Genotypes and population genetics of cryptococcus neoformans and cryptococcus gattii species complexes in Europe and the mediterranean area

Massimo Cogliati; Marie Desnos-Ollivier; Ilka Mccormick-Smith; Volker Rickerts; Kennio Ferreira-Paim; Wieland Meyer; Teun Boekhout; Ferry Hagen; Bart Theelen; Joäo Inácio; Beatriz Alonso; Maria Colom; Luciana Trilles; Maria Montagna; Antonella de Donno; Serdar Susever; Cagri Ergin; Aristea Velegraki; Mohamed Ellabib; Simona Nardoni; Cristina Macci; Laura Trovato; Ludovico Dipineto; Sevim Akcaglar; Emilija Mlinaric-Missoni; Sébastien Bertout; Ana C.F. Vencá; Ana Sampaio; Giuseppe Criseo; Stephane Ranque; Nilgün Çerikçioğlu; Anna Marchese; Luigi Vezzulli; Macit Ilkit; Vincenzo Pasquale; Itzhack Polacheck; Shawn Lockhart

doi:10.1016/j.fgb.2019.04.001

Article dans une revue Fungal Genetics and Biology Année : 2019

Genotypes and population genetics of cryptococcus neoformans and cryptococcus gattii species complexes in Europe and the mediterranean area

(1) , (2) , (3) , (3) , (4) , (5) , (6) , (7) , (7) , (8) , (8) , (9) , (10) , (11) , (12) , (13) , (14) , (15) , (16) , (17) , (18) , (19) , (20) , (21) , (22) , (23, 24) , (25) , (26) , (27) , (28) , (29) , (30) , (30) , (31) , (32) , (33) , (34)

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Massimo Cogliati

Fonction : Auteur

Università degli Studi di Milano = University of Milan

Marie Desnos-Ollivier

Fonction : Auteur
PersonId : 746841
IdHAL : desnos-ollivier-marie
ORCID : 0000-0002-9137-0466

Institut Pasteur [Paris]

Ilka Mccormick-Smith

Fonction : Auteur

Robert Koch Institute [Berlin]

Volker Rickerts

Fonction : Auteur

Robert Koch Institute [Berlin]

Kennio Ferreira-Paim

Fonction : Auteur

The University of Sydney

Wieland Meyer

Fonction : Auteur

The Westmead Institute for Medical Research

Teun Boekhout

Fonction : Auteur

University of Amsterdam [Amsterdam] = Universiteit van Amsterdam

Ferry Hagen

Fonction : Auteur

Westerdijk Fungal Biodiversity Institute [Utrecht]

Bart Theelen

Fonction : Auteur

Westerdijk Fungal Biodiversity Institute [Utrecht]

Joäo Inácio

Fonction : Auteur

University of Brighton

Beatriz Alonso

Fonction : Auteur
PersonId : 884771

University of Brighton

Maria Colom

Fonction : Auteur

Universidad Miguel Hernández [Elche]

Luciana Trilles

Fonction : Auteur

Fundação Oswaldo Cruz / Oswaldo Cruz Foundation

Maria Montagna

Fonction : Auteur

Università degli studi di Bari Aldo Moro = University of Bari Aldo Moro

Antonella de Donno

Fonction : Auteur

Università del Salento = University of Salento [Lecce]

Serdar Susever

Fonction : Auteur

Cyprus Near East University

Cagri Ergin

Fonction : Auteur

Pamukkale University

Aristea Velegraki

Fonction : Auteur

National and Kapodistrian University of Athens

Mohamed Ellabib

Fonction : Auteur

University of Tripoli - University Al Fateh

Simona Nardoni

Fonction : Auteur

University of Pisa [Italy] = Università di Pisa [Italia] = Université de Pise [Italie]

Cristina Macci

Fonction : Auteur

Research Institute on Terrestrial Ecosystems [CNR, Italy]

