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Evolution of an endofungal lifestyle: Deductions from the Burkholderia rhizoxinica genome.

Lackner G, Moebius N, Partida-Martinez LP, Boland S, Hertweck C - BMC Genomics (2011)

Bottom Line: Notably, B. rhizoxinica lacks common genes which are dedicated to quorum sensing systems, but is equipped with a large number of virulence-related factors and putative type III effectors.Gene clusters for biosynthesis of secondary metabolites represent novel targets for genomic mining of cryptic natural products.In silico analyses of virulence-associated genes, secreted proteins and effectors might inspire future studies on molecular mechanisms underlying bacterial-fungal interaction.

View Article: PubMed Central - HTML - PubMed

Affiliation: Leibniz Institute for Natural Product Research and Infection Biology (HKI), Department of Biomolecular Chemistry, Beutenbergstr, 11a, 07745 Jena, Germany.

ABSTRACT

Background: Burkholderia rhizoxinica is an intracellular symbiont of the phytopathogenic zygomycete Rhizopus microsporus, the causative agent of rice seedling blight. The endosymbiont produces the antimitotic macrolide rhizoxin for its host. It is vertically transmitted within vegetative spores and is essential for spore formation of the fungus. To shed light on the evolution and genetic potential of this model organism, we analysed the whole genome of B. rhizoxinica HKI 0454 - a type strain of endofungal Burkholderia species.

Results: The genome consists of a structurally conserved chromosome and two plasmids. Compared to free-living Burkholderia species, the genome is smaller in size and harbors less transcriptional regulator genes. Instead, we observed accumulation of transposons over the genome. Prediction of primary metabolic pathways and transporters suggests that endosymbionts consume host metabolites like citrate, but might deliver some amino acids and cofactors to the host. The rhizoxin biosynthesis gene cluster shows evolutionary traces of horizontal gene transfer. Furthermore, we analysed gene clusters coding for nonribosomal peptide synthetases (NRPS). Notably, B. rhizoxinica lacks common genes which are dedicated to quorum sensing systems, but is equipped with a large number of virulence-related factors and putative type III effectors.

Conclusions: B. rhizoxinica is the first endofungal bacterium, whose genome has been sequenced. Here, we present models of evolution, metabolism and tools for host-symbiont interaction of the endofungal bacterium deduced from whole genome analyses. Genome size and structure suggest that B. rhizoxinica is in an early phase of adaptation to the intracellular lifestyle (genome in transition). By analysis of tranporters and metabolic pathways we predict how metabolites might be exchanged between the symbiont and its host. Gene clusters for biosynthesis of secondary metabolites represent novel targets for genomic mining of cryptic natural products. In silico analyses of virulence-associated genes, secreted proteins and effectors might inspire future studies on molecular mechanisms underlying bacterial-fungal interaction.

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Representation of each PKS (polyketide synthase) and NRPS (nonribosomal peptide synthetase) gene cluster discovered on the genome of B. rhizoxinica. Arrows represent ORFs and indicate direction of transcription, circles represent domains of deduced NRPS enzymes. A = adenylation domain responsible for recognition and activation of the amino acids. C = condensation domain (catalyzes the peptide bond formation). T = peptidyl carrier protein (carries the growing peptide chain bond as a thioester.
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Figure 3: Representation of each PKS (polyketide synthase) and NRPS (nonribosomal peptide synthetase) gene cluster discovered on the genome of B. rhizoxinica. Arrows represent ORFs and indicate direction of transcription, circles represent domains of deduced NRPS enzymes. A = adenylation domain responsible for recognition and activation of the amino acids. C = condensation domain (catalyzes the peptide bond formation). T = peptidyl carrier protein (carries the growing peptide chain bond as a thioester.

Mentions: In addition to the rhizoxin biosynthesis gene cluster, B. rhizoxinica harbors 14 non-ribosomal peptide synthetase (NRPS) gene clusters (Figure 3). NRPSs are giant multimodular enzymes [23]. Each module typically catalyzes incorporation of one amino acid into the peptide product [44]. The gene clusters and the module architecture of their corresponding NRPS systems are summarized in Figure 3. There are two gene clusters coding for octamodular NRPSs. One of the deduced assembly lines is equipped with three additional methylation domains that catalyze N-methylation of the incorporated amino acid. Another NRPS is encoded by the longest ORF in the genome, which has a total length of 23.3 kb. Notably, the total DNA of all PKS and NRPS loci sums up to 322 kb, covering 9% of the whole genomic sequence. In addition, the megaplasmid bears a gene related to lantibiotic biosynthesis (RBRH_00226), whose closest homolog is found in cyanobacteria [45]. However, its function is unclear, since it is not flanked by genes for secretion or leader peptide processing. Taken together, this considerable biosynthetic potential is surprising, since no peptides corresponding to the gene clusters could be isolated from B. rhizoxinica up to now. We hypothesize that some NRPS products may function as siderophores or antibiotics. It is well conceivable that peptides serve as signal molecules, effectors in bacterial-fungal interaction or support virulence of the phytopathogenic host fungus.


