Tick-borne Apicomplexa in wildlife and ticks of French Guiana.

Tick-borne Apicomplexa encompass a group of parasites responsible for significant medical and veterinary diseases, including babesiosis, theileriosis, and hepatozoonosis. In this study, we investigated the presence and diversity of tick-borne Apicomplexa in wildlife and ticks inhabiting the Amazon rainforests of French Guiana. To this end, we conducted molecular screening and typing using 18S rRNA sequences on a collection of 1161 specimens belonging to 71 species, including 44 species of wild mammals, five species of passerines, and 22 species of ticks. We characterized eight genovariants of Babesia, Theileria, Hemolivia, and Hepatozoon parasites, some matching known species, while others suggested potential novel species. These parasites were detected in wild mammals, including opossums, sloths, armadillos, porcupines, margays, greater grisons, and ticks, but not in passerines. Finally, similarities with surveys conducted in Brazil highlight the specific sylvatic transmission cycles of South American tick-borne Apicomplexa.

Title: Apicomplexes transmis par les tiques chez la faune sauvage et les tiques de Guyane française. Abstract: Les Apicomplexes transmis par les tiques englobent un groupe de parasites responsables de maladies médicales et vétérinaires importantes, notamment la babésiose, la theilériose et l'hépatozoonose. Dans cette étude, nous avons étudié la présence et la diversité des Apicomplexes transmis par les tiques dans la faune sauvage et les tiques habitant les forêts tropicales amazoniennes de Guyane française. À cette fin, nous avons effectué un criblage moléculaire et un typage à l'aide de séquences d'ARNr 18S sur une collection de 1 161 spécimens appartenant à 71 espèces, dont 44 espèces de mammifères sauvages, cinq espèces de passereaux et 22 espèces de tiques. Nous avons caractérisé huit génovariants des parasites Babesia, Theileria, Hemolivia et Hepatozoon, certains correspondant à des espèces connues tandis que d'autres suggéraient de nouvelles espèces potentielles. Ces parasites ont été détectés chez des mammifères sauvages, dont des opossums, des paresseux, des tatous, des porcs-épics, des margays, des grisons et des tiques, mais pas chez des passereaux. Enfin, des similitudes avec des enquêtes menées au Brésil mettent en évidence les cycles de transmission sylvatiques spécifiques des Apicomplexa transmis par les tiques d'Amérique du Sud.

Reassessment of the genetic basis of natural rifampin resistance in the genus Rickettsia.

Rickettsia, a genus of obligate intracellular bacteria, includes species that cause significant human diseases. This study challenges previous claims that the Leucine-973 residue in the RNA polymerase beta subunit is the primary determinant of rifampin resistance in Rickettsia. We investigated a previously untested Rickettsia species, R. lusitaniae, from the Transitional group and found it susceptible to rifampin, despite possessing the Leu-973 residue. Interestingly, we observed the conservation of this residue in several rifampin-susceptible species across most Rickettsia phylogenetic groups. Comparative genomics revealed potential alternative resistance mechanisms, including additional amino acid variants that could hinder rifampin binding and genes that could facilitate rifampin detoxification through efflux pumps. Importantly, the evolutionary history of Rickettsia genomes indicates that the emergence of natural rifampin resistance is phylogenetically constrained within the genus, originating from ancient genetic features shared among a unique set of closely related Rickettsia species. Phylogenetic patterns appear to be the most reliable predictors of natural rifampin resistance, which is confined to a distinct monophyletic subclade known as Massiliae. The distinctive features of the RNA polymerase beta subunit in certain untested Rickettsia species suggest that R. raoultii, R. amblyommatis, R. gravesii, and R. kotlanii may also be naturally rifampin-resistant species.

Wolbachia populations across organs of individual Culex pipiens: highly conserved intra-individual core pangenome with inter-individual polymorphisms.

