scholarly journals A Rickettsiella endosymbiont is a potential source of essential B-vitamins for the poultry red mite, Dermanyssus gallinae

2021 ◽  
Author(s):  
Daniel R. G. Price ◽  
Kathryn Bartley ◽  
Damer P. Blake ◽  
Eleanor Karp-Tatham ◽  
Francesca Nunn ◽  
...  

AbstractObligate blood-sucking arthropods rely on symbiotic bacteria to provision essential B vitamins that are either missing or at sub-optimal amounts in their nutritionally challenging blood diet. The poultry red mite Dermanyssus gallinae, an obligate blood-feeding ectoparasite, is primarily associated with poultry and a serious threat to the hen egg industry. Thus far, the identity and biological role of nutrient provisioning bacterial mutualists from D. gallinae are little understood. Here, we demonstrate that a Rickettsiella Gammaproteobacteria in maternally transmitted in D. gallinae and universally present in D. gallinae mites collected at different sites throughout Europe. In addition, we report the genome sequence of uncultivable endosymbiont “Candidatus Rickettsiella rubrum” from D. gallinae eggs. The endosymbiont has a circular 1. 89 Mbp genome that encodes 1973 protein. Phylogenetic analysis confirms the placement R. rubrum within the Rickettsiella genus, closely related to a facultative endosymbiont from the pea aphid and Coxiella-like endosymbionts from blood feeding ticks. Analysis of the R. rubrum genome reveals many protein-coding sequences are either pseudogenized or lost, but R. rubrum has retained several B vitamin biosynthesis pathways, confirming the importance of these pathways in evolution of its nutritional symbiosis with D. gallinae. In silico metabolic pathway reconstruction revealed that R. rubrum is unable to synthesise protein amino acids and therefore these nutrients are likely provisioned by the host. In contrast R. rubrum retains biosynthetic pathways for B vitamins: thiamine (vitamin B1) via the salvage pathway; riboflavin (vitamin B2) and pyridoxine (vitamin B6) and the cofactors: flavin adenine dinucleotide (FAD) and coenzyme A (CoA) that likely provision these nutrients to the host. We propose that bacterial symbionts which are essential to blood-feeding arthropod survival provide attractive targets for the development of novel control methods.

2021 ◽  
Vol 12 ◽  
Author(s):  
Daniel R. G. Price ◽  
Kathryn Bartley ◽  
Damer P. Blake ◽  
Eleanor Karp-Tatham ◽  
Francesca Nunn ◽  
...  

Many obligate blood-sucking arthropods rely on symbiotic bacteria to provision essential B vitamins that are either missing or at sub-optimal levels in their nutritionally challenging blood diet. The poultry red mite Dermanyssus gallinae, an obligate blood-feeding ectoparasite, is a serious threat to the hen egg industry. Poultry red mite infestation has a major impact on hen health and welfare and causes a significant reduction in both egg quality and production. Thus far, the identity and biological role of nutrient provisioning bacterial mutualists from D. gallinae are little understood. Here, we demonstrate that an obligate intracellular bacterium of the Rickettsiella genus is detected in D. gallinae mites collected from 63 sites (from 15 countries) across Europe. In addition, we report the genome sequence of Rickettsiella from D. gallinae (Rickettsiella – D. gallinae endosymbiont; Rickettsiella DGE). Rickettsiella DGE has a circular 1.89Mbp genome that encodes 1,973 proteins. Phylogenetic analysis confirms the placement of Rickettsiella DGE within the Rickettsiella genus, related to a facultative endosymbiont from the pea aphid and Coxiella-like endosymbionts (CLEs) from blood feeding ticks. Analysis of the Rickettsiella DGE genome reveals that many protein-coding sequences are either pseudogenized or lost, but Rickettsiella DGE has retained several B vitamin biosynthesis pathways, suggesting the importance of these pathways in evolution of a nutritional symbiosis with D. gallinae. In silico metabolic pathway reconstruction revealed that Rickettsiella DGE is unable to synthesize protein amino acids and, therefore, amino acids are potentially provisioned by the host. In contrast, Rickettsiella DGE retains biosynthetic pathways for B vitamins: thiamine (vitamin B1) via the salvage pathway; riboflavin (vitamin B2) and pyridoxine (vitamin B6) and the cofactors: flavin adenine dinucleotide (FAD) and coenzyme A (CoA) that likely provision these nutrients to the host.


2021 ◽  
Author(s):  
Kathryn Bartley ◽  
Wan Chen ◽  
Richard Lloyd Mills ◽  
Francesca Nunn ◽  
Daniel Price ◽  
...  

