Torix group Rickettsia are widespread in Culicoides biting midges (Diptera: Ceratopogonidae), reach high frequency and carry unique genomic features

Summary There is increasing interest in the heritable bacteria of invertebrate vectors of disease as they present novel targets for control initiatives. Previous studies on biting midges (Culicoides spp.), known to transmit several RNA viruses of veterinary importance, have revealed infections with the endosymbiotic bacteria, Wolbachia and Cardinium. However, rickettsial symbionts in these vectors are underexplored. Here, we present the genome of a previously uncharacterized Rickettsia endosymbiont from Culicoides newsteadi (RiCNE). This genome presents unique features potentially associated with host invasion and adaptation, including genes for the complete non‐oxidative phase of the pentose phosphate pathway, and others predicted to mediate lipopolysaccharides and cell wall modification. Screening of 414 Culicoides individuals from 29 Palearctic or Afrotropical species revealed that Rickettsia represent a widespread but previously overlooked association, reaching high frequencies in midge populations and present in 38% of the species tested. Sequence typing clusters the Rickettsia within the Torix group of the genus, a group known to infect several aquatic and hematophagous taxa. FISH analysis indicated the presence of Rickettsia bacteria in ovary tissue, indicating their maternal inheritance. Given the importance of biting midges as vectors, a key area of future research is to establish the impact of this endosymbiont on vector competence.

• Publication year

  2017

• Venue

  Environmental Microbiology

• Publication date

  2017-09-18

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1111/1462-2920.13887PMID 28805302PMCID 5656822
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Evolview v2: an online visualization and management tool for customized and annotated phylogenetic trees

  2016cited by this paper
• LPS Remodeling Triggers Formation of Outer Membrane Vesicles in Salmonella

  2016cited by this paper
• blobtools: blobtools v0.9.19.4

  2016cited by this paper
• An automated system for evaluation of the potential functionome: MAPLE version 2.1.0

  2016influential reference
• Grandeur Alliances: Symbiont Metabolic Integration and Obligate Arthropod Hematophagy.

  2016cited by this paper
• The incidence of bacterial endosymbionts in terrestrial arthropods

  2015influential reference
• Rickettsia-related bacteria associated with papaya plants showing bunchy top disease in Cuba

  2015cited by this paper
• eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences

  2015cited by this paper
• A Coxiella-Like Endosymbiont Is a Potential Vitamin Source for the Lone Star Tick

  2015cited by this paper
• Reproductive parasitism: maternally inherited symbionts in a biparental world.

  2015cited by this paper
• BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs

  2015cited by this paper
• Solving a Bloody Mess: B-Vitamin Independent Metabolic Convergence among Gammaproteobacterial Obligate Endosymbionts from Blood-Feeding Arthropods and the Leech Haementeria officinalis

  2015cited by this paper
• OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy

  2015cited by this paper
• The Phylogeny of Rickettsia Using Different Evolutionary Signatures: How Tree-Like is Bacterial Evolution?

  2015cited by this paper
• Detection of Low-Level Cardinium and Wolbachia Infections in Culicoides

  2015influential reference
• RDP4: Detection and analysis of recombination patterns in virus genomes

  2015influential reference
• Delineation of Culicoides species by morphology and barcode exemplified by three new species of the subgenus Culicoides (Diptera: Ceratopogonidae) from Scandinavia

  2015cited by this paper
• Editorial: A home for virology, ecology, epidemiology, and evolutionary biology

  2015cited by this paper
• First detection of endosymbiotic bacteria in biting midges Culicoides pulicaris and Culicoides punctatus, important Palaearctic vectors of bluetongue virus

  2014influential reference
• Prokka: rapid prokaryotic genome annotation

  2014influential reference
• Evolutionary origin of insect–Wolbachia nutritional mutualism

  2014cited by this paper
• Intrasperm vertical symbiont transmission

  2014cited by this paper
• Implication of the Bacterial Endosymbiont Rickettsia spp. in Interactions of the Whitefly Bemisia tabaci with Tomato yellow leaf curl virus

