Metagenomics of black grains: new highlights in the understanding of eumycetoma.


Journal

Transactions of the Royal Society of Tropical Medicine and Hygiene
ISSN: 1878-3503
Titre abrégé: Trans R Soc Trop Med Hyg
Pays: England
ID NLM: 7506129

Informations de publication

Date de publication:
14 04 2021
Historique:
received: 18 09 2020
revised: 19 11 2020
accepted: 16 12 2020
pubmed: 16 1 2021
medline: 25 6 2021
entrez: 15 1 2021
Statut: ppublish

Résumé

Eumycetoma is a chronic subcutaneous granulomatous disease that is endemic in Sudan and other countries. It can be caused by eight different fungal orders. The gold standard diagnostic test is culture, however, culture-independent methods such as imaging, histopathological and molecular techniques can support diagnosis, especially in cases of negative cultures. The amplicon-based internal transcribed spacer 2 metagenomic technique was used to study black grains isolated from 14 tissue biopsies from patients with mycetoma. Furthermore, mycological culture and surgical biopsy histopathological examinations of grains were performed. Madurella mycetomatis (n=5) and Falciformispora spp. (n=4) organisms were identified by culture and confirmed by metagenomics. Metagenomics recognised, at the species level, Falciformispora as Falciformispora tompkinsii (n=3) and Falciformispora senegalensis (n=1), while in culture-negative cases (n=5), Madurella mycetomatis (n=3), Falciformispora senegalensis (n=1) and Fusarium spp. (n=1) were identified. Interestingly, the metagenomics results showed a 'consortium' of different fungi in each sample, mainly Ascomycota phylum, including various species associated with eumycetoma. The microbial co-occurrence in eumycetoma showed the co-presence of Madurella with Trichoderma, Chaetomium, Malasseziales and Sordariales spp., while Falciformispora co-presented with Inocybe and Alternaria and was in mutual exclusion with Subramaniula, Aspergillus and Trichothecium. Metagenomics provides new insights into the aetiology of eumycetoma in samples with negative culture and into the diversity and complexity of grains mycobiota, calling into question the accuracy of traditional culture for the identification of causative agents.

Sections du résumé

BACKGROUND
Eumycetoma is a chronic subcutaneous granulomatous disease that is endemic in Sudan and other countries. It can be caused by eight different fungal orders. The gold standard diagnostic test is culture, however, culture-independent methods such as imaging, histopathological and molecular techniques can support diagnosis, especially in cases of negative cultures.
METHODS
The amplicon-based internal transcribed spacer 2 metagenomic technique was used to study black grains isolated from 14 tissue biopsies from patients with mycetoma. Furthermore, mycological culture and surgical biopsy histopathological examinations of grains were performed.
RESULTS
Madurella mycetomatis (n=5) and Falciformispora spp. (n=4) organisms were identified by culture and confirmed by metagenomics. Metagenomics recognised, at the species level, Falciformispora as Falciformispora tompkinsii (n=3) and Falciformispora senegalensis (n=1), while in culture-negative cases (n=5), Madurella mycetomatis (n=3), Falciformispora senegalensis (n=1) and Fusarium spp. (n=1) were identified. Interestingly, the metagenomics results showed a 'consortium' of different fungi in each sample, mainly Ascomycota phylum, including various species associated with eumycetoma. The microbial co-occurrence in eumycetoma showed the co-presence of Madurella with Trichoderma, Chaetomium, Malasseziales and Sordariales spp., while Falciformispora co-presented with Inocybe and Alternaria and was in mutual exclusion with Subramaniula, Aspergillus and Trichothecium.
CONCLUSION
Metagenomics provides new insights into the aetiology of eumycetoma in samples with negative culture and into the diversity and complexity of grains mycobiota, calling into question the accuracy of traditional culture for the identification of causative agents.

Identifiants

pubmed: 33449116
pii: 6101237
doi: 10.1093/trstmh/traa177
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

307-314

Informations de copyright

© The Author(s) 2021. Published by Oxford University Press on behalf of Royal Society of Tropical Medicine and Hygiene.

Auteurs

Antonella Santona (A)

Department of Biomedical Sciences, University of Sassari, Viale San Pietro 43b, 07100 Sassari, Italy.

Najwa A Mhmoud (NA)

Mycetoma Research Centre, University of Khartoum, PO Box 102, Khartoum, Sudan.
Faculty of Medical Laboratory Sciences, University of Khartoum, Khartoum, Sudan.

Emmanuel Edwar Siddig (EE)

Mycetoma Research Centre, University of Khartoum, PO Box 102, Khartoum, Sudan.
Faculty of Medical Laboratory Sciences, University of Khartoum, Khartoum, Sudan.

Massimo Deligios (M)

Department of Biomedical Sciences, University of Sassari, Viale San Pietro 43b, 07100 Sassari, Italy.

Maura Fiamma (M)

Department of Biomedical Sciences, University of Sassari, Viale San Pietro 43b, 07100 Sassari, Italy.

Sahar Mubarak Bakhiet (SM)

Mycetoma Research Centre, University of Khartoum, PO Box 102, Khartoum, Sudan.
Institute for Endemic Diseases, University of Khartoum, PO Box 102, Khartoum, Sudan.

Aleksandra Barac (A)

Clinic for Infectious and Tropical Diseases, Clinical Centre of Serbia, Bu. Oslobodjenja 16, 11000 Belgrade, Serbia.
Faculty of Medicine, University of Belgrade, Dr Subotica 1, 11000 Belgrade, Serbia.

Bianca Paglietti (B)

Department of Biomedical Sciences, University of Sassari, Viale San Pietro 43b, 07100 Sassari, Italy.

Salvatore Rubino (S)

Department of Biomedical Sciences, University of Sassari, Viale San Pietro 43b, 07100 Sassari, Italy.

Ahmed Hassan Fahal (AH)

Mycetoma Research Centre, University of Khartoum, PO Box 102, Khartoum, Sudan.

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