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Rickettsia buchneri sp. nov., a rickettsial endosymbiont of the blacklegged tick Ixodes scapularis.

ABSTRACT: We obtained a rickettsial isolate from the ovaries of the blacklegged tick, Ixodes scapularis. The isolate (ISO7(T)) was grown in the Ixodes ricinus embryonic cell line IRE11. We characterized the isolate by transmission electron microscopy and gene sequencing. Phylogenetic analysis of 11 housekeeping genes demonstrated that the isolate fulfils the criteria to be classified as a representative of a novel rickettsial species closely related to 'Rickettsia monacensis'. These rickettsiae form a clade separate from other species of rickettsiae. Gene sequences indicated that several genes important in rickettsial motility, invasiveness and temperature adaptation were mutated (e.g. sca2, rickA, hsp22, pldA and htrA). We propose the name Rickettsia buchneri sp. nov. for this bacterium that infects the ovaries of the tick I. scapularis to acknowledge the pioneering contributions of Professor Paul Buchner (1886-1978) to research on bacterial symbionts. The type strain of R. buchneri sp. nov. is strain ISO-7(T) (?=?DSM 29016(T)?=?ATCC VR-1814(T)).

SUBMITTER: Kurtti TJ

PROVIDER: S-EPMC4365292 | biostudies-literature | 2015 Mar

REPOSITORIES: biostudies-literature

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Rickettsia buchneri sp. nov., a rickettsial endosymbiont of the blacklegged tick Ixodes scapularis.

Kurtti Timothy J TJ Felsheim Roderick F RF Burkhardt Nicole Y NY Oliver Jonathan D JD Heu Chan C CC Munderloh Ulrike G UG

International journal of systematic and evolutionary microbiology 20150106 Pt 3

We obtained a rickettsial isolate from the ovaries of the blacklegged tick, Ixodes scapularis. The isolate (ISO7(T)) was grown in the Ixodes ricinus embryonic cell line IRE11. We characterized the isolate by transmission electron microscopy and gene sequencing. Phylogenetic analysis of 11 housekeeping genes demonstrated that the isolate fulfils the criteria to be classified as a representative of a novel rickettsial species closely related to 'Rickettsia monacensis'. These rickettsiae form a cla ...[more]

PMID: 25563918

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Project description:BackgroundThe emergence of vector-borne pathogens in novel geographic areas is regulated by the migration of their arthropod vectors. Blacklegged ticks (Ixodes scapularis) and the pathogens they vector, including the causative agents of Lyme disease, babesiosis and anaplasmosis, continue to grow in their population sizes and to expand in geographic range. Migration of this vector over the previous decades has been implicated as the cause of the re-emergence of the most prevalent infectious diseases in North America.MethodsWe systematically collected ticks from across New York State (hereafter referred to as New York) from 2004 to 2017 as part of routine tick-borne pathogen surveillance in the state. This time frame corresponds with an increase in range and incidence of tick-borne diseases within New York. We randomly sampled ticks from this collection to explore the evolutionary history and population dynamics of I. scapularis. We sequenced the mitochondrial genomes of each tick to characterize their current and historical spatial genetic structure and population growth using phylogeographic methods.ResultsWe sequenced whole mitochondrial genomes from 277 ticks collected across New York between 2004 and 2017. We found evidence of population genetic structure at a broad geographic scale due to differences in the relative abundance, but not the composition, of haplotypes among sampled ticks. Ticks were often most closely related to ticks from the same and nearby collection sites. The data indicate that both short- and long-range migration events shape the population dynamics of blacklegged ticks in New York.ConclusionsWe detailed the population dynamics of the blacklegged tick (Ixodes scapularis) in New York during a time frame in which tick-borne diseases were increasing in range and incidence. Migration of ticks occurred at both coarse and fine scales in the recent past despite evidence of limits to gene flow. Past and current tick population dynamics have implications for further range expansion as habitat suitability for ticks changes due to global climate change. Analyses of mitochondrial genome sequencing data will expound upon previously identified drivers of tick presence and abundance as well as identify additional drivers. These data provide a foundation on which to generate testable hypotheses on the drivers of tick population dynamics occurring at finer scales.

