Importance of Resolving Fungal Nomenclature: the Case of Multiple Pathogenic Species in the Cryptococcus Genus

Ferry Hagen^{1

2}, H Thorsten Lumbsch³, Valentina Arsic Arsenijevic⁴, Hamid Badali⁵, Sebastien Bertout⁶, R Blake Billmyre⁷, M Rosa Bragulat⁸, F Javier Cabañes⁸, Mauricio Carbia⁹, Arunaloke Chakrabarti¹⁰, Sudha Chaturvedi¹¹, Vishnu Chaturvedi¹¹, Min Chen^{12

13}, Anuradha Chowdhary¹⁴, Maria-Francisca Colom¹⁵, Oliver A Cornely^{16

17

18}, Pedro W Crous^{19

20

21}, Maria S Cuétara²², Mara R Diaz^{23

24}, Ana Espinel-Ingroff²⁵, Hamed Fakhim²⁶, Rama Falk^{27

28}, Wenjie Fang^{12

13}, Patricia F Herkert^{1

29}, Consuelo Ferrer Rodríguez¹⁵, James A Fraser³⁰, Josepa Gené³¹, Josep Guarro³¹, Alexander Idnurm³², María-Teresa Illnait-Zaragozi³³, Ziauddin Khan³⁴, Kantarawee Khayhan^{35

36}, Anna Kolecka³⁶, Cletus P Kurtzman³⁷, Katrien Lagrou^{38

39}, Wanqing Liao^{12

13}, Carlos Linares¹⁵, Jacques F Meis^{1

2}, Kirsten Nielsen⁴⁰, Tinashe K Nyazika^{41

42

43}, Weihua Pan^{12

13}, Marina Pekmezovic⁴⁴, Itzhack Polacheck²⁷, Brunella Posteraro⁴⁵, Flavio de Queiroz Telles Filho⁴⁶, Orazio Romeo^{47

48}, Manuel Sánchez¹⁵, Ana Sampaio⁴⁹, Maurizio Sanguinetti⁵⁰, Pojana Sriburee⁵¹, Takashi Sugita⁵², Saad J Taj-Aldeen⁵³, Masako Takashima⁵⁴, John W Taylor⁵⁵, Bart Theelen³⁶, Rok Tomazin⁵⁶, Paul E Verweij^{2

