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Ancient horizontal gene transfer from bacteria enhances biosynthetic capabilities of fungi.

Schmitt I, Lumbsch HT - PLoS ONE (2009)

Bottom Line: Our results support an ancient horizontal gene transfer event from an actinobacterial source into ascomycete fungi, followed by gene duplication.Given that actinobacteria are unrivaled producers of biologically active compounds, such as antibiotics, it appears particularly promising to study biosynthetic genes of actinobacterial origin in fungi.The large number of 6-MSA-type PKS sequences found in lichen-forming fungi leads us hypothesize that the evolution of typical lichen compounds, such as orsellinic acid derivatives, was facilitated by the gain of this bacterial polyketide synthase.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Biology and Bell Museum of Natural History, University of Minnesota, St Paul, MN, USA. schm2109@umn.edu

ABSTRACT

Background: Polyketides are natural products with a wide range of biological functions and pharmaceutical applications. Discovery and utilization of polyketides can be facilitated by understanding the evolutionary processes that gave rise to the biosynthetic machinery and the natural product potential of extant organisms. Gene duplication and subfunctionalization, as well as horizontal gene transfer are proposed mechanisms in the evolution of biosynthetic gene clusters. To explain the amount of homology in some polyketide synthases in unrelated organisms such as bacteria and fungi, interkingdom horizontal gene transfer has been evoked as the most likely evolutionary scenario. However, the origin of the genes and the direction of the transfer remained elusive.

Methodology/principal findings: We used comparative phylogenetics to infer the ancestor of a group of polyketide synthase genes involved in antibiotic and mycotoxin production. We aligned keto synthase domain sequences of all available fungal 6-methylsalicylic acid (6-MSA)-type PKSs and their closest bacterial relatives. To assess the role of symbiotic fungi in the evolution of this gene we generated 24 6-MSA synthase sequence tags from lichen-forming fungi. Our results support an ancient horizontal gene transfer event from an actinobacterial source into ascomycete fungi, followed by gene duplication.

Conclusions/significance: Given that actinobacteria are unrivaled producers of biologically active compounds, such as antibiotics, it appears particularly promising to study biosynthetic genes of actinobacterial origin in fungi. The large number of 6-MSA-type PKS sequences found in lichen-forming fungi leads us hypothesize that the evolution of typical lichen compounds, such as orsellinic acid derivatives, was facilitated by the gain of this bacterial polyketide synthase.

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Phylogeny of fungal and bacterial type I PKS genes based on an amino acid alignment of the KS domain (165 sequences).This is a cartoon summary of a 50% majority rule consensus tree of 120,000 trees from a Bayesian analysis. Major clades are collapsed and shown as triangles. Numbers at tips indicate numbers of sequences in the group. Bold branches have significant support (posterior probabilities >94). We reconstructed ancestral character state at nodes 1–5.
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pone-0004437-g002: Phylogeny of fungal and bacterial type I PKS genes based on an amino acid alignment of the KS domain (165 sequences).This is a cartoon summary of a 50% majority rule consensus tree of 120,000 trees from a Bayesian analysis. Major clades are collapsed and shown as triangles. Numbers at tips indicate numbers of sequences in the group. Bold branches have significant support (posterior probabilities >94). We reconstructed ancestral character state at nodes 1–5.

Mentions: Our initial phylogenetic analysis of 165 KS sequences confirms that the fungal 6-MSAS-type clade is more closely related to bacterial than to other fungal PKSs (Fig. 2). This result is in agreement with tree topologies in Kroken et al. (2003) and Castoe et al. (2007). Sister group to the fungal 6-MSAS-type clade is a small group of bacterial modular PKSs (4 sequences), followed by a clade of bacterial iterative type I PKSs (10 sequences). Also closely related are two further clades of bacterial modular PKSs (25 sequences total), which code for enzymes involved in the production of cell-wall-associated lipids in the genus Mycobacterium, such as phenolphthiocerol.