  2014cited by this paper
• The Facultative Symbiont Rickettsia Protects an Invasive Whitefly against Entomopathogenic Pseudomonas syringae Strains

  2014cited by this paper
• InterProScan 5: genome-scale protein function classification

  2014influential reference
• RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies

  2014influential reference
• The return of metabolism: biochemistry and physiology of the pentose phosphate pathway

  2014cited by this paper
• High quality draft genome sequence and description of Occidentia massiliensis gen. nov., sp. nov., a new member of the family Rickettsiaceae

  2014cited by this paper
• Assembling Genomes and Mini-metagenomes from Highly Chimeric Reads

  2013influential reference
• Elucidation of the 3-O-Deacylase Gene, pagL, Required for the Removal of Primary β-Hydroxy Fatty Acid from the Lipid A in the Nitrogen-fixing Endosymbiont Rhizobium etli CE3*

  2013cited by this paper
• MEGA6: Molecular Evolutionary Genetics Analysis version 6.0.

  2013cited by this paper
• Usefulness of rickettsial PCR assays for the molecular diagnosis of human rickettsioses.

  2013cited by this paper
• ‘Candidatus Megaira polyxenophila’ gen. nov., sp. nov.: Considerations on Evolutionary History, Host Range and Shift of Early Divergent Rickettsiae

  2013influential reference
• Barcoding of biting midges in the genus Culicoides: a tool for species determination

  2013influential reference
• which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. REAPR: a universal tool for genome assembly evaluation

  2013influential reference
• Blobology: exploring raw genome data for contaminants, symbionts and parasites using taxon-annotated GC-coverage plots

  2013cited by this paper
• Protection against a fungal pathogen conferred by the aphid facultative endosymbionts Rickettsia and Spiroplasma is expressed in multiple host genotypes and species and is not influenced by co‐infection with another symbiont

  2013cited by this paper
• Infections with Wolbachia, Spiroplasma, and Rickettsia in the Dolichopodidae and other Empidoidea.

  2013cited by this paper
• MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability

  2013cited by this paper
• Impact of Wolbachia on Infection with Chikungunya and Yellow Fever Viruses in the Mosquito Vector Aedes aegypti

  2012cited by this paper
• Prevalence of the symbiont Cardinium in Culicoides (Diptera: Ceratopogonidae) vector species is associated with land surface temperature

  2012cited by this paper
• Fast gapped-read alignment with Bowtie 2

  2012cited by this paper
• Insight into the Transmission Biology and Species-Specific Functional Capabilities of Tsetse (Diptera: Glossinidae) Obligate Symbiont Wigglesworthia

  2012cited by this paper
• Metabolic adaptation of human pathogenic and related nonpathogenic bacteria to extra- and intracellular habitats.

  2012cited by this paper
• MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space

  2012influential reference
• Microbial community of predatory bugs of the genus Macrolophus (Hemiptera: Miridae)

  2012influential reference
• LPS remodeling is an evolved survival strategy for bacteria

  2012cited by this paper
• Dramatic Increase in Glycerol Biosynthesis upon Oxidative Stress in the Anaerobic Protozoan Parasite Entamoeba histolytica

  2012cited by this paper
• Unipro UGENE: a unified bioinformatics toolkit

  2012cited by this paper
• Bacterial symbionts in insects or the story of communities affecting communities

  2011cited by this paper
• Wolbachia strain wMel induces cytoplasmic incompatibility and blocks dengue transmission in Aedes albopictus

  2011cited by this paper
• Wolbachia and the biological control of mosquito‐borne disease

  2011cited by this paper
• Mobilizable bacterial DNA packaged into membrane vesicles induces serial transduction.