57}, Retno Wahyuningsih^{58

59}, Ping Wang^{60

61}, Teun Boekhout^{62

36}

Affiliations

¹ Department of Medical Microbiology and Infectious Diseases, Canisius-Wilhelmina Hospital, Nijmegen, The Netherlands.
² Centre of Expertise in Mycology Radboudumc/CWZ, Nijmegen, The Netherlands.
³ Science & Education, The Field Museum, Chicago, Illinois, USA.
⁴ Institute of Microbiology and Immunology, Faculty of Medicine, University of Belgrade, Belgrade, Serbia.
⁵ Department of Medical Mycology and Parasitology/Invasive Fungi Research Center (IFRC), Mazandaran University of Medical Sciences, Sari, Iran.
⁶ Unité Mixte Internationale Recherches Translationnelles sur l'Infection à VIH et les Maladies Infectieuses, Laboratoire de Parasitologie et Mycologie Médicale, UFR Pharmacie, Université Montpellier, Montpellier, France.
⁷ Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, USA.
⁸ Veterinary Mycology Group, Department of Animal Health and Anatomy, Universitat Autònoma de Barcelona, Bellaterra, Barcelona, Spain.
⁹ Departamento de Parasitología y Micología, Instituto de Higiene, Facultad de Medicina, Universidad de la República, Montevideo, Uruguay.
¹⁰ Department of Medical Microbiology, Postgraduate Institute of Medical Education and Research, Chandigarh, India.
¹¹ Mycology Laboratory, Wadsworth Center, New York State Department of Health, Albany, New York, USA.
¹² Shanghai Key Laboratory of Molecular Medical Mycology, Shanghai Institute of Medical Mycology, Second Military Medical University, Shanghai, China.
¹³ Department of Dermatology, Changzheng Hospital, Second Military Medical University, Shanghai, China.
¹⁴ Department of Medical Mycology, Vallabhbhai Patel Chest Institute, University of Delhi, Delhi, India.
¹⁵ Medical School, Universidad Miguel Hernández, Alicante, Spain.
¹⁶ CECAD Cluster of Excellence, University of Cologne, Cologne, Germany.
¹⁷ Department I for Internal Medicine, University Hospital of Cologne, Cologne, Germany.
¹⁸ Center for Clinical Trials, University Hospital Cologne, Cologne, Germany.
¹⁹ Phytopathology Research, Westerdijk Fungal Biodiversity Institute, Utrecht, The Netherlands.
²⁰ Department of Entomology and Plant Pathology, Faculty of Agriculture, Chiang Mai University, Chiang Mai, Thailand.
²¹ Department of Microbiology and Plant Pathology, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, South Africa.
²² Department of Microbiology, Hospital Severo Ochoa, Madrid, Spain.
²³ University of Miami, NSF NIEHS Oceans and Human Health Center, Miami, Florida, USA.
²⁴ Rosentiel School of Marine and Atmospheric Science, Division of Marine Biology and Fisheries, University of Miami, Miami, Florida, USA.
²⁵ VCU Medical Center, Richmond, Virginia, USA.
²⁶ Department of Medical Parasitology and Mycology/Cellular and Molecular Research Center, Urmia University of Medical Sciences, Urmia, Iran.
²⁷ Department of Clinical Microbiology and Infectious Diseases, Hadassah-Hebrew University Medical Center, Ein Kerem, Jerusalem, Israel.
²⁸ Department of Fisheries and Aquaculture, Ministry of Agriculture and Rural Development, Nir-David, Israel.
²⁹ Postgraduate Program in Microbiology, Parasitology and Pathology, Biological Sciences, Department of Basic Pathology, Federal University of Parana, Curitiba, Brazil.
³⁰ Australian Infectious Diseases Research Centre, School of Chemistry & Molecular Biosciences, University of Queensland, Brisbane, Australia.
³¹ Unitat de Micologia, Facultat de Medicina i Ciències de la Salut, IISPV, Universitat Rovira i Virgili, Reus, Spain.
³² School of BioSciences, BioSciences 2, University of Melbourne, Melbourne, Australia.
³³ Department of Bacteriology and Mycology, Tropical Medicine Institute Pedro Kouri, Havana, Cuba.
³⁴ Department of Microbiology, Faculty of Medicine, Kuwait University, Safat, Kuwait.
³⁵ Department of Microbiology and Parasitology, Faculty of Medical Sciences, University of Phayao, Phayao, Thailand.
³⁶ Yeast Research, Westerdijk Fungal Biodiversity Institute, Utrecht, The Netherlands.
³⁷ Mycotoxin Prevention and Applied Microbiology Research Unit, National Center for Agricultural Utilization Research, USDA-ARS, Peoria, Illinois, USA.
³⁸ Department of Laboratory Medicine, University Hospitals Leuven, Leuven, Belgium.
³⁹ Department of Microbiology and Immunology, KU Leuven - University of Leuven, Leuven, Belgium.
⁴⁰ Department of Microbiology and Immunology, University of Minnesota, Minneapolis, Minnesota, USA.
⁴¹ Department of Medical Microbiology, College of Health Sciences, University of Zimbabwe, Harare, Zimbabwe.
⁴² Malawi-Liverpool-Wellcome Trust, College of Medicine, University of Malawi, Blantyre, Malawi.
⁴³ School of Tropical Medicine, Liverpool, United Kingdom.
⁴⁴ Faculty of Medicine. University of Belgrade, Belgrade, Serbia.
⁴⁵ Institute of Public Health (Section of Hygiene), Università Cattolica del Sacro Cuore, Fondazione Policlinico Universitario Agostino Gemelli, Rome, Italy.
⁴⁶ Department of Communitarian Health, Hospital de Clínicas, Federal University of Parana, Curitiba, Brazil.
⁴⁷ Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina, Messina, Italy.
⁴⁸ IRCCS Centro Neurolesi Bonino-Pulejo, Messina, Italy.
⁴⁹ Centro de Investigação e de Tecnologias Agro-ambientais e Biológicas (CITAB), Universidade de Trás-os-Montes e Alto Douro (UTAD), Quinta dos Prados, Vila Real, Portugal.
⁵⁰ Institute of Microbiology, Università Cattolica del Sacro Cuore, Fondazione Policlinico Universitario Agostino Gemelli, Rome, Italy.
⁵¹ Department of Microbiology, Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand.
⁵² Department of Microbiology, Meiji Pharmaceutical University, Noshio, Kiyose, Tokyo, Japan.
⁵³ Mycology Unit, Microbiology Division, Department of Laboratory Medicine and Pathology, Hamad Medical Corporation, Doha, Qatar.
⁵⁴ Japan Collection of Microorganisms, RIKEN BioResource Center, Koyadai, Tsukuba, Ibaraki, Japan.
⁵⁵ Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, California, USA.
⁵⁶ Institute of Microbiology and Immunology, Faculty of Medicine, University of Ljubljana, Ljubljana, Slovenia.
⁵⁷ Department of Medical Microbiology, Radboud University Medical Centre, Nijmegen, The Netherlands.
⁵⁸ Department of Parasitology, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia.
⁵⁹ Department of Parasitology, School of Medicine, Universitas Kristen Indonesia, Jakarta, Indonesia.
⁶⁰ Department of Microbiology, Immunology and Parasitology, Louisiana State University Health Sciences Center, New Orleans, Louisiana, USA.
⁶¹ Department of Pediatrics, Louisiana State University Health Sciences Center, New Orleans, Louisiana, USA.
⁶² Institute of Biodiversity and Ecosystems Dynamics (IBED), University of Amsterdam, Amsterdam, The Netherlands.