Evolution of an endofungal lifestyle: Deductions from the Burkholderia rhizoxinica genome.

Lackner G, Moebius N, Partida-Martinez LP, Boland S, Hertweck C - BMC Genomics (2011)

Representation of each PKS (polyketide synthase) and NRPS (nonribosomal peptide synthetase) gene cluster discovered on the genome of B. rhizoxinica. Arrows represent ORFs and indicate direction of transcription, circles represent domains of deduced NRPS enzymes. A = adenylation domain responsible for recognition and activation of the amino acids. C = condensation domain (catalyzes the peptide bond formation). T = peptidyl carrier protein (carries the growing peptide chain bond as a thioester.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3102044&req=5

Figure 3: Representation of each PKS (polyketide synthase) and NRPS (nonribosomal peptide synthetase) gene cluster discovered on the genome of B. rhizoxinica. Arrows represent ORFs and indicate direction of transcription, circles represent domains of deduced NRPS enzymes. A = adenylation domain responsible for recognition and activation of the amino acids. C = condensation domain (catalyzes the peptide bond formation). T = peptidyl carrier protein (carries the growing peptide chain bond as a thioester.
Mentions: In addition to the rhizoxin biosynthesis gene cluster, B. rhizoxinica harbors 14 non-ribosomal peptide synthetase (NRPS) gene clusters (Figure 3). NRPSs are giant multimodular enzymes [23]. Each module typically catalyzes incorporation of one amino acid into the peptide product [44]. The gene clusters and the module architecture of their corresponding NRPS systems are summarized in Figure 3. There are two gene clusters coding for octamodular NRPSs. One of the deduced assembly lines is equipped with three additional methylation domains that catalyze N-methylation of the incorporated amino acid. Another NRPS is encoded by the longest ORF in the genome, which has a total length of 23.3 kb. Notably, the total DNA of all PKS and NRPS loci sums up to 322 kb, covering 9% of the whole genomic sequence. In addition, the megaplasmid bears a gene related to lantibiotic biosynthesis (RBRH_00226), whose closest homolog is found in cyanobacteria [45]. However, its function is unclear, since it is not flanked by genes for secretion or leader peptide processing. Taken together, this considerable biosynthetic potential is surprising, since no peptides corresponding to the gene clusters could be isolated from B. rhizoxinica up to now. We hypothesize that some NRPS products may function as siderophores or antibiotics. It is well conceivable that peptides serve as signal molecules, effectors in bacterial-fungal interaction or support virulence of the phytopathogenic host fungus.

Bottom Line: Notably, B. rhizoxinica lacks common genes which are dedicated to quorum sensing systems, but is equipped with a large number of virulence-related factors and putative type III effectors.Gene clusters for biosynthesis of secondary metabolites represent novel targets for genomic mining of cryptic natural products.In silico analyses of virulence-associated genes, secreted proteins and effectors might inspire future studies on molecular mechanisms underlying bacterial-fungal interaction.

View Article: PubMed Central - HTML - PubMed

Affiliation: Leibniz Institute for Natural Product Research and Infection Biology (HKI), Department of Biomolecular Chemistry, Beutenbergstr, 11a, 07745 Jena, Germany.

ABSTRACT

Background: Burkholderia rhizoxinica is an intracellular symbiont of the phytopathogenic zygomycete Rhizopus microsporus, the causative agent of rice seedling blight. The endosymbiont produces the antimitotic macrolide rhizoxin for its host. It is vertically transmitted within vegetative spores and is essential for spore formation of the fungus. To shed light on the evolution and genetic potential of this model organism, we analysed the whole genome of B. rhizoxinica HKI 0454 - a type strain of endofungal Burkholderia species.

Results: The genome consists of a structurally conserved chromosome and two plasmids. Compared to free-living Burkholderia species, the genome is smaller in size and harbors less transcriptional regulator genes. Instead, we observed accumulation of transposons over the genome. Prediction of primary metabolic pathways and transporters suggests that endosymbionts consume host metabolites like citrate, but might deliver some amino acids and cofactors to the host. The rhizoxin biosynthesis gene cluster shows evolutionary traces of horizontal gene transfer. Furthermore, we analysed gene clusters coding for nonribosomal peptide synthetases (NRPS). Notably, B. rhizoxinica lacks common genes which are dedicated to quorum sensing systems, but is equipped with a large number of virulence-related factors and putative type III effectors.

Conclusions: B. rhizoxinica is the first endofungal bacterium, whose genome has been sequenced. Here, we present models of evolution, metabolism and tools for host-symbiont interaction of the endofungal bacterium deduced from whole genome analyses. Genome size and structure suggest that B. rhizoxinica is in an early phase of adaptation to the intracellular lifestyle (genome in transition). By analysis of tranporters and metabolic pathways we predict how metabolites might be exchanged between the symbiont and its host. Gene clusters for biosynthesis of secondary metabolites represent novel targets for genomic mining of cryptic natural products. In silico analyses of virulence-associated genes, secreted proteins and effectors might inspire future studies on molecular mechanisms underlying bacterial-fungal interaction.

Show MeSH
Related in: MedlinePlus