  2011cited by this paper
• Rickettsial evolution in the light of comparative genomics

  2011cited by this paper
• A Rickettsia Genome Overrun by Mobile Genetic Elements Provides Insight into the Acquisition of Genes Characteristic of an Obligate Intracellular Lifestyle

  2011influential reference
• ProtTest 3: fast selection of best-fit models of protein evolution

  2011influential reference
• The Endosymbiotic Bacterium Wolbachia Induces Resistance to Dengue Virus in Aedes aegypti

  2010cited by this paper
• Bacterial Genes in the Aphid Genome: Absence of Functional Gene Transfer from Buchnera to Its Host

  2010cited by this paper
• Virulence and Immunomodulatory Roles of Bacterial Outer Membrane Vesicles

  2010cited by this paper
• Nutrient provisioning facilitates homeostasis between tsetse fly (Diptera: Glossinidae) symbionts

  2010cited by this paper
• Rickettsia Symbionts Cause Parthenogenetic Reproduction in the Parasitoid Wasp Pnigalio soemius (Hymenoptera: Eulophidae)

  2010influential reference
• High prevalence of Rickettsia gravesii sp. nov. in Amblyomma triguttatum collected from feral pigs.

  2010cited by this paper
• Adaptation via Symbiosis: Recent Spread of a Drosophila Defensive Symbiont

  2010cited by this paper
• ProtTest-HPC: Fast Selection of Best-Fit Models of Protein Evolution

  2010cited by this paper
• An Anomalous Type IV Secretion System in Rickettsia Is Evolutionarily Conserved

  2009cited by this paper
• trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses

  2009cited by this paper
• Identification of cryptic species of Culicoides (Diptera: Ceratopogonidae) in the subgenus Culicoides and development of species-specific PCR assays based on barcode regions.

  2009cited by this paper
• Prevalence of Cardinium Bacteria in Planthoppers and Spider Mites and Taxonomic Revision of “Candidatus Cardinium hertigii” Based on Detection of a New Cardinium Group from Biting Midges

  2009influential reference
• Structural rna homology search and alignment using covariance models

  2009cited by this paper
• A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium.

  2009cited by this paper
• Endosymbiotic Bacteria in the Parasitic Ciliate Ichthyophthirius multifiliis

  2009cited by this paper
• The microbial dimension in insect nutritional ecology

  2009cited by this paper
• DESCRIPTIONS OF THREE SPECIES OF CULICOIDES LATREILLE (DIPTERA: CERATOPOGONIDAE) NEW TO SCIENCE, TOGETHER WITH NOTES ON, AND A REVISED KEY TO THE BRITISH SPECIES OF THE PULICARIS AND OBSOLETUS GROUPS

  2009cited by this paper
• Circos: an information aesthetic for comparative genomics.

  2009cited by this paper
• Conjugation genes are common throughout the genus Rickettsia and are transmitted horizontally

  2009influential reference
• Evolution and diversity of Rickettsia bacteria

  2009influential reference
• Composition of Bacterial Communities Associated with Natural and Laboratory Populations of Asobara tabida Infected with Wolbachia

  2009cited by this paper
• DnaSP v5: a software for comprehensive analysis of DNA polymorphism data

  2009cited by this paper
• Microbial modification of host long-distance dispersal capacity

  2009cited by this paper
• Characterization and localization of Rickettsia sp. in water beetles of genus Deronectes (Coleoptera: Dytiscidae).

  2009influential reference
• The Sequence Alignment/Map format and SAMtools

  2009cited by this paper
• Pathogen Screening and Bionomics of Lutzomyia apache (Diptera: Psychodidae) in Wyoming, USA

  2008cited by this paper
• Wolbachia: master manipulators of invertebrate biology

  2008cited by this paper
• Structure and Function of Sedoheptulose-7-phosphate Isomerase, a Critical Enzyme for Lipopolysaccharide Biosynthesis and a Target for Antibiotic Adjuvants*

  2008cited by this paper
• An Anhydro-N-Acetylmuramyl-l-Alanine Amidase with Broad Specificity Tethered to the Outer Membrane of Escherichia coli

  2007cited by this paper
• Antibiotic Treatment of the Tick Vector Amblyomma americanum Reduced Reproductive Fitness

  2007cited by this paper
• The Orientia tsutsugamushi genome reveals massive proliferation of conjugative type IV secretion system and host–cell interaction genes

  2007influential reference
• Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation

  2007cited by this paper
• The genomic and metabolic diversity of Rickettsia.