Laura Trovato

Fonction : Auteur

Università degli studi di Catania = University of Catania

Ludovico Dipineto

Fonction : Auteur
PersonId : 883652

University of Naples Federico II = Università degli studi di Napoli Federico II

Sevim Akcaglar

Fonction : Auteur

Uludağ Üniversitesi = Uludag University

Emilija Mlinaric-Missoni

Fonction : Auteur

Croatian Institute of Public Health [Zagreb]

Sébastien Bertout

Fonction : Auteur
PersonId : 791794
ORCID : 0000-0001-9724-4690

Recherches Translationnelles sur le VIH et les maladies infectieuses endémiques et émergentes

Université de Montpellier

Ana C.F. Vencá

Fonction : Auteur

Instituto de Higiene e Medicina Tropical

Ana Sampaio

Fonction : Auteur

Universidade de Trás-os-Montes e Alto Douro

Giuseppe Criseo

Fonction : Auteur

University of Messina

Stephane Ranque

Fonction : Auteur
PersonId : 8429
IdHAL : stephane-ranque
ORCID : 0000-0003-3293-5276
IdRef : 111050936

Vecteurs - Infections tropicales et méditerranéennes

Nilgün Çerikçioğlu

Fonction : Auteur

Marmara University [Kadıköy - İstanbul]

Anna Marchese

Fonction : Auteur

Università degli studi di Genova = University of Genoa

Luigi Vezzulli

Fonction : Auteur
PersonId : 773624
ORCID : 0000-0002-4368-1454
IdRef : 24990909X

Università degli studi di Genova = University of Genoa

Macit Ilkit

Fonction : Auteur

Cukurova University

Vincenzo Pasquale

Fonction : Auteur

Università degli Studi di Napoli “Parthenope” = University of Naples

Itzhack Polacheck

Fonction : Auteur

Hadassah Hebrew University Medical Center [Jerusalem]

Shawn Lockhart

Fonction : Auteur
PersonId : 795796
ORCID : 0000-0002-4383-5994

Centers for Disease Control and Prevention [Atlanta]

Résumé

A total of 476 European isolates (310 Cryptococcus neoformans var. grubii, 150 C. neoformans var. neoformans, and 16 C. gattii species complex) from both clinical and environmental sources were analyzed by multi-locus sequence typing. Phylogenetic and population genetic analyses were performed. Sequence analysis identified 74 sequence types among C. neoformans var. neoformans (VNIV), 65 among C. neoformans var. grubii (56 VNI, 8 VNII, 1 VNB), and 5 among the C. gattii species complex (4 VGI and 1 VGIV) isolates. ST23 was the most frequent genotype (22%) among VNI isolates which were mostly grouped in a large clonal cluster including 50% of isolates. Among VNIV isolates, a predominant genotype was not identified. A high percentage of autochthonous STs were identified in both VNI (71%) and VNIV (96%) group of isolates. The 16 European C. gattii species complex isolates analyzed in the present study originated all from the environment and all belonged to a large cluster endemic in the Mediterranean area. Population genetic analysis confirmed that VNI group of isolates were characterized by low variability and clonal expansion while VNIV by a higher variability and a number of recombination events. However, when VNI and VNIV environmental isolates were compared, they showed a similar population structure with a high percentage of shared mutations and the absence of fixed mutations. Also linkage disequilibrium analysis reveals differences between clinical and environmental isolates showing a key role of PLB1 allele combinations in host infection as well as the key role of LAC1 allele combinations for survival of the fungus in the environment. The present study shows that genetic comparison of clinical and environmental isolates represents a first step to understand the genetic characteristics that cause the shift of some genotypes from a saprophytic to a parasitic life style.