PMID: 28875175
PMCID: PMC5577652
DOI: 10.1128/mSphere.00238-17

Importance of Resolving Fungal Nomenclature: the Case of Multiple Pathogenic Species in the Cryptococcus Genus

Ferry Hagen et al. mSphere. 2017.

. 2017 Aug 30;2(4):e00238-17.

doi: 10.1128/mSphere.00238-17. eCollection 2017 Jul-Aug.

Authors

Affiliations

¹ Department of Medical Microbiology and Infectious Diseases, Canisius-Wilhelmina Hospital, Nijmegen, The Netherlands.
² Centre of Expertise in Mycology Radboudumc/CWZ, Nijmegen, The Netherlands.
³ Science & Education, The Field Museum, Chicago, Illinois, USA.
⁴ Institute of Microbiology and Immunology, Faculty of Medicine, University of Belgrade, Belgrade, Serbia.
⁵ Department of Medical Mycology and Parasitology/Invasive Fungi Research Center (IFRC), Mazandaran University of Medical Sciences, Sari, Iran.
⁶ Unité Mixte Internationale Recherches Translationnelles sur l'Infection à VIH et les Maladies Infectieuses, Laboratoire de Parasitologie et Mycologie Médicale, UFR Pharmacie, Université Montpellier, Montpellier, France.
⁷ Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, USA.
⁸ Veterinary Mycology Group, Department of Animal Health and Anatomy, Universitat Autònoma de Barcelona, Bellaterra, Barcelona, Spain.
⁹ Departamento de Parasitología y Micología, Instituto de Higiene, Facultad de Medicina, Universidad de la República, Montevideo, Uruguay.
¹⁰ Department of Medical Microbiology, Postgraduate Institute of Medical Education and Research, Chandigarh, India.
¹¹ Mycology Laboratory, Wadsworth Center, New York State Department of Health, Albany, New York, USA.
¹² Shanghai Key Laboratory of Molecular Medical Mycology, Shanghai Institute of Medical Mycology, Second Military Medical University, Shanghai, China.
¹³ Department of Dermatology, Changzheng Hospital, Second Military Medical University, Shanghai, China.
¹⁴ Department of Medical Mycology, Vallabhbhai Patel Chest Institute, University of Delhi, Delhi, India.
¹⁵ Medical School, Universidad Miguel Hernández, Alicante, Spain.
¹⁶ CECAD Cluster of Excellence, University of Cologne, Cologne, Germany.
¹⁷ Department I for Internal Medicine, University Hospital of Cologne, Cologne, Germany.
¹⁸ Center for Clinical Trials, University Hospital Cologne, Cologne, Germany.
¹⁹ Phytopathology Research, Westerdijk Fungal Biodiversity Institute, Utrecht, The Netherlands.
²⁰ Department of Entomology and Plant Pathology, Faculty of Agriculture, Chiang Mai University, Chiang Mai, Thailand.
²¹ Department of Microbiology and Plant Pathology, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, South Africa.
²² Department of Microbiology, Hospital Severo Ochoa, Madrid, Spain.
²³ University of Miami, NSF NIEHS Oceans and Human Health Center, Miami, Florida, USA.
²⁴ Rosentiel School of Marine and Atmospheric Science, Division of Marine Biology and Fisheries, University of Miami, Miami, Florida, USA.
²⁵ VCU Medical Center, Richmond, Virginia, USA.
²⁶ Department of Medical Parasitology and Mycology/Cellular and Molecular Research Center, Urmia University of Medical Sciences, Urmia, Iran.
²⁷ Department of Clinical Microbiology and Infectious Diseases, Hadassah-Hebrew University Medical Center, Ein Kerem, Jerusalem, Israel.
²⁸ Department of Fisheries and Aquaculture, Ministry of Agriculture and Rural Development, Nir-David, Israel.
²⁹ Postgraduate Program in Microbiology, Parasitology and Pathology, Biological Sciences, Department of Basic Pathology, Federal University of Parana, Curitiba, Brazil.
