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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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The Af293 RosA and NosA Proteins.Shown in bold red are RosA, NosA and Pro1 proteins that have been experimentally characterized are shown in bold black. Branches with a bootstrap of 75% or more are indicated in bold black. The trees are maximum-likelihood trees (see Materials and Methods).
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pgen-1000046-g004: The Af293 RosA and NosA Proteins.Shown in bold red are RosA, NosA and Pro1 proteins that have been experimentally characterized are shown in bold black. Branches with a bootstrap of 75% or more are indicated in bold black. The trees are maximum-likelihood trees (see Materials and Methods).

Mentions: Furthermore, at least five putative A. fumigatus het genes exhibit a pattern of trans-species (or trans-specific) polymorphism (Table S5), which has been previously associated with somatic and sexual incompatibility in fungi, self-incompatibility in plants, and the major histocompatibility complex (MHC) in vertebrates. These genes are more similar to their orthologs from other Aspergillus species than to those from A1163. We chose one putative het gene, rosA (AFUA_1G15910), and its close relative, nosA (AFUA_4G09710), whose orthologs encode two Zn2C6 transcriptional regulators of sexual development in A. nidulans [27],[28] for phylogenetic analysis (Figure 4). Unexpectedly, Af293 RosA clusters with its A. clavatus ortholog, while A1163 RosA clusters with N. fischeri. This is in contrast with the NosA tree, which perfectly mirrors the species tree (Figure 2), suggesting that these allelic classes may transcend species boundaries in the aspergilli.


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)

The Af293 RosA and NosA Proteins.Shown in bold red are RosA, NosA and Pro1 proteins that have been experimentally characterized are shown in bold black. Branches with a bootstrap of 75% or more are indicated in bold black. The trees are maximum-likelihood trees (see Materials and Methods).
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1000046-g004: The Af293 RosA and NosA Proteins.Shown in bold red are RosA, NosA and Pro1 proteins that have been experimentally characterized are shown in bold black. Branches with a bootstrap of 75% or more are indicated in bold black. The trees are maximum-likelihood trees (see Materials and Methods).
Mentions: Furthermore, at least five putative A. fumigatus het genes exhibit a pattern of trans-species (or trans-specific) polymorphism (Table S5), which has been previously associated with somatic and sexual incompatibility in fungi, self-incompatibility in plants, and the major histocompatibility complex (MHC) in vertebrates. These genes are more similar to their orthologs from other Aspergillus species than to those from A1163. We chose one putative het gene, rosA (AFUA_1G15910), and its close relative, nosA (AFUA_4G09710), whose orthologs encode two Zn2C6 transcriptional regulators of sexual development in A. nidulans [27],[28] for phylogenetic analysis (Figure 4). Unexpectedly, Af293 RosA clusters with its A. clavatus ortholog, while A1163 RosA clusters with N. fischeri. This is in contrast with the NosA tree, which perfectly mirrors the species tree (Figure 2), suggesting that these allelic classes may transcend species boundaries in the aspergilli.

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