Mots clés

Cryptococcus neoformans Cryptococcus gattii MLST Population genetics Europe

Domaines

Bactériologie Virologie Parasitologie Cardiologie et système cardiovasculaire Maladies émergentes Maladies infectieuses

Liste complète des métadonnées

Format du dépôt	Fichier
Type de dépôt	Article dans une revue
Résumé	en A total of 476 European isolates (310 Cryptococcus neoformans var. grubii, 150 C. neoformans var. neoformans, and 16 C. gattii species complex) from both clinical and environmental sources were analyzed by multi-locus sequence typing. Phylogenetic and population genetic analyses were performed. Sequence analysis identified 74 sequence types among C. neoformans var. neoformans (VNIV), 65 among C. neoformans var. grubii (56 VNI, 8 VNII, 1 VNB), and 5 among the C. gattii species complex (4 VGI and 1 VGIV) isolates. ST23 was the most frequent genotype (22%) among VNI isolates which were mostly grouped in a large clonal cluster including 50% of isolates. Among VNIV isolates, a predominant genotype was not identified. A high percentage of autochthonous STs were identified in both VNI (71%) and VNIV (96%) group of isolates. The 16 European C. gattii species complex isolates analyzed in the present study originated all from the environment and all belonged to a large cluster endemic in the Mediterranean area. Population genetic analysis confirmed that VNI group of isolates were characterized by low variability and clonal expansion while VNIV by a higher variability and a number of recombination events. However, when VNI and VNIV environmental isolates were compared, they showed a similar population structure with a high percentage of shared mutations and the absence of fixed mutations. Also linkage disequilibrium analysis reveals differences between clinical and environmental isolates showing a key role of PLB1 allele combinations in host infection as well as the key role of LAC1 allele combinations for survival of the fungus in the environment. The present study shows that genetic comparison of clinical and environmental isolates represents a first step to understand the genetic characteristics that cause the shift of some genotypes from a saprophytic to a parasitic life style.
Titre	en Genotypes and population genetics of cryptococcus neoformans and cryptococcus gattii species complexes in Europe and the mediterranean area
Auteur(s)	Massimo Cogliati ¹ , Marie Desnos-Ollivier ² , Ilka Mccormick-Smith ³ , Volker Rickerts ³ , Kennio Ferreira-Paim ⁴ , Wieland Meyer ⁵ , Teun Boekhout ⁶ , Ferry Hagen ⁷ , Bart Theelen ⁷ , Joäo Inácio ⁸ , Beatriz Alonso ⁸ , Maria Colom ⁹ , Luciana Trilles ¹⁰ , Maria Montagna ¹¹ , Antonella de Donno ¹² , Serdar Susever ¹³ , Cagri Ergin ¹⁴ , Aristea Velegraki ¹⁵ , Mohamed Ellabib ¹⁶ , Simona Nardoni ¹⁷ , Cristina Macci ¹⁸ , Laura Trovato ¹⁹ , Ludovico Dipineto ²⁰ , Sevim Akcaglar ²¹ , Emilija Mlinaric-Missoni ²² , Sébastien Bertout ^{23, 24} , Ana C.F. Vencá ²⁵ , Ana Sampaio ²⁶ , Giuseppe Criseo ²⁷ , Stephane Ranque ²⁸ , Nilgün Çerikçioğlu ²⁹ , Anna Marchese ³⁰ , Luigi Vezzulli ³⁰ , Macit Ilkit ³¹ , Vincenzo Pasquale ³² , Itzhack Polacheck ³³ , Shawn Lockhart ³⁴ 1 UNIMI - Università degli Studi di Milano = University of Milan ( 300694 ) - Via Festa del Perdono 7 - 20122 Milano - Italie 2 IP - Institut Pasteur [Paris] ( 300027 ) - 25-28, rue du docteur Roux, 75724 Paris cedex 15 - France 3 RKI - Robert Koch Institute [Berlin] ( 478253 ) - Nordufer 