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Wide dispersal and possible multiple origins of low-copy-number plasmids in rickettsia species associated with blood-feeding arthropods.

ABSTRACT: Plasmids are mobile genetic elements of bacteria that can impart important adaptive traits, such as increased virulence or antibiotic resistance. We report the existence of plasmids in Rickettsia (Rickettsiales; Rickettsiaceae) species, including Rickettsia akari, "Candidatus Rickettsia amblyommii," R. bellii, R. rhipicephali, and REIS, the rickettsial endosymbiont of Ixodes scapularis. All of the rickettsiae were isolated from humans or North and South American ticks. R. parkeri isolates from both continents did not possess plasmids. We have now demonstrated plasmids in nearly all Rickettsia species that we have surveyed from three continents, which represent three of the four major proposed phylogenetic groups associated with blood-feeding arthropods. Gel-based evidence consistent with the existence of multiple plasmids in some species was confirmed by cloning plasmids with very different sequences from each of two "Ca. Rickettsia amblyommii" isolates. Phylogenetic analysis of rickettsial ParA plasmid partitioning proteins indicated multiple parA gene origins and plasmid incompatibility groups, consistent with possible multiple plasmid origins. Phylogenetic analysis of potentially host-adaptive rickettsial small heat shock proteins showed that hsp2 genes were plasmid specific and that hsp1 genes, found only on plasmids of "Ca. Rickettsia amblyommii," R. felis, R. monacensis, and R. peacockii, were probably acquired independently of the hsp2 genes. Plasmid copy numbers in seven Rickettsia species ranged from 2.4 to 9.2 per chromosomal equivalent, as determined by real-time quantitative PCR. Plasmids may be of significance in rickettsial evolution and epidemiology by conferring genetic plasticity and host-adaptive traits via horizontal gene transfer that counteracts the reductive genome evolution typical of obligate intracellular bacteria.

SUBMITTER: Baldridge GD

PROVIDER: S-EPMC2838022 | biostudies-literature | 2010 Mar

REPOSITORIES: biostudies-literature

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Wide dispersal and possible multiple origins of low-copy-number plasmids in rickettsia species associated with blood-feeding arthropods.

Baldridge Gerald D GD Burkhardt Nicole Y NY Labruna Marcelo B MB Pacheco Richard C RC Paddock Christopher D CD Williamson Philip C PC Billingsley Peggy M PM Felsheim Roderick F RF Kurtti Timothy J TJ Munderloh Ulrike G UG

Applied and environmental microbiology 20100122 6

Plasmids are mobile genetic elements of bacteria that can impart important adaptive traits, such as increased virulence or antibiotic resistance. We report the existence of plasmids in Rickettsia (Rickettsiales; Rickettsiaceae) species, including Rickettsia akari, "Candidatus Rickettsia amblyommii," R. bellii, R. rhipicephali, and REIS, the rickettsial endosymbiont of Ixodes scapularis. All of the rickettsiae were isolated from humans or North and South American ticks. R. parkeri isolates from b ...[more]

PMID: 20097813

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Project description:Bacterial plasmids are extrachromosomal DNA that provides selective advantages for bacterial survival. Plasmid partitioning can be remarkably robust. For high-copy-number plasmids, diffusion ensures that both daughter cells inherit plasmids after cell division. In contrast, most low-copy-number plasmids need to be actively partitioned by a conserved tripartite ParA-type system. ParA is an ATPase that binds to chromosomal DNA; ParB is the stimulator of the ParA ATPase and specifically binds to the plasmid at a centromere-like site, parS. ParB stimulation of the ParA ATPase releases ParA from the bacterial chromosome, after which it takes a long time to reset its DNA-binding affinity. We previously demonstrated in vitro that the ParA system can exploit this biochemical asymmetry for directed cargo transport. Multiple ParA-ParB bonds can bridge a parS-coated cargo to a DNA carpet, and they can work collectively as a Brownian ratchet that directs persistent cargo movement with a ParA-depletion zone trailing behind. By extending this model, we suggest that a similar Brownian ratchet mechanism recapitulates the full range of actively segregated plasmid motilities observed in vivo. We demonstrate that plasmid motility is tuned as the replenishment rate of the ParA-depletion zone progressively increases relative to the cargo speed, evolving from diffusion to pole-to-pole oscillation, local excursions, and, finally, immobility. When the plasmid replicates, the daughters largely display motilities similar to that of their mother, except that when the single-focus progenitor is locally excursive, the daughter foci undergo directed segregation. We show that directed segregation maximizes the fidelity of plasmid partition. Given that local excursion and directed segregation are the most commonly observed modes of plasmid motility in vivo, we suggest that the operation of the ParA-type partition system has been shaped by evolution for high fidelity of plasmid segregation.

Project description:BackgroundFeeding costs represent the largest expenditures in beef production. Therefore, the animal efficiency in converting feed in high-quality protein for human consumption plays a major role in the environmental impact of the beef industry and in the beef producers' profitability. In this context, breeding animals for improved feed efficiency through genomic selection has been considered as a strategic practice in modern breeding programs around the world. Copy number variation (CNV) is a less-studied source of genetic variation that can contribute to phenotypic variability in complex traits. In this context, this study aimed to: (1) identify CNV and CNV regions (CNVRs) in the genome of Nellore cattle (Bos taurus indicus); (2) assess potential associations between the identified CNVR and weaning weight (W210), body weight measured at the time of selection (WSel), average daily gain (ADG), dry matter intake (DMI), residual feed intake (RFI), time spent at the feed bunk (TF), and frequency of visits to the feed bunk (FF); and, (3) perform functional enrichment analyses of the significant CNVR identified for each of the traits evaluated.ResultsA total of 3,161 CNVs and 561 CNVRs ranging from 4,973 bp to 3,215,394 bp were identified. The CNVRs covered up to 99,221,894 bp (3.99%) of the Nellore autosomal genome. Seventeen CNVR were significantly associated with dry matter intake and feeding frequency (number of daily visits to the feed bunk). The functional annotation of the associated CNVRs revealed important candidate genes related to metabolism that may be associated with the phenotypic expression of the evaluated traits. Furthermore, Gene Ontology (GO) analyses revealed 19 enrichment processes associated with FF.ConclusionsA total of 3,161 CNVs and 561 CNVRs were identified and characterized in a Nellore cattle population. Various CNVRs were significantly associated with DMI and FF, indicating that CNVs play an important role in key biological pathways and in the phenotypic expression of feeding behavior and growth traits in Nellore cattle.

Dataset Information

Wide dispersal and possible multiple origins of low-copy-number plasmids in rickettsia species associated with blood-feeding arthropods.

Publications

Wide dispersal and possible multiple origins of low-copy-number plasmids in rickettsia species associated with blood-feeding arthropods.

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