec-10-enoic acid, hymeglusin), antibacterial (e.g., NovobiocinA), anticancer (e.g., daunomycinone, isoreserpin, flavopiridol), and anti-inflammatory (e.g., 2’-O-Galloylhyperin) metabolites. We also detected unknown compounds with no structural match in the databases used. The metabolites’ profiles of E. cladophorae MUM 19.33 fermentations were salt dependent. The results of this study contribute to unravel aspects of the biology and ecology of this marine fungus. The genome and metabolome data are relevant for future biotechnological exploitation of the species. Full article
(This article belongs to the Special Issue Fungi: What Have We Learned from Omics?)
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22 pages, 21133 KiB  
Article
Comparative Genomics and Gene Pool Analysis Reveal the Decrease of Genome Diversity and Gene Number in Rice Blast Fungi by Stable Adaption with Rice
by Qi Wu, Yi Wang, Li-Na Liu, Kai Shi and Cheng-Yun Li
J. Fungi 2022, 8(1), 5; https://doi.org/10.3390/jof8010005 - 22 Dec 2021
Cited by 5 | Viewed by 3415
Abstract
Magnaporthe oryzae caused huge losses in rice and wheat production worldwide. Comparing to long-term co-evolution history with rice, wheat-infecting isolates were new-emerging. To reveal the genetic differences between rice and wheat blast on global genomic scale, 109 whole-genome sequences of M. oryzae from [...] Read more.
Magnaporthe oryzae caused huge losses in rice and wheat production worldwide. Comparing to long-term co-evolution history with rice, wheat-infecting isolates were new-emerging. To reveal the genetic differences between rice and wheat blast on global genomic scale, 109 whole-genome sequences of M. oryzae from rice, wheat, and other hosts were reanalyzed in this study. We found that the rice lineage had gone through stronger selective sweep and fewer conserved genes than those of Triticum and Lolium lineages, which indicated that rice blast fungi adapted to rice by gene loss and rapid evolution of specific loci. Furthermore, 228 genes associated with host adaptation of M. oryzae were found by presence/absence variation (PAV) analyses. The functional annotation of these genes found that the fine turning of genes gain/loss involved with transport and transcription factor, thiol metabolism, and nucleotide metabolism respectively are major mechanisms for rice adaption. This result implies that genetic base of specific host plant may lead to gene gain/loss variation of pathogens, so as to enhance their adaptability to host. Further characterization of these specific loci and their roles in adaption and evaluation of the fungi may eventually lead to understanding of interaction mechanism and develop new strategies of the disease management. Full article
(This article belongs to the Special Issue Fungi: What Have We Learned from Omics?)
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Review

Jump to: Editorial, Research

16 pages, 672 KiB  
Review
Application of Metabolomics in the Study of Starvation-Induced Autophagy in Saccharomyces cerevisiae: A Scoping Review
by Muhammad Luqman Nasaruddin and Khaizurin Tajul Arifin
J. Fungi 2021, 7(11), 987; https://doi.org/10.3390/jof7110987 - 19 Nov 2021
Cited by 2 | Viewed by 3061
Abstract
This scoping review is aimed at the application of the metabolomics platform to dissect key metabolites and their intermediates to observe the regulatory mechanisms of starvation-induced autophagy in Saccharomyces cerevisiae. Four research papers were shortlisted in this review following the inclusion and [...] Read more.
This scoping review is aimed at the application of the metabolomics platform to dissect key metabolites and their intermediates to observe the regulatory mechanisms of starvation-induced autophagy in Saccharomyces cerevisiae. Four research papers were shortlisted in this review following the inclusion and exclusion criteria. We observed a commonly shared pathway undertaken by S. cerevisiae under nutritional stress. Targeted and untargeted metabolomics was applied in either of these studies using varying platforms resulting in the annotation of several different observable metabolites. We saw a commonly shared pathway undertaken by S. cerevisiae under nutritional stress. Following nitrogen starvation, the concentration of cellular nucleosides was altered as a result of autophagic RNA degradation. Additionally, it is also found that autophagy replenishes amino acid pools to sustain macromolecule synthesis. Furthermore, in glucose starvation, nucleosides were broken down into carbonaceous metabolites that are being funneled into the non-oxidative pentose phosphate pathway. The ribose salvage allows for the survival of starved yeast. Moreover, acute glucose starvation showed autophagy to be involved in maintaining ATP/energy levels. We highlighted the practicality of metabolomics as a tool to better understand the underlying mechanisms involved to maintain homeostasis by recycling degradative products to ensure the survival of S. cerevisiae under starvation. The application of metabolomics has extended the scope of autophagy and provided newer intervention targets against cancer as well as neurodegenerative diseases in which autophagy is implicated. Full article
(This article belongs to the Special Issue Fungi: What Have We Learned from Omics?)
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