Poor Unstable Midgut Microbiome of Hard Ticks Contrasts With Abundant and Stable Monospecific Microbiome in Ovaries

Guizzo, Melina Garcia; Neupane, Saraswoti; Kučera, Matěj; Perner, Jan; Frantová, Helena; Vaz, Itabajara Junior da Silva; Oliveira, Paulo Roberto; Kopáček, Petr; Zurek, Ludek

doi:10.3389/fcimb.2020.00211

Cited by 42 publications

(54 citation statements)

References 59 publications

(69 reference statements)

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“…However, transcripts receiving an immune label were mainly related to bacterial killing by phagocytosis (ixoderins, plus a set of proteins related to lysosomal function). This is consistent with the digestive function of these cells being exerted by means of digestion of blood proteins in a lysosomal acid compartment and can be related to very low bacterial levels observed in the gut, including during blood feeding 43 , 102 .…”

Section: Resultssupporting

confidence: 84%

“…In ticks, the ovary is the residence of intracellular bacteria symbionts that are essential to tick development [40][41][42] . However, Guizzo et al 43 recently reported a quantitative analysis of the R. microplus microbial www.nature.com/scientificreports/ community revealing that, different from most animals, the tick gut harbors a very modest (if any) resident microbiota, in contrast to the ovary which has a large population of a Coxiella mutualist symbiont, that increase following the blood meal, paralleling the course of ovarian growth 43 . Interesting, Amblyomma sculptum and Amblyomma aureolatum have distinct transcriptional profiles of gut 44 and microbiota composition 45 that can be related to susceptibility to Rickettsia rickettsii.…”

Section: Resultsmentioning

confidence: 99%

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A physiologic overview of the organ-specific transcriptome of the cattle tick Rhipicephalus microplus

Tirloni

Braz

Nunes

et al. 2020

Sci Rep

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To further obtain insights into the Rhipicephalus microplus transcriptome, we used RNA-seq to carry out a study of expression in (i) embryos; (ii) ovaries from partially and fully engorged females; (iii) salivary glands from partially engorged females; (iv) fat body from partially and fully engorged females; and (v) digestive cells from partially, and (vi) fully engorged females. We obtained > 500 million Illumina reads which were assembled de novo, producing > 190,000 contigs, identifying 18,857 coding sequences (CDS). Reads from each library were mapped back into the assembled transcriptome giving a view of gene expression in different tissues. Transcriptomic expression and pathway analysis showed that several genes related in blood digestion and host-parasite interaction were overexpressed in digestive cells compared with other tissues. Furthermore, essential genes for the cell development and embryogenesis were overexpressed in ovaries. Taken altogether, these data offer novel insights into the physiology of production and role of saliva, blood digestion, energy metabolism, and development with submission of 10,932 novel tissue/cell specific CDS to the NCBI database for this important tick species.

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Section: Resultssupporting

confidence: 84%

Section: Resultsmentioning

confidence: 99%

A physiologic overview of the organ-specific transcriptome of the cattle tick Rhipicephalus microplus

Tirloni

Braz

Nunes

et al. 2020

Sci Rep

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“…The microbiota of several tick species of the genera Ixodes, Dermacentor, Haemaphysalis, Rhipicephalus and Amblyomma has been studied (see in [15]) and all these works have given crucial details on microbial communities in ticks and improved our knowledge on tick microbial community ecology. However, few information are currently available on the microbiota composition of the tick Ixodes ricinus [6,12,[16][17][18][19][20][21][22], the predominant tick species in western Europe, able to transmit the largest variety of pathogens, including the Lyme disease agent Borrelia burgdorferi s.l.. Moreover, several of these previous I. ricinus microbiota analyses may have overestimated the microbiota diversity due to extraction step contamination and the lack of controls in their analysis [22].…”

Section: Introductionmentioning

confidence: 99%

Temporal patterns inIxodes ricinusmicrobial communities: an insight into tick-borne microbe interactions

