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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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A. fumigatus-Species Specific Genes Supported by Homology and Expression Data.Genes with no orthologs in N. fischeri and A. clavatus constitute the A. fumigatus-specific group (Afum). Genes that have homologs in other fungal genomes constitute the Homology group. Genes differentially expressed in microarray studies represent the Expressed group.
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pgen-1000046-g006: A. fumigatus-Species Specific Genes Supported by Homology and Expression Data.Genes with no orthologs in N. fischeri and A. clavatus constitute the A. fumigatus-specific group (Afum). Genes that have homologs in other fungal genomes constitute the Homology group. Genes differentially expressed in microarray studies represent the Expressed group.

Mentions: These vast differences in gene features between core and specific genes are more likely to be explained by relaxed selective constraints (as discussed below) than by poor annotation quality of LS genes (due to misannotated gene models, gene fragments or random ORFs). We made significant improvements to Af294 gene models by leveraging the comparative genomic data (see Materials and Methods). In addition, all Affc-specific genes have orthologs in N. fischeri and A. clavatus and 43% of them are differentially expressed in various expression studies, which is similar to the A. fumigatus genome average (Table 3). On the other hand, many Afum-specific genes may be non-functional, since only 32% of them are differentially expressed in microarray studies (vs. the 43% genome average) and only 60% of them show sequence similarity to other fungal proteins (Table S7; Figure 6). Nonetheless, at least 20% of Afum-specific genes are supported by combined evidence (homology and expression data) and therefore are likely to be functional. Nonetheless, even these genes are still smaller in size than average Affc- and Asp-core genes.


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)

A. fumigatus-Species Specific Genes Supported by Homology and Expression Data.Genes with no orthologs in N. fischeri and A. clavatus constitute the A. fumigatus-specific group (Afum). Genes that have homologs in other fungal genomes constitute the Homology group. Genes differentially expressed in microarray studies represent the Expressed group.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1000046-g006: A. fumigatus-Species Specific Genes Supported by Homology and Expression Data.Genes with no orthologs in N. fischeri and A. clavatus constitute the A. fumigatus-specific group (Afum). Genes that have homologs in other fungal genomes constitute the Homology group. Genes differentially expressed in microarray studies represent the Expressed group.
Mentions: These vast differences in gene features between core and specific genes are more likely to be explained by relaxed selective constraints (as discussed below) than by poor annotation quality of LS genes (due to misannotated gene models, gene fragments or random ORFs). We made significant improvements to Af294 gene models by leveraging the comparative genomic data (see Materials and Methods). In addition, all Affc-specific genes have orthologs in N. fischeri and A. clavatus and 43% of them are differentially expressed in various expression studies, which is similar to the A. fumigatus genome average (Table 3). On the other hand, many Afum-specific genes may be non-functional, since only 32% of them are differentially expressed in microarray studies (vs. the 43% genome average) and only 60% of them show sequence similarity to other fungal proteins (Table S7; Figure 6). Nonetheless, at least 20% of Afum-specific genes are supported by combined evidence (homology and expression data) and therefore are likely to be functional. Nonetheless, even these genes are still smaller in size than average Affc- and Asp-core genes.

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