Wolbachia is a maternally inherited intracellular bacterium that infects a wide range of arthropods including mosquitoes. The endosymbiont is widely used in biocontrol strategies due to its capacity to modulate arthropod reproduction and limit pathogen transmission. Wolbachia infections in Culex spp. are generally assumed to be monoclonal but the potential presence of genetically distinct Wolbachia subpopulations within and between individual organs has not been investigated using whole genome sequencing. Here we reconstructed Wolbachia genomes from ovary and midgut metagenomes of single naturally infected Culex pipiens mosquitoes from Southern France to investigate patterns of intra- and inter-individual differences across mosquito organs. Our analyses revealed a remarkable degree of intra-individual conservancy among Wolbachia genomes from distinct organs of the same mosquito both at the level of gene presence-absence signal and single-nucleotide polymorphisms (SNPs). Yet, we identified several synonymous and non-synonymous substitutions between individuals, demonstrating the presence of some level of genomic heterogeneity among Wolbachia that infect the same C. pipiens field population. Overall, the absence of genetic heterogeneity within Wolbachia populations in a single individual confirms the presence of a dominant Wolbachia that is maintained under strong purifying forces of evolution.

Nutritional symbiosis in ticks: singularities of the genus Ixodes.

Symbiosis with intracellular bacteria is essential for the nutrition of ticks, particularly through the biosynthesis of B vitamins. Yet, ticks of the genus Ixodes, which include major vectors of human pathogens, lack the nutritional symbionts usually found in other tick genera. This paradox raises questions about the mechanisms that Ixodes ticks use to prevent nutritional deficiencies. Nonetheless, Ixodes ticks commonly harbor other symbionts belonging to the order Rickettsiales. Although these obligate intracellular bacteria are primarily known as human pathogens, Rickettsiales symbionts often dominate the Ixodes microbial community without causing diseases. They also significantly influence Ixodes physiology, synthesize key B vitamins, and are crucial for immatures. These findings underscore unique associations between Rickettsiales and Ixodes ticks distinct from other tick genera.

Detection of Anaplasma and Ehrlichia bacteria in humans, wildlife, and ticks in the Amazon rainforest.

Tick-borne bacteria of the genera Ehrlichia and Anaplasma cause several emerging human infectious diseases worldwide. In this study, we conduct an extensive survey for Ehrlichia and Anaplasma infections in the rainforests of the Amazon biome of French Guiana. Through molecular genetics and metagenomics reconstruction, we observe a high indigenous biodiversity of infections circulating among humans, wildlife, and ticks inhabiting these ecosystems. Molecular typing identifies these infections as highly endemic, with a majority of new strains and putative species specific to French Guiana. They are detected in unusual rainforest wild animals, suggesting they have distinctive sylvatic transmission cycles. They also present potential health hazards, as revealed by the detection of Candidatus Anaplasma sparouinense in human red blood cells and that of a new close relative of the human pathogen Ehrlichia ewingii, Candidatus Ehrlichia cajennense, in the tick species that most frequently bite humans in South America. The genome assembly of three new putative species obtained from human, sloth, and tick metagenomes further reveals the presence of major homologs of Ehrlichia and Anaplasma virulence factors. These observations converge to classify health hazards associated with Ehrlichia and Anaplasma infections in the Amazon biome as distinct from those in the Northern Hemisphere.

Multi-locus sequence analysis unveils a novel genus of filarial nematodes associated with ticks in French Guiana.

Filarial nematodes of the Dipetalonema lineage include tick-borne filarioids that infect both domestic and wild vertebrate hosts, but they remain understudied in many cases. In this study, we conducted a molecular characterization of a Dipetalonema-like filarioid (DLF) recently identified in two tick species in French Guiana, South America. While the cox1 mitochondrial gene was the sole marker initially sequenced for describing DLF, its classification and phylogenetic relationship with other members of the Dipetalonema lineage were unclear. Therefore, we better characterized DLF through the sequencing of six additional gene markers and conducted phylogenetic analyses. Based on this multi-locus typing scheme, DLF exhibited significant divergence from known genera and species of filarioids, or other sequences available in public databases, suggesting its potential classification as a novel genus within the Dipetalonema lineage. Phylogenetic analyses further unveiled a close evolutionary relationship between DLF and all other filarioids associated with Acari (ticks and mites) within a robust monophyletic subclade in the Dipetalonema lineage. Overall, these findings confirm the existence of a specialized, Acari-borne group of filarioids and underscore the need for comprehensive investigations into their epidemiology and potential impact on animal health.