20, 13353 Berlin, Germany - Allemagne 4 The University of Sydney ( 374701 ) - New South Wales 2006 - Australie 5 The Westmead Institute for Medical Research ( 509020 ) - 176 Hawkesbury Rd, Westmead NSW 2145, Australie - Australie 6 UvA - University of Amsterdam [Amsterdam] = Universiteit van Amsterdam ( 120654 ) - Spui 21 1012 WX Amsterdam - Pays-Bas 7 WI - Westerdijk Fungal Biodiversity Institute [Utrecht] ( 542339 ) - (previously the Fungal Biodiversity Centre, CBS) Uppsalalaan 8, 3584 CT Utrecht, Pays-Bas - Pays-Bas Royal Netherlands Academy of Arts and Sciences ( 444582 ) 8 University of Brighton ( 209121 ) - Mithras House, Lewes Road - Brighton BN2 4AT - Royaume-Uni 9 UMH - Universidad Miguel Hernández [Elche] ( 239392 ) - Av. Universidad S/N, Ed. Torrevaillo, 03202 Elche, Alicante - Espagne 10 FIOCRUZ - Fundação Oswaldo Cruz / Oswaldo Cruz Foundation ( 488707 ) - Av. Brasil, 4365 - Manguinhos, Rio de Janeiro - Brésil Pasteur Network (Réseau International des Instituts Pasteur) ( 301247 ) 11 UNIBA - Università degli studi di Bari Aldo Moro = University of Bari Aldo Moro ( 300766 ) - Piazza Umberto I - 70121 Bari - Italie 12 Università del Salento = University of Salento [Lecce] ( 213256 ) - Piazza Tancredi, 7, 73100 Lecce LE, Italie - Italie 13 Cyprus Near East University ( 1007393 ) - Nicosia - Chypre 14 Pamukkale University ( 461659 ) - Denizli Turkey - Turquie 15 NKUA - National and Kapodistrian University of Athens ( 502478 ) - Athens 157 72 - Grèce 16 University of Tripoli - University Al Fateh ( 360549 ) - Tripoli - Libye 17 UniPi - University of Pisa [Italy] = Università di Pisa [Italia] = Université de Pise [Italie] ( 366408 ) - Lungarno Pacinotti 43 – 56126 Pisa – Italia - Italie 18 IRET - Research Institute on Terrestrial Ecosystems [CNR, Italy] ( 567037 ) - Porano - Italie National Research Council of Italy \| Consiglio Nazionale delle Ricerche ( 254021 ) 19 Unict - Università degli studi di Catania = University of Catania ( 132974 ) - Piazza Università, 2 95131 Catania - Italie 20 University of Naples Federico II = Università degli studi di Napoli Federico II ( 544964 ) - Via Cintia Monte S. Angelo, 80126 Napoli, Italy - Italie 21 Uludağ Üniversitesi = Uludag University ( 556678 ) - Özlüce Mahallesi, Görükle Kampüsü, 16059 Nilüfer/Bursa - Turquie 22 CIPH - Croatian Institute of Public Health [Zagreb] ( 521164 ) - Rockefeller str. 7, 10000 Zagreb - Croatie 23 TransVIHMI - Recherches Translationnelles sur le VIH et les maladies infectieuses endémiques et émergentes ( 1087128 ) - Centre IRD France Sud 911, avenue Agropolis BP 64501 F-34394 Montpellier cedex 5 - France Institut de Recherche pour le Développement UMI 233 ( 67872 ) ; Université de Yaoundé I ( 217395 ) ; Institut National de la Santé et de la Recherche Médicale U 1175 ( 303623 ) ; Université de Montpellier ( 410122 ) ; Université Cheikh Anta Diop de Dakar [Sénégal] ( 1175215 ) 24 UM - Université de Montpellier ( 410122 ) - 163 rue Auguste Broussonnet - 34090 Montpellier - France 25 IHMT - Instituto de Higiene e Medicina Tropical ( 244184 ) - Rua da Junqueira, 100 1349-008 Lisboa - Portugal Universidade Nova de Lisboa = NOVA University Lisbon ( 327246 ) 26 UTAD - Universidade de Trás-os-Montes e Alto Douro ( 206605 ) - Secção Florestal, 5000 Vila Real - Portugal Universidade do Trás-os-Montes e Alto Douro ( 350617 ) 27 University of Messina ( 311402 ) - Italie 28 VITROME - Vecteurs - Infections tropicales