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Genomic islands in the pathogenic filamentous fungus Aspergillus fumigatus.

Fedorova ND, Khaldi N, Joardar VS, Maiti R, Amedeo P, Anderson MJ, Crabtree J, Silva JC, Badger JH, Albarraq A, Angiuoli S, Bussey H, Bowyer P, Cotty PJ, Dyer PS, Egan A, Galens K, Fraser-Liggett CM, Haas BJ, Inman JM, Kent R, Lemieux S, Malavazi I, Orvis J, Roemer T, Ronning CM, Sundaram JP, Sutton G, Turner G, Venter JC, White OR, Whitty BR, Youngman P, Wolfe KH, Goldman GH, Wortman JR, Jiang B, Denning DW, Nierman WC - PLoS Genet. (2008)

Bottom Line: The most divergent loci appear to contain heterokaryon incompatibility (het) genes associated with fungal programmed cell death such as developmental regulator rosA.Contrary to what was suggested previously, their origin cannot be attributed to horizontal gene transfer (HGT), but instead is likely to involve duplication, diversification and differential gene loss (DDL).The role of duplication in the origin of lineage-specific genes is further underlined by the discovery of genomic islands that seem to function as designated "gene dumps" and, perhaps, simultaneously, as "gene factories".

View Article: PubMed Central - PubMed

Affiliation: The J. Craig Venter Institute, Rockville, Maryland, United States of America.

ABSTRACT
We present the genome sequences of a new clinical isolate of the important human pathogen, Aspergillus fumigatus, A1163, and two closely related but rarely pathogenic species, Neosartorya fischeri NRRL181 and Aspergillus clavatus NRRL1. Comparative genomic analysis of A1163 with the recently sequenced A. fumigatus isolate Af293 has identified core, variable and up to 2% unique genes in each genome. While the core genes are 99.8% identical at the nucleotide level, identity for variable genes can be as low 40%. The most divergent loci appear to contain heterokaryon incompatibility (het) genes associated with fungal programmed cell death such as developmental regulator rosA. Cross-species comparison has revealed that 8.5%, 13.5% and 12.6%, respectively, of A. fumigatus, N. fischeri and A. clavatus genes are species-specific. These genes are significantly smaller in size than core genes, contain fewer exons and exhibit a subtelomeric bias. Most of them cluster together in 13 chromosomal islands, which are enriched for pseudogenes, transposons and other repetitive elements. At least 20% of A. fumigatus-specific genes appear to be functional and involved in carbohydrate and chitin catabolism, transport, detoxification, secondary metabolism and other functions that may facilitate the adaptation to heterogeneous environments such as soil or a mammalian host. Contrary to what was suggested previously, their origin cannot be attributed to horizontal gene transfer (HGT), but instead is likely to involve duplication, diversification and differential gene loss (DDL). The role of duplication in the origin of lineage-specific genes is further underlined by the discovery of genomic islands that seem to function as designated "gene dumps" and, perhaps, simultaneously, as "gene factories".

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Molecular Divergence in Molds and Yeasts.A. fumigatus proteins are compared to their orthologs in N. fischeri, A. clavatus, A. terreus, A. oryzae, A. nidulans, and A. niger (mean values: 95%, 84%, 71%, 71%, 68%, and 69%, respectively). Saccharomyces paradoxus, Saccharomyces uvarum, Candida glabrata, and Kluyveromyces lactis are compared to Saccharomyces cerevisiae (adapted from [74,75]). Mean values for these species are 90%, 82%, 64%, and 60%, respectively. Median percent identity between pairs of orthologs from A. fumigatus and each successive genome in the tree is shown. Relative divergence of humans, mice, birds and fish are shown for reference.
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pgen-1000046-g001: Molecular Divergence in Molds and Yeasts.A. fumigatus proteins are compared to their orthologs in N. fischeri, A. clavatus, A. terreus, A. oryzae, A. nidulans, and A. niger (mean values: 95%, 84%, 71%, 71%, 68%, and 69%, respectively). Saccharomyces paradoxus, Saccharomyces uvarum, Candida glabrata, and Kluyveromyces lactis are compared to Saccharomyces cerevisiae (adapted from [74,75]). Mean values for these species are 90%, 82%, 64%, and 60%, respectively. Median percent identity between pairs of orthologs from A. fumigatus and each successive genome in the tree is shown. Relative divergence of humans, mice, birds and fish are shown for reference.

Mentions: Recently we presented the genomic sequence of A. fumigatus strain Af293 (FGSC A1100) [7] isolated from a neutropenic patient, who died from invasive aspergillosis [8]. Its comparison with the genomes of two distantly related species, Aspergillus nidulans and Aspergillus oryzae, has led to many unexpected discoveries, including the possibility of a hidden sexual cycle in A. fumigatus and A. oryzae, and the detection of remarkable genetic variability of this genus [9],[10]. Although members of the same genus, these three species are approximately as evolutionarily distant from each other at the molecular level as humans and fish (Figures 1 and 2) [11]. This significant phylogenetic distance has hindered some aspects of comparative genomic analysis of the aspergilli such as identification of the genetic traits responsible for differences in virulence as well as in sexual and physiological properties.