Title: Une analyse de séquences multi-locus dévoile un nouveau genre de nématodes filaires, associé aux tiques en Guyane française. Abstract: Les filaires de la lignée Dipetalonema comprennent des espèces transmises par les tiques qui infectent à la fois des hôtes vertébrés domestiques et sauvages, mais qui restent sous-étudiées dans de nombreux cas. Dans cette étude, nous avons réalisé une caractérisation moléculaire d'un filarioïde ressemblant à Dipetalonema (FRD) récemment identifié dans deux espèces de tiques en Guyane française. Alors que la séquence du gène mitochondrial cox1 était le seul marqueur génétique initialement séquencé pour décrire FRD, sa classification et sa relation phylogénétique avec d'autres membres de la lignée Dipetalonema étaient incertaines. Par conséquent, nous avons caractérisé plus précisément DLF en séquençant six gènes supplémentaires et en réalisant des analyses phylogénétiques. Sur la base de ce typage multi-locus, FRD présentait une divergence significative par rapport aux genres et espèces connus de filarioïdes, ou à d'autres séquences disponibles dans les bases de données publiques, suggérant sa classification potentielle en tant que nouveau genre au sein de la lignée Dipetalonema. Les analyses phylogénétiques ont en outre révélé une relation évolutive étroite entre FRD et tous les autres filarioïdes associés aux tiques et acariens au sein d'un sous-clade monophylétique dans la lignée Dipetalonema. Dans l'ensemble, ces résultats confirment l'existence d'un groupe spécialisé de filarioïdes transmis par les tiques et acariens et soulignent la nécessité d'études approfondies sur leur épidémiologie et leur impact potentiel sur la santé animale.

Limited association between Wolbachia and Plasmodium falciparum infections in natural populations of the major malaria mosquito Anopheles moucheti.

Since the discovery of natural malaria vector populations infected by the endosymbiont bacterium Wolbachia, a renewed interest has arisen for using this bacterium as an alternative for malaria control. Among naturally infected mosquitoes, Anopheles moucheti, a major malaria mosquito in Central Africa, exhibits one of the highest prevalences of Wolbachia infection. To better understand whether this maternally inherited bacterium could be used for malaria control, we investigated Wolbachia influence in An. moucheti populations naturally infected by the malaria parasite Plasmodium falciparum. To this end, we collected mosquitoes in a village from Cameroon, Central Africa, where this mosquito is the main malaria vector. We found that the prevalence of Wolbachia bacterium was almost fixed in the studied mosquito population, and was higher than previously recorded. We also quantified Wolbachia in whole mosquitoes and dissected abdomens, confirming that the bacterium is also elsewhere than in the abdomen, but at lower density. Finally, we analyzed the association of Wolbachia presence and density on P. falciparum infection. Wolbachia density was slightly higher in mosquitoes infected with the malaria parasite than in uninfected mosquitoes. However, we observed no correlation between the P. falciparum and Wolbachia densities. In conclusion, our study indicates that naturally occurring Wolbachia infection is not associated to P. falciparum development within An. moucheti mosquitoes.

Cross-alteration of murine skin and tick microbiome concomitant with pathogen transmission after Ixodes ricinus bite.

BACKGROUND: Ticks are major vectors of diseases affecting humans such as Lyme disease or domestic animals such as anaplasmosis. Cross-alteration of the vertebrate host skin microbiome and the tick microbiome may be essential during the process of tick feeding and for the mechanism of pathogen transmission. However, it has been poorly investigated. METHODS: We used mice bitten by field-collected ticks (nymphs and adult ticks) in different experimental conditions to investigate, by 16S rRNA gene metabarcoding, the impact of blood feeding on both the mouse skin microbiome and the tick microbiome. We also investigated by PCR and 16S rRNA gene metabarcoding, the diversity of microorganisms transmitted to the host during the process of tick bite at the skin interface and the dissemination of the pathogen in host tissues (blood, heart, and spleen). RESULTS: Most of the commensal bacteria present in the skin of control mice were replaced during the blood-feeding process by bacteria originating from the ticks. The microbiome of the ticks was also impacted by the blood feeding. Several pathogens including tick-borne pathogens (Borrelia/Borreliella, Anaplasma, Neoehrlichia, Rickettsia) and opportunistic bacteria (Williamsia) were transmitted to the skin microbiome and some of them disseminated to the blood or spleen of the mice. In the different experiments of this study, skin microbiome alteration and Borrelia/Borreliella transmission were different depending on the tick stages (nymphs or adult female ticks). CONCLUSIONS: Host skin microbiome at the bite site was deeply impacted by the tick bite, to an extent which suggests a role in the tick feeding, in the pathogen transmission, and a potentially important impact on the skin physiopathology. The diversified taxonomic profiles of the tick microbiome were also modified by the blood feeding. Video Abstract.

