Analysis of a Food-Borne Fungal Pathogen Outbreak: Virulence and Genome of a <italic toggle="yes">Mucor circinelloides</italic> Isolate from Yogurt

ABSTRACT Food-borne pathogens are ongoing problems, and new pathogens are emerging. The impact of fungi, however, is largely underestimated. Recently, commercial yogurts contaminated with Mucor circinelloides were sold, and >200 consumers became ill with nausea, vomiting, and diarrhea. Mucoralean...

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Autores principales:	Soo Chan Lee, R. Blake Billmyre, Alicia Li, Sandra Carson, Sean M. Sykes, Eun Young Huh, Piotr Mieczkowski, Dennis C. Ko, Christina A. Cuomo, Joseph Heitman
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Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/4f1204adec92496ba0ae8d20a168ae86
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spelling	oai:doaj.org-article:4f1204adec92496ba0ae8d20a168ae862021-11-15T15:47:22ZAnalysis of a Food-Borne Fungal Pathogen Outbreak: Virulence and Genome of a <italic toggle="yes">Mucor circinelloides</italic> Isolate from Yogurt10.1128/mBio.01390-142150-7511https://doaj.org/article/4f1204adec92496ba0ae8d20a168ae862014-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01390-14https://doaj.org/toc/2150-7511ABSTRACT Food-borne pathogens are ongoing problems, and new pathogens are emerging. The impact of fungi, however, is largely underestimated. Recently, commercial yogurts contaminated with Mucor circinelloides were sold, and >200 consumers became ill with nausea, vomiting, and diarrhea. Mucoralean fungi cause the fatal fungal infection mucormycosis, whose incidence has been continuously increasing. In this study, we isolated an M. circinelloides strain from a yogurt container, and multilocus sequence typing identified the strain as Mucor circinelloides f. circinelloides. M. circinelloides f. circinelloides is the most virulent M. circinelloides subspecies and is commonly associated with human infections, whereas M. circinelloides f. lusitanicus and M. circinelloides f. griseocyanus are less common causes of infection. Whole-genome analysis of the yogurt isolate confirmed it as being close to the M. circinelloides f. circinelloides subgroup, with a higher percentage of divergence with the M. circinelloides f. lusitanicus subgroup. In mating assays, the yogurt isolate formed sexual zygospores with the (−) M. circinelloides f. circinelloides tester strain, which is congruent with its sex locus encoding SexP, the (+) mating type sex determinant. The yogurt isolate was virulent in murine and wax moth larva host systems. In a murine gastromucormycosis model, Mucor was recovered from fecal samples of infected mice for up to 10 days, indicating that Mucor can survive transit through the GI tract. In interactions with human immune cells, M. circinelloides f. lusitanicus induced proinflammatory cytokines but M. circinelloides f. circinelloides did not, which may explain the different levels of virulence in mammalian hosts. This study demonstrates that M. circinelloides can spoil food products and cause gastrointestinal illness in consumers and may pose a particular risk to immunocompromised patients. IMPORTANCE The U.S. FDA reported that yogurt products were contaminated with M. circinelloides, a mucoralean fungal pathogen, and >200 consumers complained of symptoms, including vomiting, nausea, and diarrhea. The manufacturer voluntarily withdrew the affected yogurt products from the market. Compared to other food-borne pathogens, including bacteria, viruses, and parasites, less focus has been placed on the risk of fungal pathogens. This study evaluates the potential risk from the food-borne fungal pathogen M. circinelloides that was isolated from the contaminated commercial yogurt. We successfully cultured an M. circinelloides isolate and found that the isolate belongs to the species M. circinelloides f. circinelloides, which is often associated with human infections. In murine and insect host models, the isolate was virulent. While information disseminated in the popular press would suggest this fungal contaminant poses little or no risk to consumers, our results show instead that it is capable of causing significant infections in animals.Soo Chan LeeR. Blake BillmyreAlicia LiSandra CarsonSean M. SykesEun Young HuhPiotr MieczkowskiDennis C. KoChristina A. CuomoJoseph HeitmanAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 4 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Soo Chan Lee R. Blake Billmyre Alicia Li Sandra Carson Sean M. Sykes Eun Young Huh Piotr Mieczkowski Dennis C. Ko Christina A. Cuomo Joseph Heitman Analysis of a Food-Borne Fungal Pathogen Outbreak: Virulence and Genome of a <italic toggle="yes">Mucor circinelloides</italic> Isolate from Yogurt
