The genome of opportunistic fungal pathogen Fusarium oxysporum carries a unique set of lineage-specific chromosomes

Yong Zhang,Kerry O’ Donnell,David C Schwartz,Dilay Hazal Ayhan,David Turrà ,Gregory A Deiulio,Karen Broz,Li Guo,Qiandong Zeng,Eric Pearlman,H Corby Kistler,Jeffrey J Coleman,Nathan P Wiederhold ,Terrance Shea,Ilan Youngster,Alexander J Mcadam,Sergey N Savinov ,Antonio Di Pietro,Martijn Rep,Sarah Young,He Yang,Shiguo Zhou,Jun Li

doi:10.1038/s42003-020-0770-2

Abstract

Fusarium oxysporum is a cross-kingdom fungal pathogen that infects plants and humans. Horizontally transferred lineage-specific (LS) chromosomes were reported to determine host-specific pathogenicity among phytopathogenic F. oxysporum. However, the existence and functional importance of LS chromosomes among human pathogenic isolates are unknown. Here we report four unique LS chromosomes in a human pathogenic strain NRRL 32931, isolated from a leukemia patient. These LS chromosomes were devoid of housekeeping genes, but were significantly enriched in genes encoding metal ion transporters and cation transporters. Homologs of NRRL 32931 LS genes, including a homolog of ceruloplasmin and the genes that contribute to the expansion of the alkaline pH-responsive transcription factor PacC/Rim1p, were also present in the genome of NRRL 47514, a strain associated with Fusarium keratitis outbreak. This study provides the first evidence, to our knowledge, for genomic compartmentalization in two human pathogenic fungal genomes and suggests an important role of LS chromosomes in niche adaptation.

Highlights

1234567890():,; Fusarium oxysporum is a cross-kingdom fungal pathogen that infects plants and humans
NRRL 47514 was collected from the contaminated contact lens of a patient during the USA 2005/06 Fusarium keratitis outbreak[28]
The phylogenetic analysis using 55 conserved single-copy orthologous genes within the Fusarium genus confirmed that most human pathogenic isolates are phylogenetically related[22] and two human pathogenic isolates are placed in the same clade, which are within a subclade (100% bootstrap support) comprising isolates Fol4287 (NRRL 34936) of F. oxysporum f. sp. lycopersici, a vascular wilt pathogen of tomato (S. lycopersicum), and Fo47 (NRRL 54002), a nonpathogenic strain used for biological control[29] (Fig. 1 and Supplementary Data 1 and 2)

Summary

Introduction

1234567890():,; Fusarium oxysporum is a cross-kingdom fungal pathogen that infects plants and humans. We report four unique LS chromosomes in a human pathogenic strain NRRL 32931, isolated from a leukemia patient. These LS chromosomes were devoid of housekeeping genes, but were significantly enriched in genes encoding metal ion transporters and cation transporters. As Fusarium spp. are broadly resistant to most clinically available antifungals[15], fusariosis in immunocompromised patients is associated with high mortality rates[7] and may approach 100% in persistently neutropenic patients[16,17], and Fusarium keratitis is identified as the leading cause of blindness among fungal keratitis patients[18,19]

Methods

Results

Conclusion