Molecular detection of Cercopithifilaria, Cruorifilaria and Dipetalonema-like filarial nematodes in ticks of French Guiana.

Filarial nematodes of the Dipetalonema lineage are widespread parasites and include some species that are transmitted by ticks. In this study, we conducted a large molecular survey of ticks in French Guiana, South America, to understand the overall diversity of tick-borne filarioids in this remote region largely covered by dense tropical forests. Out of 682 ticks belonging to 22 species and 6 genera, 21 ticks (3.1%) of the species Amblyomma cajennense, A. oblongoguttatum, A. romitii, Ixodes luciae and Rhipicephalus sanguineus sensu lato were positive for infection by filarioids. Molecular typing and phylogenetic analysis identified all these filarioids as members of the Dipetalonema lineage. While the filarioid of R. sanguineus sensu lato is a previously described species, the canine worm Cercopithifilaria bainae Almeida & Vicente, 1984, all other filarioids detected in this study are related but distinct to already known species in the genera Cercopithifilaria, Cruorifilaria and Dipetalonema. Their vertebrate host range may include a wide variety of mammals present in French Guiana, but dogs, capybaras, and opossums are the best candidate hosts for some of these filarioids. Although the detection of members of the Dipetalonema lineage in ticks of significant medical or veterinary interest is of concern, the risk of contracting a tick-borne filarial infection is still largely unknown. The pathogenicity of these filarioids, their epidemiology, developmental cycles, and mechanisms of transmission by South American tick species now require further study.

Title: Détection moléculaire des nématodes filaires de type Cercopithifilaria, Cruorifilaria et Dipetalonema chez les tiques de Guyane française. Abstract: Les nématodes filaires de la lignée Dipetalonema sont des parasites répandus dont plusieurs espèces sont transmises par les tiques. Dans cette étude, nous avons mené une vaste surveillance moléculaire des tiques en Guyane française, en Amérique du Sud, afin de caractériser la diversité des filaires transmis par les tiques dans cette région largement couverte de forêts tropicales denses. Sur 682 tiques appartenant à 22 espèces et 6 genres, 21 tiques (3.1 %) des espèces Amblyomma cajennense, A. oblongoguttatum, A. romitii, Ixodes luciae et Rhipicephalus sanguineus sensu lato étaient positives pour la détection des filaires. Le typage moléculaire et l'analyse phylogénétique ont permis d'identifier toutes ces filaires comme des membres de la lignée Dipetalonema. Alors que la filaire de R. sanguineus sensu lato est une espèce décrite, la filaire canine Cercopithifilaria bainae Almeida & Vicente, 1984, toutes les autres filaires détectées ici sont apparentées mais distinctes des espèces déjà connues au sein des genres Cercopithifilaria, Cruorifilaria et Dipetalonema. Leur spectre d'hôtes vertébrés pourrait inclure une grande variété de mammifères présents en Guyane française, mais les chiens, les capibaras et les opossums sont les hôtes candidats probables pour certaines de ces filaires. Bien que la détection de membres de la lignée Dipetalonema chez des tiques d'intérêt médical ou vétérinaire soit préoccupante, le risque de contracter une filariose à tiques est encore largement inconnu. La pathogénicité de ces filaires à tiques, leur épidémiologie, leurs cycles de développement et les mécanismes de transmission par les espèces de tiques sud-américaines doivent maintenant être étudiés plus en détail.

The evolution of intramitochondriality in Midichloria bacteria.