description	ABSTRACT Food-borne pathogens are ongoing problems, and new pathogens are emerging. The impact of fungi, however, is largely underestimated. Recently, commercial yogurts contaminated with Mucor circinelloides were sold, and >200 consumers became ill with nausea, vomiting, and diarrhea. Mucoralean fungi cause the fatal fungal infection mucormycosis, whose incidence has been continuously increasing. In this study, we isolated an M. circinelloides strain from a yogurt container, and multilocus sequence typing identified the strain as Mucor circinelloides f. circinelloides. M. circinelloides f. circinelloides is the most virulent M. circinelloides subspecies and is commonly associated with human infections, whereas M. circinelloides f. lusitanicus and M. circinelloides f. griseocyanus are less common causes of infection. Whole-genome analysis of the yogurt isolate confirmed it as being close to the M. circinelloides f. circinelloides subgroup, with a higher percentage of divergence with the M. circinelloides f. lusitanicus subgroup. In mating assays, the yogurt isolate formed sexual zygospores with the (−) M. circinelloides f. circinelloides tester strain, which is congruent with its sex locus encoding SexP, the (+) mating type sex determinant. The yogurt isolate was virulent in murine and wax moth larva host systems. In a murine gastromucormycosis model, Mucor was recovered from fecal samples of infected mice for up to 10 days, indicating that Mucor can survive transit through the GI tract. In interactions with human immune cells, M. circinelloides f. lusitanicus induced proinflammatory cytokines but M. circinelloides f. circinelloides did not, which may explain the different levels of virulence in mammalian hosts. This study demonstrates that M. circinelloides can spoil food products and cause gastrointestinal illness in consumers and may pose a particular risk to immunocompromised patients. IMPORTANCE The U.S. FDA reported that yogurt products were contaminated with M. circinelloides, a mucoralean fungal pathogen, and >200 consumers complained of symptoms, including vomiting, nausea, and diarrhea. The manufacturer voluntarily withdrew the affected yogurt products from the market. Compared to other food-borne pathogens, including bacteria, viruses, and parasites, less focus has been placed on the risk of fungal pathogens. This study evaluates the potential risk from the food-borne fungal pathogen M. circinelloides that was isolated from the contaminated commercial yogurt. We successfully cultured an M. circinelloides isolate and found that the isolate belongs to the species M. circinelloides f. circinelloides, which is often associated with human infections. In murine and insect host models, the isolate was virulent. While information disseminated in the popular press would suggest this fungal contaminant poses little or no risk to consumers, our results show instead that it is capable of causing significant infections in animals.
format	article
author	Soo Chan Lee R. Blake Billmyre Alicia Li Sandra Carson Sean M. Sykes Eun Young Huh Piotr Mieczkowski Dennis C. Ko Christina A. Cuomo Joseph Heitman
author_facet	Soo Chan Lee R. Blake Billmyre Alicia Li Sandra Carson Sean M. Sykes Eun Young Huh Piotr Mieczkowski Dennis C. Ko Christina A. Cuomo Joseph Heitman
author_sort	Soo Chan Lee
title	Analysis of a Food-Borne Fungal Pathogen Outbreak: Virulence and Genome of a <italic toggle="yes">Mucor circinelloides</italic> Isolate from Yogurt
title_short	Analysis of a Food-Borne Fungal Pathogen Outbreak: Virulence and Genome of a <italic toggle="yes">Mucor circinelloides</italic> Isolate from Yogurt
title_full	Analysis of a Food-Borne Fungal Pathogen Outbreak: Virulence and Genome of a <italic toggle="yes">Mucor circinelloides</italic> Isolate from Yogurt
title_fullStr	Analysis of a Food-Borne Fungal Pathogen Outbreak: Virulence and Genome of a <italic toggle="yes">Mucor circinelloides</italic> Isolate from Yogurt
title_full_unstemmed	Analysis of a Food-Borne Fungal Pathogen Outbreak: Virulence and Genome of a <italic toggle="yes">Mucor circinelloides</italic> Isolate from Yogurt
title_sort	analysis of a food-borne fungal pathogen outbreak: virulence and genome of a <italic toggle="yes">mucor circinelloides</italic> isolate from yogurt
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/4f1204adec92496ba0ae8d20a168ae86
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Analysis of a Food-Borne Fungal Pathogen Outbreak: Virulence and Genome of a <italic toggle="yes">Mucor circinelloides</italic> Isolate from Yogurt

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