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Cofeeding intra- and interspecific transmission of an emerging insect-borne rickettsial pathogen.

ABSTRACT: Cat fleas (Ctenocephalides felis) are known as the primary vector and reservoir of Rickettsia felis, the causative agent of flea-borne spotted fever; however, field surveys regularly report molecular detection of this infectious agent from other blood-feeding arthropods. The presence of R. felis in additional arthropods may be the result of chance consumption of an infectious bloodmeal, but isolation of viable rickettsiae circulating in the blood of suspected vertebrate reservoirs has not been demonstrated. Successful transmission of pathogens between actively blood-feeding arthropods in the absence of a disseminated vertebrate infection has been verified, referred to as cofeeding transmission. Therefore, the principal route from systemically infected vertebrates to uninfected arthropods may not be applicable to the R. felis transmission cycle. Here, we show both intra- and interspecific transmission of R. felis between cofeeding arthropods on a vertebrate host. Analyses revealed that infected cat fleas transmitted R. felis to naïve cat fleas and rat fleas (Xenopsylla cheopis) via fleabite on a nonrickettsemic vertebrate host. Also, cat fleas infected by cofeeding were infectious to newly emerged uninfected cat fleas in an artificial system. Furthermore, we utilized a stochastic model to demonstrate that cofeeding is sufficient to explain the enzootic spread of R. felis amongst populations of the biological vector. Our results implicate cat fleas in the spread of R. felis amongst different vectors, and the demonstration of cofeeding transmission of R. felis through a vertebrate host represents a novel transmission paradigm for insect-borne Rickettsia and furthers our understanding of this emerging rickettsiosis.

SUBMITTER: Brown LD

PROVIDER: S-EPMC4831916 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND:Vector-borne pathogens must overcome arthropod infection and escape barriers (e.g. midgut and salivary glands) during the extrinsic incubation period (EIP) before subsequent transmission to another host. This particular timespan is undetermined for the etiological agent of flea-borne spotted fever (Rickettsia felis). Artificial acquisition of R. felis by blood-feeding cat fleas revealed dissemination to the salivary glands after seven days; however, this length of time is inconsistent with co-feeding studies that produced infectious cat fleas within 24 h of infection. In the current study, we demonstrated that an alternative mechanism is responsible for the early-phase transmission that typifies flea-borne R. felis spread. METHODS:Co-feeding transmission bioassays were constructed to assess temporal dynamics of R. felis amongst cat fleas, including exposure time to produce infectious fleas and association time to transmit infection to naïve fleas. Additional experiments examined the proportion of R. felis-exposed cat fleas with contaminated mouthparts, as well as the likelihood for cat fleas to release R. felis from their mouthparts following exposure to an infectious bloodmeal. The potential for mechanical transmission of R. felis by co-feeding cat fleas was further examined using fluorescent latex beads, as opposed to a live pathogen, which would not require a biological mechanism to achieve transmission. RESULTS:Analyses revealed that R. felis-infected cat fleas were infectious to naïve fleas less than 24 h after exposure to the pathogen, but showed no rickettsial dissemination to the salivary glands during this early-phase transmission. Additionally, the current study revealed that R. felis-infected cat fleas must co-feed with naïve fleas for more than 12 h in order for early-phase transmission to occur. Further evidence supported that contaminated flea mouthparts may be the source of the bacteria transmitted early, and demonstrated that R. felis is released from the mouthparts during brief probing events. Moreover, the use of fluorescent latex beads supports the notion that early-phase transmission of R. felis is a mechanical mechanism. CONCLUSIONS:Determination of the transmission mechanisms utilized by R. felis is essential to fully understand the vulnerability of susceptible vertebrate hosts, including humans, to this pathogen.