Midichloria spp. are intracellular bacterial symbionts of ticks. Representatives of this genus colonise mitochondria in the cells of their hosts. To shed light on this unique interaction we evaluated the presence of an intramitochondrial localization for three Midichloria in the respective tick host species and generated eight high-quality draft genomes and one closed genome, showing that this trait is non-monophyletic, either due to losses or multiple acquisitions. Comparative genomics supports the first hypothesis, as the genomes of non-mitochondrial symbionts are reduced subsets of those capable of colonising the organelles. We detect genomic signatures of mitochondrial tropism, including the differential presence of type IV secretion system and flagellum, which could allow the secretion of unique effectors and/or direct interaction with mitochondria. Other genes, including adhesion molecules, proteins involved in actin polymerisation, cell wall and outer membrane proteins, are only present in mitochondrial symbionts. The bacteria could use these to manipulate host structures, including mitochondrial membranes, to fuse with the organelles or manipulate the mitochondrial network.

Diversity and phylogeny of the tick-borne bacterial genus Candidatus Allocryptoplasma (Anaplasmataceae).

The family Anaplasmataceae includes tick-borne bacteria of major public and veterinary health interest, as best illustrated by members of the genera Anaplasma and Ehrlichia. Recent epidemiological surveys have also reported on the presence of a novel putative genus in the Anaplasmataceae, Candidatus Allocryptoplasma, previously described as Candidatus Cryptoplasma in the western black-legged tick, Ixodes pacificus. However, the genetic diversity of Ca. Allocryptoplasma and its phylogenetic relationship with other Anaplasmataceae remain unclear. In this study, we developed a multi-locus sequence typing approach, examining the DNA sequence variation at five genes of Ca. Allocryptoplasma found in ticks. Combining this multi-locus sequence typing and genetic data available on public databases, we found that substantial genetic diversity of Ca. Allocryptoplasma is present in Ixodes, Amblyomma and Haemaphysalis spp. ticks on most continents. Further analyses confirmed that the Ca. Allocryptoplasma of ticks, the Ca. Allocryptoplasma of lizards and some Anaplasma-like bacteria of wild mice cluster into a monophyletic genus, divergent from all other genera of the family Anaplasmataceae. Candidatus Allocryptoplasma appears as a sister genus of Anaplasma and, with the genera Ehrlichia and Neoehrlichia, they form a monophyletic subgroup of Anaplasmataceae associated with tick-borne diseases. The detection of genetically distinct Ca. Allocryptoplasma in ticks of significant medical or veterinary interest supports the hypothesis that it is an emergent genus of tick-borne pathogens of general concern.

Title: Diversité et phylogénie du genre bactérien transmis par les tiques Candidatus Allocryptoplasma (Anaplasmataceae). Abstract: La famille des Anaplasmataceae comprend des bactéries transmises par les tiques qui présentent un intérêt majeur pour la santé publique et vétérinaire, comme les membres des genres Anaplasma et Ehrlichia. Des surveillances épidémiologiques récentes ont également signalé la présence d'un nouveau genre putatif dans les Anaplasmataceae, Candidatus Allocryptoplasma, initialement décrit comme Ca. Cryptoplasma chez une tique nord-américaine, Ixodes pacificus. Cependant, la diversité génétique des bactéries Ca. Allocryptoplasma et leurs relations phylogénétiques avec d'autres Anaplasmataceae restent méconnues. Dans cette étude, nous avons développé une approche de typage génétique multi-locus, en examinant la variation nucléotidique pour cinq gènes de bactéries Ca. Allocryptoplasma détectées chez les tiques. En combinant ce typage génétique multi-locus et les données génétiques disponibles dans les bases de données publiques, nous avons mis en évidence qu'une diversité génétique substantielle des bactéries Ca. Allocryptoplasma est présente chez les tiques des genres Ixodes, Amblyomma et Haemaphysalis sur la plupart des continents. Des analyses complémentaires confirment que les bactéries Ca. Allocryptoplasma des tiques, les bactéries Ca. Allocryptoplasma de lézards et des bactéries Anaplasma-like de souris sauvages se regroupent dans un genre monophylétique, divergent de tous les autres genres de la famille Anaplasmataceae. Candidatus Allocryptoplasma apparaît comme un genre frère d'Anaplasma et, avec les genres Ehrlichia et Neoehrlichia, ces trois genres forment un sous-groupe monophylétique d'Anaplasmataceae associé aux maladies transmises par les tiques. La détection de Ca. Allocryptoplasma dans des tiques d'intérêt médical et vétérinaire soutient l'hypothèse qu'il s'agit d'un genre émergent d'agents pathogènes majeurs.