Genomic islands in the pathogenic filamentous fungus Aspergillus fumigatus.

Fedorova ND, Khaldi N, Joardar VS, Maiti R, Amedeo P, Anderson MJ, Crabtree J, Silva JC, Badger JH, Albarraq A, Angiuoli S, Bussey H, Bowyer P, Cotty PJ, Dyer PS, Egan A, Galens K, Fraser-Liggett CM, Haas BJ, Inman JM, Kent R, Lemieux S, Malavazi I, Orvis J, Roemer T, Ronning CM, Sundaram JP, Sutton G, Turner G, Venter JC, White OR, Whitty BR, Youngman P, Wolfe KH, Goldman GH, Wortman JR, Jiang B, Denning DW, Nierman WC - PLoS Genet. (2008)

Molecular Divergence in Molds and Yeasts.A. fumigatus proteins are compared to their orthologs in N. fischeri, A. clavatus, A. terreus, A. oryzae, A. nidulans, and A. niger (mean values: 95%, 84%, 71%, 71%, 68%, and 69%, respectively). Saccharomyces paradoxus, Saccharomyces uvarum, Candida glabrata, and Kluyveromyces lactis are compared to Saccharomyces cerevisiae (adapted from [74,75]). Mean values for these species are 90%, 82%, 64%, and 60%, respectively. Median percent identity between pairs of orthologs from A. fumigatus and each successive genome in the tree is shown. Relative divergence of humans, mice, birds and fish are shown for reference.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2289846&req=5

pgen-1000046-g001: Molecular Divergence in Molds and Yeasts.A. fumigatus proteins are compared to their orthologs in N. fischeri, A. clavatus, A. terreus, A. oryzae, A. nidulans, and A. niger (mean values: 95%, 84%, 71%, 71%, 68%, and 69%, respectively). Saccharomyces paradoxus, Saccharomyces uvarum, Candida glabrata, and Kluyveromyces lactis are compared to Saccharomyces cerevisiae (adapted from [74,75]). Mean values for these species are 90%, 82%, 64%, and 60%, respectively. Median percent identity between pairs of orthologs from A. fumigatus and each successive genome in the tree is shown. Relative divergence of humans, mice, birds and fish are shown for reference.
Mentions: Recently we presented the genomic sequence of A. fumigatus strain Af293 (FGSC A1100) [7] isolated from a neutropenic patient, who died from invasive aspergillosis [8]. Its comparison with the genomes of two distantly related species, Aspergillus nidulans and Aspergillus oryzae, has led to many unexpected discoveries, including the possibility of a hidden sexual cycle in A. fumigatus and A. oryzae, and the detection of remarkable genetic variability of this genus [9],[10]. Although members of the same genus, these three species are approximately as evolutionarily distant from each other at the molecular level as humans and fish (Figures 1 and 2) [11]. This significant phylogenetic distance has hindered some aspects of comparative genomic analysis of the aspergilli such as identification of the genetic traits responsible for differences in virulence as well as in sexual and physiological properties.

Bottom Line: The most divergent loci appear to contain heterokaryon incompatibility (het) genes associated with fungal programmed cell death such as developmental regulator rosA.Contrary to what was suggested previously, their origin cannot be attributed to horizontal gene transfer (HGT), but instead is likely to involve duplication, diversification and differential gene loss (DDL).The role of duplication in the origin of lineage-specific genes is further underlined by the discovery of genomic islands that seem to function as designated "gene dumps" and, perhaps, simultaneously, as "gene factories".

View Article: PubMed Central - PubMed

Affiliation: The J. Craig Venter Institute, Rockville, Maryland, United States of America.

ABSTRACT
We present the genome sequences of a new clinical isolate of the important human pathogen, Aspergillus fumigatus, A1163, and two closely related but rarely pathogenic species, Neosartorya fischeri NRRL181 and Aspergillus clavatus NRRL1. Comparative genomic analysis of A1163 with the recently sequenced A. fumigatus isolate Af293 has identified core, variable and up to 2% unique genes in each genome. While the core genes are 99.8% identical at the nucleotide level, identity for variable genes can be as low 40%. The most divergent loci appear to contain heterokaryon incompatibility (het) genes associated with fungal programmed cell death such as developmental regulator rosA. Cross-species comparison has revealed that 8.5%, 13.5% and 12.6%, respectively, of A. fumigatus, N. fischeri and A. clavatus genes are species-specific. These genes are significantly smaller in size than core genes, contain fewer exons and exhibit a subtelomeric bias. Most of them cluster together in 13 chromosomal islands, which are enriched for pseudogenes, transposons and other repetitive elements. At least 20% of A. fumigatus-specific genes appear to be functional and involved in carbohydrate and chitin catabolism, transport, detoxification, secondary metabolism and other functions that may facilitate the adaptation to heterogeneous environments such as soil or a mammalian host. Contrary to what was suggested previously, their origin cannot be attributed to horizontal gene transfer (HGT), but instead is likely to involve duplication, diversification and differential gene loss (DDL). The role of duplication in the origin of lineage-specific genes is further underlined by the discovery of genomic islands that seem to function as designated "gene dumps" and, perhaps, simultaneously, as "gene factories".

Show MeSH