  2007cited by this paper
• The First Finding of a Rickettsia Bacterium Associated with Parthenogenesis Induction Among Insects

  2006influential reference
• Genome Sequence of Rickettsia bellii Illuminates the Role of Amoebae in Gene Exchanges between Intracellular Pathogens

  2006cited by this paper
• The emerging diversity of Rickettsia

  2006influential reference
• Sequence-based species delimitation for the DNA taxonomy of undescribed insects.

  2006cited by this paper
• Rickettsia as obligate and mycetomic

  2006cited by this paper
• Wolbachia and other endosymbiont infections in spiders

  2006influential reference
• Rickettsia Infection in Natural Leech Populations

  2005cited by this paper
• Molecular evolution of rickettsia surface antigens: evidence of positive selection.

  2005cited by this paper
• Culture-Independent Analysis of Midgut Microbiota in the Arbovirus Vector Culicoides sonorensis (Diptera: Ceratopogonidae)

  2004cited by this paper
• Nuclearia pattersoni sp. n. (Filosea), a new species of amphizoic amoeba isolated from gills of roach (Rutilus rutilus), and its rickettsial endosymbiont.

  2003cited by this paper
• Gene Sequence-Based Criteria for Identification of New Rickettsia Isolates and Description of Rickettsia heilongjiangensis sp. nov

  2003cited by this paper

• Characterization of the Bacteriome of Culicoides reevesi from Chihuahua, Northern Mexico: Symbiotic and Pathogenic Associations

  2026cites this paper
• Gut microbiome diversity and functional profiles of Culicoides across Sanya, Ruili, and Linyi, China.

  2026cites this paper
• Unification of Symbiotic Bacteria During Larva-to-Adult Transition in Culicoides circumscriptus (Diptera: Ceratopogonidae).

  2025cites this paper
• Genomic analysis of co-infection with Wolbachia and Candidatus Tisiphia in the sand fly Sergentomyia squamirostris

  2025cites this paper
• A comparison of the structure and diversity of the microbial communities of Culicoides midges.

  2025cites this paper
• Metagenome diversity illuminates the origins of pathogen effectors

  2024cites this paper
• Development, feeding, and sex shape the relative quantity of the nutritional obligatory symbiont Wolbachia in bed bugs

  2024cites this paper
• Comparative genomics of a novel Erwinia species associated with the Highland midge (Culicoides impunctatus)

  2023cites this paper
• ‘Candidatus Tisiphia’ is a widespread Rickettsiaceae symbiont in the mosquito Anopheles plumbeus (Diptera: Culicidae)

  2023cites this paper
• Orientia and Rickettsia: different flowers from the same garden.

  2023cites this paper
• A novel Rickettsia species closely related to Rickettsia felis in Anopheles mosquitoes from Yingkou City, Northeast China

  2023cites this paper
• The terrestrial isopod symbiont ‘Candidatus Hepatincola porcellionum’ is a potential nutrient scavenger related to Holosporales symbionts of protists

  2023cites this paper
• ‘Candidatus Tisiphia’ is a widespread Rickettsiaceae symbiont in the mosquito Anopheles plumbeus (Diptera: Culicidae)

  2023cites this paper
• Metagenome diversity illuminates origins of pathogen effectors

  2023cites this paper
• Biting Midges (Diptera: Ceratopogonidae) as Vectors of Viruses

  2023cites this paper
• One to host them all: genomics of the diverse bacterial endosymbionts of the spider Oedothorax gibbosus

  2022cites this paper
• The opportunities of research parasitism: A case study using the Barcode of Life Data System (BOLD)

  2022cites this paper
• 'Candidatus Megaira' are diverse symbionts of algae and ciliates with the potential for defensive symbiosis