Ancient horizontal gene transfer from bacteria enhances biosynthetic capabilities of fungi.

Schmitt I, Lumbsch HT - PLoS ONE (2009)

Phylogeny of fungal and bacterial type I PKS genes based on an amino acid alignment of the KS domain (165 sequences).This is a cartoon summary of a 50% majority rule consensus tree of 120,000 trees from a Bayesian analysis. Major clades are collapsed and shown as triangles. Numbers at tips indicate numbers of sequences in the group. Bold branches have significant support (posterior probabilities >94). We reconstructed ancestral character state at nodes 1–5.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2636887&req=5

pone-0004437-g002: Phylogeny of fungal and bacterial type I PKS genes based on an amino acid alignment of the KS domain (165 sequences).This is a cartoon summary of a 50% majority rule consensus tree of 120,000 trees from a Bayesian analysis. Major clades are collapsed and shown as triangles. Numbers at tips indicate numbers of sequences in the group. Bold branches have significant support (posterior probabilities >94). We reconstructed ancestral character state at nodes 1–5.
Mentions: Our initial phylogenetic analysis of 165 KS sequences confirms that the fungal 6-MSAS-type clade is more closely related to bacterial than to other fungal PKSs (Fig. 2). This result is in agreement with tree topologies in Kroken et al. (2003) and Castoe et al. (2007). Sister group to the fungal 6-MSAS-type clade is a small group of bacterial modular PKSs (4 sequences), followed by a clade of bacterial iterative type I PKSs (10 sequences). Also closely related are two further clades of bacterial modular PKSs (25 sequences total), which code for enzymes involved in the production of cell-wall-associated lipids in the genus Mycobacterium, such as phenolphthiocerol.

Bottom Line: Our results support an ancient horizontal gene transfer event from an actinobacterial source into ascomycete fungi, followed by gene duplication.Given that actinobacteria are unrivaled producers of biologically active compounds, such as antibiotics, it appears particularly promising to study biosynthetic genes of actinobacterial origin in fungi.The large number of 6-MSA-type PKS sequences found in lichen-forming fungi leads us hypothesize that the evolution of typical lichen compounds, such as orsellinic acid derivatives, was facilitated by the gain of this bacterial polyketide synthase.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Biology and Bell Museum of Natural History, University of Minnesota, St Paul, MN, USA. schm2109@umn.edu

ABSTRACT

Background: Polyketides are natural products with a wide range of biological functions and pharmaceutical applications. Discovery and utilization of polyketides can be facilitated by understanding the evolutionary processes that gave rise to the biosynthetic machinery and the natural product potential of extant organisms. Gene duplication and subfunctionalization, as well as horizontal gene transfer are proposed mechanisms in the evolution of biosynthetic gene clusters. To explain the amount of homology in some polyketide synthases in unrelated organisms such as bacteria and fungi, interkingdom horizontal gene transfer has been evoked as the most likely evolutionary scenario. However, the origin of the genes and the direction of the transfer remained elusive.

Methodology/principal findings: We used comparative phylogenetics to infer the ancestor of a group of polyketide synthase genes involved in antibiotic and mycotoxin production. We aligned keto synthase domain sequences of all available fungal 6-methylsalicylic acid (6-MSA)-type PKSs and their closest bacterial relatives. To assess the role of symbiotic fungi in the evolution of this gene we generated 24 6-MSA synthase sequence tags from lichen-forming fungi. Our results support an ancient horizontal gene transfer event from an actinobacterial source into ascomycete fungi, followed by gene duplication.

Conclusions/significance: Given that actinobacteria are unrivaled producers of biologically active compounds, such as antibiotics, it appears particularly promising to study biosynthetic genes of actinobacterial origin in fungi. The large number of 6-MSA-type PKS sequences found in lichen-forming fungi leads us hypothesize that the evolution of typical lichen compounds, such as orsellinic acid derivatives, was facilitated by the gain of this bacterial polyketide synthase.

Show MeSH
Related in: MedlinePlus