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The complete multipartite genome sequence of Cupriavidus necator JMP134, a versatile pollutant degrader.

ABSTRACT: BACKGROUND: Cupriavidus necator JMP134 is a Gram-negative beta-proteobacterium able to grow on a variety of aromatic and chloroaromatic compounds as its sole carbon and energy source. METHODOLOGY/PRINCIPAL FINDINGS: Its genome consists of four replicons (two chromosomes and two plasmids) containing a total of 6631 protein coding genes. Comparative analysis identified 1910 core genes common to the four genomes compared (C. necator JMP134, C. necator H16, C. metallidurans CH34, R. solanacearum GMI1000). Although secondary chromosomes found in the Cupriavidus, Ralstonia, and Burkholderia lineages are all derived from plasmids, analyses of the plasmid partition proteins located on those chromosomes indicate that different plasmids gave rise to the secondary chromosomes in each lineage. The C. necator JMP134 genome contains 300 genes putatively involved in the catabolism of aromatic compounds and encodes most of the central ring-cleavage pathways. This strain also shows additional metabolic capabilities towards alicyclic compounds and the potential for catabolism of almost all proteinogenic amino acids. This remarkable catabolic potential seems to be sustained by a high degree of genetic redundancy, most probably enabling this catabolically versatile bacterium with different levels of metabolic responses and alternative regulation necessary to cope with a challenging environment. From the comparison of Cupriavidus genomes, it is possible to state that a broad metabolic capability is a general trait for Cupriavidus genus, however certain specialization towards a nutritional niche (xenobiotics degradation, chemolithoautotrophy or symbiotic nitrogen fixation) seems to be shaped mostly by the acquisition of "specialized" plasmids. CONCLUSIONS/SIGNIFICANCE: The availability of the complete genome sequence for C. necator JMP134 provides the groundwork for further elucidation of the mechanisms and regulation of chloroaromatic compound biodegradation.

SUBMITTER: Lykidis A

PROVIDER: S-EPMC2842291 | biostudies-literature | 2010

REPOSITORIES: biostudies-literature

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The complete multipartite genome sequence of Cupriavidus necator JMP134, a versatile pollutant degrader.

Lykidis Athanasios A Pérez-Pantoja Danilo D Ledger Thomas T Mavromatis Kostantinos K Anderson Iain J IJ Ivanova Natalia N NN Hooper Sean D SD Lapidus Alla A Lucas Susan S González Bernardo B Kyrpides Nikos C NC

PloS one 20100322 3

<h4>Background</h4>Cupriavidus necator JMP134 is a Gram-negative beta-proteobacterium able to grow on a variety of aromatic and chloroaromatic compounds as its sole carbon and energy source.<h4>Methodology/principal findings</h4>Its genome consists of four replicons (two chromosomes and two plasmids) containing a total of 6631 protein coding genes. Comparative analysis identified 1910 core genes common to the four genomes compared (C. necator JMP134, C. necator H16, C. metallidurans CH34, R. sol ...[more]

PMID: 20339589

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Project description:Many bacteria secrete siderophores to enhance iron uptake under iron-restricted conditions. In this study, we found that Cupriavidus necator JMP134, a well-known aromatic pollutant-degrading bacterium, produces an unknown carboxylate-type siderophore named cupriabactin to overcome iron limitation. Using genome mining, targeted mutagenesis, and biochemical analysis, we discovered an operon containing six open reading frames (cubA-F) in the C. necator JMP134 genome that encodes proteins required for the biosynthesis and uptake of cupriabactin. As the dominant siderophore of C. necator JMP134, cupriabactin promotes the growth of C. necator JMP134 under iron-limited conditions via enhanced ferric iron uptake. Furthermore, we demonstrated that the iron concentration-dependent expression of the cub operon is mediated by the ferric uptake regulator (Fur). Physiological analyses revealed that the cupriabactin-mediated iron acquisition system influences swimming motility, biofilm formation, and resistance to oxidative and aromatic compound stress in C. necator JMP134. In conclusion, we identified a carboxylate-type siderophore named cupriabactin, which plays important roles in iron scavenging, bacterial motility, biofilm formation, and stress resistance.IMPORTANCE Since siderophores have been widely exploited for agricultural, environmental, and medical applications, the identification and characterization of new siderophores from different habitats and organisms will have great beneficial applications. Here, we identified a novel siderophore-producing gene cluster in C. necator JMP134. This gene cluster produces a previously unknown carboxylate siderophore, cupriabactin. Physiological analyses revealed that the cupriabactin-mediated iron acquisition system influences swimming motility, biofilm formation, and oxidative stress resistance. Most notably, this system also plays important roles in increasing the resistance of C. necator JMP134 to stress caused by aromatic compounds, which provide a promising strategy to engineer more efficient approaches to degrade aromatic pollutants.

Dataset Information

The complete multipartite genome sequence of Cupriavidus necator JMP134, a versatile pollutant degrader.

Publications

The complete multipartite genome sequence of Cupriavidus necator JMP134, a versatile pollutant degrader.

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