Project description:Ixodes scapularis is the primary vector of tick-borne pathogens in North America but notably does not transmit pathogenic Rickettsia species. This tick harbors the transovarially transmitted endosymbiont Rickettsia buchneri, which is widespread in I. scapularis populations, suggesting that it confers a selective advantage for tick survival such as providing essential nutrients. The R. buchneri genome includes genes with similarity to those involved in antibiotic synthesis. There are two gene clusters not found in other Rickettsiaceae, raising the possibility that these may be involved in excluding pathogenic bacteria from the tick. This study explored whether the R. buchneri antibiotic genes might exert antibiotic effects on pathogens associated with I. scapularis. Markedly reduced infectivity and replication of the tick-borne pathogens Anaplasma phagocytophilum, R. monacensis, and R. parkeri were observed in IRE11 tick cells hosting R. buchneri. Using a fluorescent plate reader assay to follow infection dynamics revealed that the presence of R. buchneri in tick cells, even at low infection rates, inhibited the growth of R. parkeri by 86-100% relative to R. buchneri-free cells. In contrast, presence of the low-pathogenic species R. amblyommatis or the endosymbiont R. peacockii only partially reduced the infection and replication of R. parkeri. Addition of host-cell free R. buchneri, cell lysate of R. buchneri-infected IRE11, or supernatant from R. buchneri-infected IRE11 cultures had no effect on R. parkeri infection and replication in IRE11, nor did these treatments show any antibiotic effect against non-obligate intracellular bacteria E. coli and S. aureus. However, lysate from R. buchneri-infected IRE11 challenged with R. parkeri showed some inhibitory effect on R. parkeri infection of treated IRE11, suggesting that challenge by pathogenic rickettsiae may induce the antibiotic effect of R. buchneri. This research suggests a potential role of the endosymbiont in preventing other rickettsiae from colonizing I. scapularis and/or being transmitted transovarially. The confirmation that the observed inhibition is linked to R. buchneri's antibiotic clusters requires further investigation but could have important implications for our understanding of rickettsial competition and vector competence of I. scapularis for rickettsiae.

Project description:A previously unrecognized Rickettsia species was isolated in 1976 from a pool of Ixodes pacificus ticks collected in 1967 from Tillamook County, Oregon, USA. The isolate produced low fever and mild scrotal oedema following intraperitoneal injection into male guinea pigs (Cavia porcellus). Subsequent serotyping characterized this isolate as distinct from recognized typhus and spotted fever group Rickettsia species; nonetheless, the isolate remained unevaluated by molecular techniques and was not identified to species level for the subsequent 30 years. Ixodes pacificus is the most frequently identified human-biting tick in the western United States, and as such, formal identification and characterization of this potentially pathogenic Rickettsia species is warranted. Whole-genome sequencing of the Tillamook isolate revealed a genome 1.43 Mbp in size with 32.4 mol% G+C content. Maximum-likelihood phylogeny of core proteins places it in the transitional group of Rickettsia basal to both Rickettsia felis and Rickettsia asembonensis. It is distinct from existing named species, with maximum average nucleotide identity of 95.1% to R. asembonensis and maximum digital DNA-DNA hybridization score similarity to R. felis at 80.1%. The closest similarity at the 16S rRNA gene (97.9%) and sca4 (97.5%/97.6% respectively) is to Candidatus 'Rickettsia senegalensis' and Rickettsia sp. cf9, both isolated from cat fleas (Ctenocephalides felis). We characterized growth at various temperatures and in multiple cell lines. The Tillamook isolate grows aerobically in Vero E6, RF/6A and DH82 cells, and growth is rapid at 28 °C and 32 °C. Using accepted genomic criteria, we propose the name Rickettsia tillamookensis sp. nov., with the type strain Tillamook 23. Strain Tillamook 23 is available from the Centers for Disease Control and Prevention Rickettsial Isolate Reference Collection (WDCM 1093), Atlanta, GA, USA (CRIRC accession number RTI001T) and the Collection de Souches de l'Unité des Rickettsies (WDCM 875), Marseille, France (CSUR accession number R5043). Using accepted genomic criteria, we propose the name Rickettsia tillamookensis sp. nov., with the type strain Tillamook 23 (=CRIRC RTI001=R5043).

Dataset Information

Rickettsia buchneri sp. nov., a rickettsial endosymbiont of the blacklegged tick Ixodes scapularis.

Publications

Rickettsia buchneri sp. nov., a rickettsial endosymbiont of the blacklegged tick Ixodes scapularis.

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