³⁰ Australian Infectious Diseases Research Centre, School of Chemistry & Molecular Biosciences, University of Queensland, Brisbane, Australia.
³¹ Unitat de Micologia, Facultat de Medicina i Ciències de la Salut, IISPV, Universitat Rovira i Virgili, Reus, Spain.
³² School of BioSciences, BioSciences 2, University of Melbourne, Melbourne, Australia.
³³ Department of Bacteriology and Mycology, Tropical Medicine Institute Pedro Kouri, Havana, Cuba.
³⁴ Department of Microbiology, Faculty of Medicine, Kuwait University, Safat, Kuwait.
³⁵ Department of Microbiology and Parasitology, Faculty of Medical Sciences, University of Phayao, Phayao, Thailand.
³⁶ Yeast Research, Westerdijk Fungal Biodiversity Institute, Utrecht, The Netherlands.
³⁷ Mycotoxin Prevention and Applied Microbiology Research Unit, National Center for Agricultural Utilization Research, USDA-ARS, Peoria, Illinois, USA.
³⁸ Department of Laboratory Medicine, University Hospitals Leuven, Leuven, Belgium.
³⁹ Department of Microbiology and Immunology, KU Leuven - University of Leuven, Leuven, Belgium.
⁴⁰ Department of Microbiology and Immunology, University of Minnesota, Minneapolis, Minnesota, USA.
⁴¹ Department of Medical Microbiology, College of Health Sciences, University of Zimbabwe, Harare, Zimbabwe.
⁴² Malawi-Liverpool-Wellcome Trust, College of Medicine, University of Malawi, Blantyre, Malawi.
⁴³ School of Tropical Medicine, Liverpool, United Kingdom.
⁴⁴ Faculty of Medicine. University of Belgrade, Belgrade, Serbia.
⁴⁵ Institute of Public Health (Section of Hygiene), Università Cattolica del Sacro Cuore, Fondazione Policlinico Universitario Agostino Gemelli, Rome, Italy.
⁴⁶ Department of Communitarian Health, Hospital de Clínicas, Federal University of Parana, Curitiba, Brazil.
⁴⁷ Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina, Messina, Italy.
⁴⁸ IRCCS Centro Neurolesi Bonino-Pulejo, Messina, Italy.
⁴⁹ Centro de Investigação e de Tecnologias Agro-ambientais e Biológicas (CITAB), Universidade de Trás-os-Montes e Alto Douro (UTAD), Quinta dos Prados, Vila Real, Portugal.
⁵⁰ Institute of Microbiology, Università Cattolica del Sacro Cuore, Fondazione Policlinico Universitario Agostino Gemelli, Rome, Italy.
⁵¹ Department of Microbiology, Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand.
⁵² Department of Microbiology, Meiji Pharmaceutical University, Noshio, Kiyose, Tokyo, Japan.
⁵³ Mycology Unit, Microbiology Division, Department of Laboratory Medicine and Pathology, Hamad Medical Corporation, Doha, Qatar.
⁵⁴ Japan Collection of Microorganisms, RIKEN BioResource Center, Koyadai, Tsukuba, Ibaraki, Japan.
⁵⁵ Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, California, USA.
⁵⁶ Institute of Microbiology and Immunology, Faculty of Medicine, University of Ljubljana, Ljubljana, Slovenia.
⁵⁷ Department of Medical Microbiology, Radboud University Medical Centre, Nijmegen, The Netherlands.
⁵⁸ Department of Parasitology, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia.
⁵⁹ Department of Parasitology, School of Medicine, Universitas Kristen Indonesia, Jakarta, Indonesia.
⁶⁰ Department of Microbiology, Immunology and Parasitology, Louisiana State University Health Sciences Center, New Orleans, Louisiana, USA.
⁶¹ Department of Pediatrics, Louisiana State University Health Sciences Center, New Orleans, Louisiana, USA.
⁶² Institute of Biodiversity and Ecosystems Dynamics (IBED), University of Amsterdam, Amsterdam, The Netherlands.