Emerging infectious diseases and new pandemics: dancing with a ghost! Lessons in inter- and transdisciplinary research in French Guiana, South America.

In light of current international public health challenges, calls for inter- and transdisciplinary research are increasing, particularly in response to complex and intersecting issues. Although widely used under the One Health flag, it is still unclear how inter- and transdisciplinary science should be applied to infectious disease research, public health, and the different stakeholders. Here, we present and discuss our common scientific and biomedical experience in French Guiana, South America to conduct and enrich research in vector-borne and zoonotic infectious diseases, with the aim to translate findings to public health and political stakeholders. We highlight the successful progressive dissolution of disciplinary boundaries that go beyond One Health positive-driven assumptions and argue that specific local conditions, as well as strong support from research and medical institutions, have facilitated an emulsion toward inter- and transdisciplinary science. This argument is intended to improve responses to public health concerns in French Guiana and other countries and regions of the world.

Phylogenetic evidence for a clade of tick-associated trypanosomes.

BACKGROUND: Trypanosomes are protozoan parasites of vertebrates that are of medical and veterinary concern. A variety of blood-feeding invertebrates have been identified as vectors, but the role of ticks in trypanosome transmission remains unclear. METHODS: In this study, we undertook extensive molecular screening for the presence and genetic diversity of trypanosomes in field ticks. RESULTS: Examination of 1089 specimens belonging to 28 tick species from Europe and South America led to the identification of two new trypanosome strains. The prevalence may be as high as 4% in tick species such as the castor bean tick Ixodes ricinus, but we found no evidence of transovarial transmission. Further phylogenetic analyses based on 18S rRNA, EF1-α, hsp60 and hsp85 gene sequences revealed that different tick species, originating from different continents, often harbour phylogenetically related trypanosome strains and species. Most tick-associated trypanosomes cluster in a monophyletic clade, the Trypanosoma pestanai clade, distinct from clades of trypanosomes associated with transmission by other blood-feeding invertebrates. CONCLUSIONS: These observations suggest that ticks may be specific arthropod hosts for trypanosomes of the T. pestanai clade. Phylogenetic analyses provide further evidence that ticks may transmit these trypanosomes to a diversity of mammal species (including placental and marsupial species) on most continents.

Survey of ticks and tick-borne pathogens in wild chimpanzee habitat in Western Uganda.

BACKGROUND: Ticks and tick-borne pathogens significantly impact both human and animal health and therefore are of major concern to the scientific community. Knowledge of tick-borne pathogens is crucial for prescription of mitigation measures. In Africa, much research on ticks has focused on domestic animals. Little is known about ticks and their pathogens in wild habitats and wild animals like the endangered chimpanzee, our closest relative. METHODS: In this study, we collected ticks in the forested habitat of a community of 100 chimpanzees living in Kibale National Park, Western Uganda, and assessed how their presence and abundance are influenced by environmental factors. We used non-invasive methods of flagging the vegetation and visual search of ticks both on human team members and in chimpanzee nests. We identified adult and nymph ticks through morphological features. Molecular techniques were used to detect and identify tick-borne piroplasmids and bacterial pathogens. RESULTS: A total of 470 ticks were collected, which led to the identification of seven tick species: Haemaphysalis parmata (68.77%), Amblyomma tholloni (20.70%), Ixodes rasus sensu lato (7.37%), Rhipicephalus dux (1.40%), Haemaphysalis punctaleachi (0.70%), Ixodes muniensis (0.70%) and Amblyomma paulopunctatum (0.35%). The presence of ticks, irrespective of species, was influenced by temperature and type of vegetation but not by relative humidity. Molecular detection revealed the presence of at least six genera of tick-borne pathogens (Babesia, Theileria, Borrelia, Cryptoplasma, Ehrlichia and Rickettsia). The Afrotopical tick Amblyomma tholloni found in one chimpanzee nest was infected by Rickettsia sp. CONCLUSIONS: In conclusion, this study presented ticks and tick-borne pathogens in a Ugandan wildlife habitat whose potential effects on animal health remain to be elucidated.