Project description:BACKGROUND:The Gram-negative bacterium Photorhabdus asymbiotica (Pa) has been recovered from human infections in both North America and Australia. Recently, Pa has been shown to have a nematode vector that can also infect insects, like its sister species the insect pathogen P. luminescens (Pl). To understand the relationship between pathogenicity to insects and humans in Photorhabdus we have sequenced the complete genome of Pa strain ATCC43949 from North America. This strain (formerly referred to as Xenorhabdus luminescens strain 2) was isolated in 1977 from the blood of an 80 year old female patient with endocarditis, in Maryland, USA. Here we compare the complete genome of Pa ATCC43949 with that of the previously sequenced insect pathogen P. luminescens strain TT01 which was isolated from its entomopathogenic nematode vector collected from soil in Trinidad and Tobago. RESULTS:We found that the human pathogen Pa had a smaller genome (5,064,808 bp) than that of the insect pathogen Pl (5,688,987 bp) but that each pathogen carries approximately one megabase of DNA that is unique to each strain. The reduced size of the Pa genome is associated with a smaller diversity in insecticidal genes such as those encoding the Toxin complexes (Tc's), Makes caterpillars floppy (Mcf) toxins and the Photorhabdus Virulence Cassettes (PVCs). The Pa genome, however, also shows the addition of a plasmid related to pMT1 from Yersinia pestis and several novel pathogenicity islands including a novel Type Three Secretion System (TTSS) encoding island. Together these data suggest that Pa may show virulence against man via the acquisition of the pMT1-like plasmid and specific effectors, such as SopB, that promote its persistence inside human macrophages. Interestingly the loss of insecticidal genes in Pa is not reflected by a loss of pathogenicity towards insects. CONCLUSION:Our results suggest that North American isolates of Pa have acquired virulence against man via the acquisition of a plasmid and specific virulence factors with similarity to those shown to play roles in pathogenicity against humans in other bacteria.

Project description:Intraspecies (homologous) phylogenetic incongruence, or 'tree conflict' between different loci within the same genome of mosquito-borne flaviviruses (MBFV), was first identified in dengue virus (DENV) and subsequently in Japanese encephalitis virus (JEV), St Louis encephalitis virus, and Zika virus (ZIKV). Recently, the first evidence of phylogenetic incongruence between interspecific members of the MBFV was reported in ZIKV and its close relative, Spondweni virus. Uniquely, these hybrid proteomes were derived from four incongruent trees involving an Aedes-associated DENV node (1 tree) and three different Culex-associated flavivirus nodes (3 trees). This analysis has now been extended across a wider spectrum of viruses within the MBFV lineage targeting the breakpoints between phylogenetic incongruent loci originally identified in ZIKV. Interspecies phylogenetic incongruence at these breakpoints was identified in 10 of 50 viruses within the MBFV lineage, representing emergent Aedes and Culex-associated viruses including JEV, West Nile virus, yellow fever virus, and insect-specific viruses. Thus, interspecies phylogenetic incongruence is widespread amongst the flaviviruses and is robustly associated with the specific breakpoints that coincide with the interspecific phylogenetic incongruence previously identified, inferring they are 'hotspots'. The incongruence amongst the emergent MBFV group was restricted to viruses within their respective associated epidemiological boundaries. This MBFV group was RY-coded at the third codon position ('wobble codon') to remove transition saturation. The resulting 'wobble codon' trees presented a single topology for the entire genome that lacked any robust evidence of phylogenetic incongruence between loci. Phylogenetic interspecific incongruence was therefore observed for exactly the same loci between amino acid and the RY-coded 'wobble codon' alignments and this incongruence represented either a major part, or the entire genomes. Maximum likelihood codon analysis revealed positive selection for the incongruent lineages. Positive selection could result in the same locus producing two opposing trees. These analyses for the clinically important MBFV suggest that robust interspecific phylogenetic incongruence resulted from amino acid selection. Convergent or parallel evolutions are evolutionary processes that would explain the observation, whilst interspecific recombination is unlikely.

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Cofeeding intra- and interspecific transmission of an emerging insect-borne rickettsial pathogen.

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