Lejal

Chiquet

Aubert

et al. 2020

Preprint

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BackgroundTicks transmit pathogens of medical and veterinary importance, and represent an increasing threat for human and animal health. Important steps in assessing disease risk and developing possible new future control strategies involve identifying tick-borne microbes, their temporal dynamics and interactions.MethodsUsing high throughput sequencing, we studied the microbiota dynamics of Ixodes ricinus from 371 nymphs collected monthly over three consecutive years in a peri-urban forest. After adjusting a Poisson Log Normal model to our data set, the implementation of a principal component analysis as well as sparse network reconstruction and differential analysis allowed us to assess inter-annual, seasonal and monthly variability of I. ricinus microbial communities as well as their interactions.ResultsAround 75% of the detected sequences belonged to five genera known to be maternally inherited bacteria in arthropods and potentially circulating in ticks: Candidatus Midichloria, Rickettsia, Spiroplasma, Arsenophonus and Wolbachia. The structure of the I. ricinus microbiota was temporally variable with interannual recurrence and seemed to be mainly driven by OTUs belonging to environmental genera. The total network analysis revealed a majority of positive (partial) correlations. We identified strong relationships between OTUs belonging to Wolbachia and Arsenophonus, betraying the presence of the parasitoid wasp Ixodiphagus hookeri in ticks, and the well known arthropod symbiont Spiroplasma, previously documented to be involved in the defense against parasitoid wasp in Drosophila melanogaster. Other associations were observed between the tick symbiont Candidatus Midichloria and pathogens belonging to Rickettsia, probably Rickettsia helvetica. More specific network analysis finally suggested that the presence of pathogens belonging to genera Borrelia, Anaplasma and Rickettsia might disrupt microbial interactions in I. ricinus.ConclusionsHere, we identified the I. ricinus microbiota and documented for the first time the existence and recurrence of marked temporal shifts in the tick microbial community dynamics. We statistically showed strong relationships between the presence of some pathogens and the structure of the I. ricinus non-pathogenic microbes. We interestingly detected close links between some tick symbionts and the potential presence of either pathogenic Rickettsia or a parasitoid in ticks. All these new findings might be very promising for the future development of new control strategies of ticks and tick-borne diseases.

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“…It is known that while CMM is present in the reproductive tissues of female I. ricinus , and it is absent from I. holocyclus [ 46 , 53 ]. The ovarian tissues of all female I. ricinus are known to be dominated by CMM, which forms part of the core microbiota [ 46 , 54 , 55 , 56 , 57 ]. It was found that CMM are lacking in the midgut of I. ricinus , and the midgut did not reflect the presence of a core microbiota and was heavily influenced by host-blood meal [ 54 ].…”

Section: Discussionmentioning

confidence: 99%

Biotic Factors Influence Microbiota of Nymph Ticks from Vegetation in Sydney, Australia

Chandra

Šlapeta

2020

Pathogens

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Ticks are haematophagous ectoparasites of medical and veterinary significance due to their excellent vector capacity. Modern sequencing techniques enabled the rapid sequencing of bacterial pathogens and symbionts. This study’s aims were two-fold; to determine the nymph diversity in Sydney, and to determine whether external biotic factors affect the microbiota. Tick DNA was isolated, and the molecular identity was determined for nymphs at the cox1 level. The tick DNA was subjected to high throughput DNA sequencing to determine the bacterial profile and the impact of biotic factors on the microbiota. Four nymph tick species were recovered from Sydney, NSW: Haemaphysalis bancrofti, Ixodes holocyclus, Ixodes trichosuri and Ixodes tasmani. Biotic factors, notably tick species and geography, were found to have a significance influence on the microbiota. The microbial analyses revealed that Sydney ticks display a core microbiota. The dominating endosymbionts among all tick species were Candidatus Midichloria sp. Ixholo1 and Candidatus Midichloria sp. Ixholo2. A novel Candidatus Midichloria sp. OTU_2090 was only found in I. holocyclus ticks (nymph: 96.3%, adult: 75.6%). Candidatus Neoehrlichia australis and Candidatus Neoehrlichia arcana was recovered from I. holocyclus and one I. trichosuri nymph ticks. Borrelia spp. was absent from all ticks. This study has shown that nymph and adult ticks carry different bacteria, and a tick bite in Sydney, Australia will result in different bacterial transfer depending on tick life stage, tick species and geography.

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Poor Unstable Midgut Microbiome of Hard Ticks Contrasts With Abundant and Stable Monospecific Microbiome in Ovaries

Cited by 42 publications

References 59 publications

A physiologic overview of the organ-specific transcriptome of the cattle tick Rhipicephalus microplus

A physiologic overview of the organ-specific transcriptome of the cattle tick Rhipicephalus microplus

Temporal patterns inIxodes ricinusmicrobial communities: an insight into tick-borne microbe interactions

Biotic Factors Influence Microbiota of Nymph Ticks from Vegetation in Sydney, Australia

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