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

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.

SUBMITTER: Lackner G

PROVIDER: S-EPMC3102044 | biostudies-literature | 2011

REPOSITORIES: biostudies-literature

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

Lackner Gerald G Moebius Nadine N Partida-Martinez Laila P LP Boland Sebastian S Hertweck Christian C

BMC genomics 20110504

<h4>Background</h4>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 str ...[more]

PMID: 21539752

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Project description:Burkholderia pseudomallei is the causative agent of the high-mortality disease melioidosis. Although melioidosis is classified as a tropical disease, rare autochthonous cases have been reported from temperate climatic regions, with uncertainty as to whether B. pseudomallei is persistent in the local environment and whether specific genetic mechanisms facilitate the survival of B. pseudomallei outside the tropics. Sporadic cases of melioidosis occurred in a valley region (latitude 31.6°S) in southwest Western Australia, Australia, between 1966 and 1992. We report a new melioidosis cluster in the same region following high rainfall in January 2017. More than 20 animals died, and B. pseudomallei was isolated from four alpacas, a parrot, and three environmental samples taken from the farm where the alpacas resided. Epidemiological data and genomics revealed that two locations on the farm were the probable sources of the alpaca infections. We determined that B. pseudomallei isolates from the 2017 cluster belonged to sequence type 284 (ST-284), as did all isolates recovered from 1966 to 1992. Genomic analysis confirmed that the ST-284 isolates were clonal and contained conserved genomic islands and limited evidence of recombination. We identified protein-coding regions unique to these isolates that might influence the persistence of B. pseudomallei in this temperate region. We demonstrate the environmental persistence of B. pseudomallei in a temperate region for over 50 years, with limited genetic changes suggesting a latent state and with activation, potential aerosolization, and local dispersal following unusually high rainfall.IMPORTANCEBurkholderia pseudomallei is predominantly a tropical pathogen uncommonly found in the environment of temperate climatic regions. It is unclear if introduction into temperate regions is sporadic and temporary or if B. pseudomallei can persist in such environments. B. pseudomallei was identified in the environment of southwest Western Australia with melioidosis cases between 1966 and 1991. We report a new cluster with 23 animal fatalities in the same region from 2017, with B. pseudomallei again being recovered from the environment. Comparison of the isolates from the first and second clusters using genomics revealed a single sequence type, high clonality, and limited recombination, even though the time of recovery of the isolates spanned 51 years. This is a major contrast to the extensive genomic diversity seen in the tropics. Our data support the suggestion that B. pseudomallei has the ability to persist in nontropical environments, potentially in a latent state, and has the ability to activate following favorable conditions (rainfall) and then infect animals and humans.

Dataset Information

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

Publications

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

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