Novel Chronic Anaplasmosis in Splenectomized Patient, Amazon Rainforest.

We report a case of unusual human anaplasmosis in the Amazon rainforest of French Guiana. Molecular typing demonstrated that the pathogen is a novel Anaplasma species, distinct to all known species, and more genetically related to recently described Anaplasma spp. causing infections in rainforest wild fauna of Brazil.

Ecological Contacts and Host Specificity Promote Replacement of Nutritional Endosymbionts in Ticks.

Symbiosis with vitamin-provisioning microbes is essential for the nutrition of animals with some specialized feeding habits. While coevolution favors the interdependence between symbiotic partners, their associations are not necessarily stable: Recently acquired symbionts can replace ancestral symbionts. In this study, we demonstrate successful replacement by Francisella-like endosymbionts (-LE), a group of B-vitamin-provisioning endosymbionts, across tick communities driven by horizontal transfers. Using a broad collection of Francisella-LE-infected tick species, we determined the diversity of Francisella-LE haplotypes through a multi-locus strain typing approach and further characterized their phylogenetic relationships and their association with biological traits of their tick hosts. The patterns observed showed that Francisella-LE commonly transfer through similar ecological networks and geographic distributions shared among different tick species and, in certain cases, through preferential shuffling across congeneric tick species. Altogether, these findings reveal the importance of geographic, ecological, and phylogenetic proximity in shaping the replacement pattern in which new nutritional symbioses are initiated.

MIxS-SA: a MIxS extension defining the minimum information standard for sequence data from symbiont-associated micro-organisms.

The symbiont-associated (SA) environmental package is a new extension to the minimum information about any (x) sequence (MIxS) standards, established by the Parasite Microbiome Project (PMP) consortium, in collaboration with the Genomics Standard Consortium. The SA was built upon the host-associated MIxS standard, but reflects the nestedness of symbiont-associated microbiota within and across host-symbiont-microbe interactions. This package is designed to facilitate the collection and reporting of a broad range of metadata information that apply to symbionts such as life history traits, association with one or multiple host organisms, or the nature of host-symbiont interactions along the mutualism-parasitism continuum. To better reflect the inherent nestedness of all biological systems, we present a novel feature that allows users to co-localize samples, to nest a package within another package, and to identify replicates. Adoption of the MIxS-SA and of the new terms will facilitate reports of complex sampling design from a myriad of environments.

A dual endosymbiosis supports nutritional adaptation to hematophagy in the invasive tick Hyalomma marginatum.

Many animals are dependent on microbial partners that provide essential nutrients lacking from their diet. Ticks, whose diet consists exclusively on vertebrate blood, rely on maternally inherited bacterial symbionts to supply B vitamins. While previously studied tick species consistently harbor a single lineage of those nutritional symbionts, we evidence here that the invasive tick Hyalomma marginatum harbors a unique dual-partner nutritional system between an ancestral symbiont, Francisella, and a more recently acquired symbiont, Midichloria. Using metagenomics, we show that Francisella exhibits extensive genome erosion that endangers the nutritional symbiotic interactions. Its genome includes folate and riboflavin biosynthesis pathways but deprived functional biotin biosynthesis on account of massive pseudogenization. Co-symbiosis compensates this deficiency since the Midichloria genome encompasses an intact biotin operon, which was primarily acquired via lateral gene transfer from unrelated intracellular bacteria commonly infecting arthropods. Thus, in H. marginatum, a mosaic of co-evolved symbionts incorporating gene combinations of distant phylogenetic origins emerged to prevent the collapse of an ancestral nutritional symbiosis. Such dual endosymbiosis was never reported in other blood feeders but was recently documented in agricultural pests feeding on plant sap, suggesting that it may be a key mechanism for advanced adaptation of arthropods to specialized diets.