  2022cites this paper
• Larvicidal and pupicidal activity of crude ethyl acetate extract fraction-7a of Cymodocea serrulata on Culex quinquefasciatus

  2022cites this paper
• Genomic diversity across the Rickettsia and ‘Candidatus Megaira’ genera and proposal of genus status for the Torix group

  2022cites this paper
• Gene Transfer Agents in Bacterial Endosymbionts of Microbial Eukaryotes

  2022cites this paper
• Large-scale comparative genomics unravels great genomic diversity across the Rickettsia and Ca. Megaira genera and identifies Torix group as an evolutionarily distinct clade

  2021cites this paper
• "Candidatus Sarmatiella mevalonica" endosymbiont of the ciliate Paramecium provides insights on evolutionary plasticity among Rickettsiales.

  2021cites this paper
• Critical realism as a continuing resource for biological research: the illustrative case study of biting midges and their symbiotic bacteria

  2021cites this paper
• Two parasites in one host: spatiotemporal dynamics and co-occurrence of Microsporidia and Rickettsia in an amphipod host

  2021cites this paper
• Species Identity, Life History, and Geographic Distance Influence Gut Bacterial Communities in Lab-Reared and European Field-Collected Culicoides Biting midges

  2021cites this paper
• Identifying potential candidate Culicoides spp. for the study of interactions with Candidatus Cardinium hertigii

  2021cites this paper
• Transmission, Tropism, and Biological Impacts of Torix Rickettsia in the Common Bed Bug Cimex lectularius (Hemiptera: Cimicidae)

  2020influential citation
• Widespread Torix Rickettsia in New Zealand amphipods and the use of blocking primers to rescue host COI sequences

  2020cites this paper
• Incidence and Diversity of Torix Rickettsia–Odonata Symbioses

  2020influential citation
• Tissue Tropisms and Transstadial Transmission of a Rickettsia Endosymbiont in the Highland Midge, Culicoides impunctatus (Diptera: Ceratopogonidae)

  2020cites this paper
• Continuous Cell Lines from the European Biting Midge Culicoides nubeculosus (Meigen, 1830)

  2020cites this paper
• Torix group Rickettsia are widespread in New Zealand freshwater amphipods: using blocking primers to rescue host COI sequences

  2020influential citation
• A newly-recorded Rickettsia of the Torix group is a recent intruder and an endosymbiont in the whitefly Bemisia tabaci.

  2020influential citation
• Torix Rickettsia are widespread in arthropods and reflect a neglected symbiosis

  2020influential citation
• Genetic diversity of Culicoides species within the Pulicaris complex (Diptera: Ceratopogonidae) in Turkey inferred from mitochondrial COI gene sequences.

  2019cites this paper
• Molecular Tools in Microbial Diversity

  2019cites this paper
• The draft genome of strain cCpun from biting midges confirms insect Cardinium are not a monophyletic group and reveals a novel gene family expansion in a symbiont

  2019influential citation
• Mosquitoes, midges and microbiota: European vector diversity and the spread of pathogens

  2019influential citation
• Rickettsia buchneri, symbiont of the deer tick Ixodes scapularis, can colonise the salivary glands of its host.

  2019cites this paper
• MAPLE Enables Functional Assessment of Microbiota in Various Environments

  2019cites this paper
• A gene transfer event suggests a long-term partnership between eustigmatophyte algae and a novel lineage of endosymbiotic bacteria

  2018cites this paper
• “Interactions between pathogenic and non-pathogenic Rickettsiales and the tick host”

  2018cites this paper
• Detection of bacterial endosymbionts in freshwater crustaceans: the applicability of non-degenerate primers to amplify the bacterial 16S rRNA gene

  2018cites this paper
• The draft genome of strain cCpun from biting midges establishes Cardinium as a paraphyletic group, and reveals a novel gene family expansion in a symbiont

  2018influential citation
• Conjugative Transposons and Their Cargo Genes Vary across Natural Populations of Rickettsia buchneri Infecting the Tick Ixodes scapularis

  2018cites this paper