et méditerranéennes ( 527045 ) - IHU Méditerranée Infection 19-21 Bd Jean Moulin 13005 Marseille - France Institut de Recherche pour le Développement UMR_D 257 ( 67872 ) ; Aix Marseille Université UMR MD4 ( 198056 ) ; Institut de Recherche Biomédicale des Armées [Brétigny-sur-Orge] ( 507058 ) 29 Marmara University [Kadıköy - İstanbul] ( 466869 ) - MÜ Göztepe Kampüsü, 34722 Kadıköy/İstanbul, Turquey - Turquie 30 UniGe - Università degli studi di Genova = University of Genoa ( 302889 ) - Via Balbi, 5 - 16126 Genova - Italie 31 Cukurova University ( 64572 ) - 01330, Sarıçam / Adana, TÜRKİYE - Turquie 32 PARTHENOPE - Università degli Studi di Napoli “Parthenope” = University of Naples ( 358818 ) - Via Amm. F. Acton, 38 - 80133 Napoli - Italie 33 Hadassah Hebrew University Medical Center [Jerusalem] ( 466445 ) - Kiryat Hadassah, POB 12000 Jerusalem, 91120 - Israël 34 CDC - Centers for Disease Control and Prevention [Atlanta] ( 215584 ) - 1600 Clifton Rd. GA 30333 Atlanta, GA - États-Unis Centers for Disease Control and Prevention ( 312442 )
Audience	Internationale
Date de publication	2019-08
Volume	129
Page/Identifiant	16-29
Langue du document	Anglais
Nom de la revue	Fungal Genet Biol - Fungal Genetics and Biology (ISSN : 1087-1845, ISSN électronique : 1096-0937) Publié par Elsevier
Vulgarisation	Non
Comité de lecture	Oui
Collaboration/Projet	We thank Dr. Kwon Chung and Prof. Dromer for contribution in the critical reading of the manuscript.
Financement	W Meyer and S Lockhart were supported by an NH&MRC grant # APP1031943. AC Sampaio was supported by Fundação para a Ciência e Tecnologia and FEDER/COMPETE/POCI provided to CITAB under the projects POCI-01-0145-FEDER-006958 and UID/AGR/04033/2019. A Velegraki was supported by SARG K.A.70/4/5905 and 70/3/6915, National and Kapodistrian University of Athens and the Bodosakis Foundation, Athens, Greece.
Domaine(s)	Sciences du Vivant [q-bio]/Microbiologie et Parasitologie/Bactériologie Sciences du Vivant [q-bio]/Microbiologie et Parasitologie/Virologie Sciences du Vivant [q-bio]/Microbiologie et Parasitologie/Parasitologie Sciences du Vivant [q-bio]/Médecine humaine et pathologie/Cardiologie et système cardiovasculaire Sciences du Vivant [q-bio]/Médecine humaine et pathologie/Maladies émergentes Sciences du Vivant [q-bio]/Médecine humaine et pathologie/Maladies infectieuses
Mots-clés	en Cryptococcus neoformans, Cryptococcus gattii, MLST, Population genetics, Europe
DOI	10.1016/j.fgb.2019.04.001
Pubmed Id	30953839

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hal-02263653, version 1 (22-04-2020)

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HAL Id : hal-02263653 , version 1
DOI : 10.1016/j.fgb.2019.04.001
PUBMED : 30953839

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Massimo Cogliati, Marie Desnos-Ollivier, Ilka Mccormick-Smith, Volker Rickerts, Kennio Ferreira-Paim, et al.. Genotypes and population genetics of cryptococcus neoformans and cryptococcus gattii species complexes in Europe and the mediterranean area. Fungal Genetics and Biology, 2019, 129, pp.16-29. ⟨10.1016/j.fgb.2019.04.001⟩. ⟨hal-02263653⟩

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Genotypes and population genetics of cryptococcus neoformans and cryptococcus gattii species complexes in Europe and the mediterranean area

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Mots clés

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