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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 6-MSAS-type PKS genes and their bacterial relatives.All PKS belong to the class type I. This is a 50% rule consensus tree from a Bayesian analysis based on a nucleotide alignment of the KS region. Bold branches indicate significant node support (posterior probabilities >94). Pie charts depict likelihood of the ancestor at this node being a fungal PKS (black), bacterial PKS (gray), or a fatty acid synthase (FAS) (white). Asterisks (*) indicate significant probabilities, as shown in Table 2. (L) denotes a lichen-forming ascomycete. Gene designations of characterized genes are indicated in bold print, GenBank accession numbers are given.
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pone-0004437-g003: Phylogeny of fungal 6-MSAS-type PKS genes and their bacterial relatives.All PKS belong to the class type I. This is a 50% rule consensus tree from a Bayesian analysis based on a nucleotide alignment of the KS region. Bold branches indicate significant node support (posterior probabilities >94). Pie charts depict likelihood of the ancestor at this node being a fungal PKS (black), bacterial PKS (gray), or a fatty acid synthase (FAS) (white). Asterisks (*) indicate significant probabilities, as shown in Table 2. (L) denotes a lichen-forming ascomycete. Gene designations of characterized genes are indicated in bold print, GenBank accession numbers are given.

Mentions: To reconstruct the ancestor of the fungal 6-MSAS-type PKS clade, we focused on the four groups of bacterial PKSs that are most closely related to the fungal 6-MSAS-type PKS clade. We analyzed this subset of data based on nucleotide alignments of the KS region. The tree topologies resulting from these alignments are identical to the topology derived from amino acid data. Further, the topologies from three alignments including different outgroups are congruent, and thus only one is shown here (Fig. 3). Results from ancestral character state analyses of three data sets including different outgroups are congruent (Table 2), indicating that outgroup selection has no influence on the reconstructions. The clade most closely related to the fungal 6-MSAS-type PKS consists of four bacterial modular PKSs of unknown function from the genus Mycobacterium. Most closely related to these two groups is an unsupported clade of iterative bacterial PKSs. The products of these genes are small aromatic polyketides, such as 6-MSA and orsellinic acid (Fig. 1). We reconstructed the ancestral character states at five selected nodes in this tree (Fig. 3). Our results support a fungal ancestor of the fungal 6-MSAS-type PKS clade (Node 1). For Node 2 we obtained an insignificant result and are unable to infer the ancestral character state. At the deeper nodes (Nodes 3, 4 and 5) we significantly reconstructed bacterial ancestors. These results are consistent with the hypothesis of horizontal gene transfer of the fungal 6-MSAS-type clade from bacteria to fungi [16].


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

Schmitt I, Lumbsch HT - PLoS ONE (2009)

Phylogeny of fungal 6-MSAS-type PKS genes and their bacterial relatives.All PKS belong to the class type I. This is a 50% rule consensus tree from a Bayesian analysis based on a nucleotide alignment of the KS region. Bold branches indicate significant node support (posterior probabilities >94). Pie charts depict likelihood of the ancestor at this node being a fungal PKS (black), bacterial PKS (gray), or a fatty acid synthase (FAS) (white). Asterisks (*) indicate significant probabilities, as shown in Table 2. (L) denotes a lichen-forming ascomycete. Gene designations of characterized genes are indicated in bold print, GenBank accession numbers are given.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0004437-g003: Phylogeny of fungal 6-MSAS-type PKS genes and their bacterial relatives.All PKS belong to the class type I. This is a 50% rule consensus tree from a Bayesian analysis based on a nucleotide alignment of the KS region. Bold branches indicate significant node support (posterior probabilities >94). Pie charts depict likelihood of the ancestor at this node being a fungal PKS (black), bacterial PKS (gray), or a fatty acid synthase (FAS) (white). Asterisks (*) indicate significant probabilities, as shown in Table 2. (L) denotes a lichen-forming ascomycete. Gene designations of characterized genes are indicated in bold print, GenBank accession numbers are given.
Mentions: To reconstruct the ancestor of the fungal 6-MSAS-type PKS clade, we focused on the four groups of bacterial PKSs that are most closely related to the fungal 6-MSAS-type PKS clade. We analyzed this subset of data based on nucleotide alignments of the KS region. The tree topologies resulting from these alignments are identical to the topology derived from amino acid data. Further, the topologies from three alignments including different outgroups are congruent, and thus only one is shown here (Fig. 3). Results from ancestral character state analyses of three data sets including different outgroups are congruent (Table 2), indicating that outgroup selection has no influence on the reconstructions. The clade most closely related to the fungal 6-MSAS-type PKS consists of four bacterial modular PKSs of unknown function from the genus Mycobacterium. Most closely related to these two groups is an unsupported clade of iterative bacterial PKSs. The products of these genes are small aromatic polyketides, such as 6-MSA and orsellinic acid (Fig. 1). We reconstructed the ancestral character states at five selected nodes in this tree (Fig. 3). Our results support a fungal ancestor of the fungal 6-MSAS-type PKS clade (Node 1). For Node 2 we obtained an insignificant result and are unable to infer the ancestral character state. At the deeper nodes (Nodes 3, 4 and 5) we significantly reconstructed bacterial ancestors. These results are consistent with the hypothesis of horizontal gene transfer of the fungal 6-MSAS-type clade from bacteria to fungi [16].

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