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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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Four Common Topologies Detected by Phylogenetic Analysis of N. fischeri-Specific Proteins.The N. fischeri proteins under consideration are in bold red. The bootstrap supporting the clade containing the N. fischeri is also in bold red. Other N. fischeri proteins are shown in bold black. Blue species names correspond to the recipient genome when different from N. fischeri. Systematic gene names are indicated. Branches with a bootstrap of 75% or more are indicated in bold black. The trees are maximum-likelihood trees (see Materials and Methods). A. Set1 protein evolved by probable duplication, differentiation and differential loss in other Aspergillus species (DDL). B. Set 2 protein evolved by probable HGT from Sordaryomycetes into the N. fischeri lineage. C. Set 2 protein evolved by probable DDL and a Fusarium solani protein (in blue) evolved by probable HGT from the N. fischeri lineage into Sordaryomycetes. D. Set 2 protein showing similarity to a protein from the Sordaryomyce Chaetomium globosum.
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pgen-1000046-g007: Four Common Topologies Detected by Phylogenetic Analysis of N. fischeri-Specific Proteins.The N. fischeri proteins under consideration are in bold red. The bootstrap supporting the clade containing the N. fischeri is also in bold red. Other N. fischeri proteins are shown in bold black. Blue species names correspond to the recipient genome when different from N. fischeri. Systematic gene names are indicated. Branches with a bootstrap of 75% or more are indicated in bold black. The trees are maximum-likelihood trees (see Materials and Methods). A. Set1 protein evolved by probable duplication, differentiation and differential loss in other Aspergillus species (DDL). B. Set 2 protein evolved by probable HGT from Sordaryomycetes into the N. fischeri lineage. C. Set 2 protein evolved by probable DDL and a Fusarium solani protein (in blue) evolved by probable HGT from the N. fischeri lineage into Sordaryomycetes. D. Set 2 protein showing similarity to a protein from the Sordaryomyce Chaetomium globosum.

Mentions: The four repetitive scenarios identified by phylogenetic analysis are displayed in Figure 7. In both A. fumigatus and N. fischeri, most of the Set 1 genes exhibit topologies that do not strictly follow the Aspergillus species tree (Figure 2), although nested within the Aspergillus clade. Similarly, all 28 A. fumigatus Set 2 genes are nested within the Aspergillus genus. In contrast to the A. fumigatus genes, N. fischeri Set 2 genes sometimes cluster with a non-Aspergillus species with high bootstrap support. As shown in Figure 7B and 7C, both N. fischeri and non-Aspergillus species genes can be nested either in this non-Aspergillus clade or in the Aspergillus clade. At first sight, these repetitive topologies can be interpreted as supportive of a horizontal gene transfer (HGT) from a non-Aspergillus species into N. fischeri or visa versa. Further analysis, however, reveals that most of the conflicts involve sparsely populated trees, long branch attraction artifacts, and other situations, where phylogenetic methods tend to mislead (e.g. [41]). The last repetitive scenario includes genes that are only present in one other distant fungal genome (Figure 7D). The evolutionary origin of genes in this category cannot be resolved at this time.


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)

Four Common Topologies Detected by Phylogenetic Analysis of N. fischeri-Specific Proteins.The N. fischeri proteins under consideration are in bold red. The bootstrap supporting the clade containing the N. fischeri is also in bold red. Other N. fischeri proteins are shown in bold black. Blue species names correspond to the recipient genome when different from N. fischeri. Systematic gene names are indicated. Branches with a bootstrap of 75% or more are indicated in bold black. The trees are maximum-likelihood trees (see Materials and Methods). A. Set1 protein evolved by probable duplication, differentiation and differential loss in other Aspergillus species (DDL). B. Set 2 protein evolved by probable HGT from Sordaryomycetes into the N. fischeri lineage. C. Set 2 protein evolved by probable DDL and a Fusarium solani protein (in blue) evolved by probable HGT from the N. fischeri lineage into Sordaryomycetes. D. Set 2 protein showing similarity to a protein from the Sordaryomyce Chaetomium globosum.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2289846&req=5

pgen-1000046-g007: Four Common Topologies Detected by Phylogenetic Analysis of N. fischeri-Specific Proteins.The N. fischeri proteins under consideration are in bold red. The bootstrap supporting the clade containing the N. fischeri is also in bold red. Other N. fischeri proteins are shown in bold black. Blue species names correspond to the recipient genome when different from N. fischeri. Systematic gene names are indicated. Branches with a bootstrap of 75% or more are indicated in bold black. The trees are maximum-likelihood trees (see Materials and Methods). A. Set1 protein evolved by probable duplication, differentiation and differential loss in other Aspergillus species (DDL). B. Set 2 protein evolved by probable HGT from Sordaryomycetes into the N. fischeri lineage. C. Set 2 protein evolved by probable DDL and a Fusarium solani protein (in blue) evolved by probable HGT from the N. fischeri lineage into Sordaryomycetes. D. Set 2 protein showing similarity to a protein from the Sordaryomyce Chaetomium globosum.
Mentions: The four repetitive scenarios identified by phylogenetic analysis are displayed in Figure 7. In both A. fumigatus and N. fischeri, most of the Set 1 genes exhibit topologies that do not strictly follow the Aspergillus species tree (Figure 2), although nested within the Aspergillus clade. Similarly, all 28 A. fumigatus Set 2 genes are nested within the Aspergillus genus. In contrast to the A. fumigatus genes, N. fischeri Set 2 genes sometimes cluster with a non-Aspergillus species with high bootstrap support. As shown in Figure 7B and 7C, both N. fischeri and non-Aspergillus species genes can be nested either in this non-Aspergillus clade or in the Aspergillus clade. At first sight, these repetitive topologies can be interpreted as supportive of a horizontal gene transfer (HGT) from a non-Aspergillus species into N. fischeri or visa versa. Further analysis, however, reveals that most of the conflicts involve sparsely populated trees, long branch attraction artifacts, and other situations, where phylogenetic methods tend to mislead (e.g. [41]). The last repetitive scenario includes genes that are only present in one other distant fungal genome (Figure 7D). The evolutionary origin of genes in this category cannot be resolved at this time.

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
Related in: MedlinePlus