PMID: 28875175
PMCID: PMC5577652
DOI: 10.1128/mSphere.00238-17

Abstract

Cryptococcosis is a major fungal disease caused by members of the Cryptococcus gattii and Cryptococcus neoformans species complexes. After more than 15 years of molecular genetic and phenotypic studies and much debate, a proposal for a taxonomic revision was made. The two varieties within C. neoformans were raised to species level, and the same was done for five genotypes within C. gattii. In a recent perspective (K. J. Kwon-Chung et al., mSphere 2:e00357-16, 2017, https://doi.org/10.1128/mSphere.00357-16), it was argued that this taxonomic proposal was premature and without consensus in the community. Although the authors of the perspective recognized the existence of genetic diversity, they preferred the use of the informal nomenclature "C. neoformans species complex" and "C. gattii species complex." Here we highlight the advantage of recognizing these seven species, as ignoring these species will impede deciphering further biologically and clinically relevant differences between them, which may in turn delay future clinical advances.

Keywords: Cryptococcus; cryptococcosis; diagnostics; species delimitation; taxonomy.

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References

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Importance of Resolving Fungal Nomenclature: the Case of Multiple Pathogenic Species in the Cryptococcus Genus

Affiliations

Importance of Resolving Fungal Nomenclature: the Case of Multiple Pathogenic Species in the Cryptococcus Genus

Authors

Affiliations

Abstract

References

Grants and funding

LinkOut - more resources

Full Text Sources

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