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Comparative genomics of emerging pathogens in the Candida glabrata clade

Toni Gabaldón113*, Tiphaine Martin2, Marina Marcet-Houben1, Pascal Durrens2, Monique Bolotin-Fukuhara3, Olivier Lespinet3, Sylvie Arnaise3, Stéphanie Boisnard3, Gabriela Aguileta1, Ralitsa Atanasova4, Christiane Bouchier5, Arnaud Couloux6, Sophie Creno5, Jose Almeida Cruz127, Hugo Devillers3, Adela Enache-Angoulvant113, Juliette Guitard4, Laure Jaouen3, Laurence Ma5, Christian Marck8, Cécile Neuvéglise9, Eric Pelletier6, Amélie Pinard3, Julie Poulain6, Julien Recoquillay3, Eric Westhof7, Patrick Wincker6, Bernard Dujon10, Christophe Hennequin4 and Cécile Fairhead3*

Author affiliations

1 Bioinformatics and Genomics Programme, Centre for Genomic Regulation (CRG) and UPF, Doctor Aiguader, 88, Barcelona, 08003, Spain

2 Université de Bordeaux 1, LaBRI, INRIA Bordeaux Sud-Ouest (MAGNOME), Talence, F-33405, France

3 Institut de Génétique et Microbiologie, UMR8621 CNRS-Université Paris Sud, Bât 400, UFR des Sciences, Orsay Cedex, F 91405, France

4 APHP, Hôpital St Antoine, Service de Parasitologie-Mycologie, and UMR S945, Inserm, Université P. M. Curie, Paris, France

5 Département Génomes et Génétique, Institut Pasteur, Plate-forme Génomique, rue du Dr. Roux, Paris, F-75015, France

6 CEA, IG, DSV, Genoscope, 2 rue Gaston Crémieux, Evry Cedex, 91057, France

7 Architecture et Réactivité de l‘ARN, Institut de Biologie Moléculaire et Cellulaire du CNRS, Université de Strasbourg, Strasbourg Cedex, F-67084, France

8 Institut de biologie et technologies de Saclay (iBiTec-S), Gif-sur-Yvette cedex, 91191, France

9 INRA, UMR 1319 Micalis, Thiverval-Grignon, F-78850, France

10 Institut Pasteur, Unité de Génétique moléculaires des levures, UMR3525 CNRS, UFR927, Université P. M. Curie, 25 rue du Docteur Roux, Paris Cedex15, F75724, France

11 APHP, Hôpital Bicêtre, Service de Microbiologie, Paris, France

12 Present adress: Champalimaud Foundation, Av. Brasília, Lisboa, 1400-038, Portugal

13 Comparative Genomics Group, CRG-Centre for Genomic Regulation, Doctor Aiguader, 88, Barcelona, 08003, Spain

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Citation and License

BMC Genomics 2013, 14:623  doi:10.1186/1471-2164-14-623

Published: 14 September 2013



Candida glabrata follows C. albicans as the second or third most prevalent cause of candidemia worldwide. These two pathogenic yeasts are distantly related, C. glabrata being part of the Nakaseomyces, a group more closely related to Saccharomyces cerevisiae. Although C. glabrata was thought to be the only pathogenic Nakaseomyces, two new pathogens have recently been described within this group: C. nivariensis and C. bracarensis. To gain insight into the genomic changes underlying the emergence of virulence, we sequenced the genomes of these two, and three other non-pathogenic Nakaseomyces, and compared them to other sequenced yeasts.


Our results indicate that the two new pathogens are more closely related to the non-pathogenic N. delphensis than to C. glabrata. We uncover duplications and accelerated evolution that specifically affected genes in the lineage preceding the group containing N. delphensis and the three pathogens, which may provide clues to the higher propensity of this group to infect humans. Finally, the number of Epa-like adhesins is specifically enriched in the pathogens, particularly in C. glabrata.


Remarkably, some features thought to be the result of adaptation of C. glabrata to a pathogenic lifestyle, are present throughout the Nakaseomyces, indicating these are rather ancient adaptations to other environments. Phylogeny suggests that human pathogenesis evolved several times, independently within the clade. The expansion of the EPA gene family in pathogens establishes an evolutionary link between adhesion and virulence phenotypes. Our analyses thus shed light onto the relationships between virulence and the recent genomic changes that occurred within the Nakaseomyces.

Sequence Accession Numbers

Nakaseomyces delphensis: CAPT01000001 to CAPT01000179

Candida bracarensis: CAPU01000001 to CAPU01000251

Candida nivariensis: CAPV01000001 to CAPV01000123

Candida castellii: CAPW01000001 to CAPW01000101

Nakaseomyces bacillisporus: CAPX01000001 to CAPX01000186

Candida glabrata; Fungal pathogens; Nakaseomyces; Yeast genomes; Yeast evolution