Abstract Background: The blood feeding poultry red mite (PRM), Dermanyssus gallinae, causes substantial economic damage to the egg laying industry worldwide, and is serious welfare concern for laying hens and poultry house workers. In this study we have investigated the temporal gene expression across the 6 stages/sexes (egg, larvae, protonymph and deutonymph, adult male and adult female) of this neglected parasite in order to understand the temporal expression associated with development, parasitic lifestyle, reproduction and allergen expression. Results: RNA-seq transcript data for the 6 stages was mapped to the PRM genome creating a publicly available gene expression atlas (on the OrcAE platform in conjunction with the PRM genome). Network analysis and clustering of stage-enriched gene expression in PRM resulted in 17 superclusters with stage-specific or multi-stage expression profiles. The 6 stage specific superclusters were clearly demarked from each other and the adult female supercluster contained the most stage specific transcripts (2,725), whilst the protonymph supercluster the fewest (165). Fifteen pairwise comparisons performed between the different stages resulting in a total of 6025 Differentially Expressed Genes (DEGs) (P>0.99). These data were evaluated alongside a Venn/Euler analysis of the top 100 most abundant genes in each stage. An expanded set of cuticle proteins and enzymes (chitinase and metallacarboxypeptidases) were identified in larvae and underpin cuticle formation and ecdysis to the protonymph stage. Two mucin/peritrophic-A salivary proteins (DEGAL6771g00070, DEGAL6824g00220) were highly expressed in the blood-feeding stages, indicating peritrophic membrane formation during feeding. Reproduction-associated vitellogenins were the most abundant transcripts in adult females, whilst in adult males, an expanded set of serine and cysteine proteinases and an epididymal protein (DEGAL6668g00010) were highly abundant. Assessment of the expression patterns of putative homologues of 32 allergen groups described for the house dust mites indicated a bias in expression towards the non-feeding larval stage.Conclusions: This study is the first evaluation of temporal gene expression across all stages of PRM and has provided insight into developmental, feeding, reproduction and survival strategies employed by this mite. The publicly available PRM resource on OrcAE offers an invaluable tool for researchers investigating the biology and novel interventions of this parasite.


2020 ◽  
Author(s):  
Ivo Petersen ◽  
Katharina Johannhörster ◽  
Eric Pagot ◽  
Damian Escribano ◽  
Eva Zschiesche ◽  
...  

Abstract Background. Infestations with the poultry red mite (PRM), Dermanyssus gallinae, can result in anaemia, stress-related behaviours linked to reduced laying hen welfare, and impaired productivity. A study was conducted to investigate the potential welfare benefits of PRM elimination following fluralaner treatment.MethodsA single poultry house was selected on each of two layer farms, one free-range, one aviary, containing 5,400 Lohmann LSL hens and 42,400 Lohmann Brown hens, respectively. Fluralaner (Exzolt®; 0.5 mg/kg body weight) was administered twice, seven days apart (Weeks 0 and 1). Mite populations were regularly monitored by traps left in place for one to two days. Infra-red cameras monitored night-time hen behaviours weekly, beginning five weeks pre-treatment, continuing for five and six weeks post-treatment on the free-range and aviary farms, respectively. Weekly daytime behaviours were recorded on the free-range farm. On the aviary farm, blood samples were collected from 50 randomly selected hens during Weeks -3, -1 and 5. On the free-range farm, eggs were randomly collected for corticosterone analysis during Weeks -6, 0 and 6, and on the aviary farm during Weeks -3, -1 and 5. Production parameters were assessed using farm records.ResultsFluralaner efficacy on the free-range farm was >99% following the first administration, and on the aviary farm was 100% at Week 1 and at all subsequent mite counts. On both farms, treatment was followed by significant reductions in night-time preening, head scratching, head shaking, and activity, and on the aviary farm in vertical wing shaking and gentle feather pecking. On the free-range farm there were significant daytime reductions in head scratching, head shaking and preening. Post-treatment increases in egg and plasma corticosterone were suggestive of stress factors extra to mite infestation. Red blood cell counts and haematocrit increased following treatment. On the free range farm, relative to standard production parameters for LSL hens, the decline in laying rate with increasing bird age was less than expected, and the increase in egg weight greater than expected. ConclusionFluralaner treatment eliminated mite challenge, leading to improved hen welfare and health, based on reductions in stress-related behaviours, and restoration of the anaemia-inducing effects of mite blood feeding.


2021 ◽  
Author(s):  
Eleanor Karp-Tatham ◽  
Dong Xia ◽  
Alasdair J Nisbet ◽  
Teresa Letra Mateus ◽  
Fiona M. Tomley ◽  
...  

Abstract The poultry red mite (Dermanyssus gallinae), an obligatory blood feeding ectoparasite, is primarily associated with egg laying hens where it is estimated to cause losses of ~€230 million per annum from European farmers. Current control strategies, including the use of acaricidal chemicals and desiccant dusts, are often ineffective and there is widespread resistance to acaricides across Europe. Alternative methods to control D. gallinae are urgently required and strategies include development of recombinant subunit vaccines and discovery of new potential acaricides. These strategies will benefit hugely from knowledge of the extent and rates of occurrence of genetic diversity within D. gallinae populations. In this study, genetic diversity of mites harvested from the UK and from sites across mainland Europe was studied at inter- and intra-farm levels. To achieve this, the genome analysis toolkit (GATK) best practices pipeline for single nucleotide polymorphism (SNP) and insertion/deletion variant calling was modified to be self-validating and used to identify 32,599 D. gallinae SNPs by comparing transcriptomic sequences (derived from mites harvested in Germany, Schicht et al.) with a D. gallinae genome assembly (derived from mites harvested in Scotland, Burgess et al.). Dermanyssus gallinae populations were sampled from 22 UK farms and 57 farms from 15 countries in mainland Europe. Analysis of 144 high-quality SNP markers across 117 pooled D. gallinae samples showed high spatial genetic diversity with significant linkage disequilibrium. Revisiting a subset of farms revealed notable temporal changes in genetic diversity.


2014 ◽  
Vol 281 (1796) ◽  
pp. 20141838 ◽  
Author(s):  
Hassan Salem ◽  
Eugen Bauer ◽  
Anja S. Strauss ◽  
Heiko Vogel ◽  
Manja Marz ◽  
...  

Despite the demonstrated functional importance of gut microbes, our understanding of how animals regulate their metabolism in response to nutritionally beneficial symbionts remains limited. Here, we elucidate the functional importance of the African cotton stainer's ( Dysdercus fasciatus ) association with two actinobacterial gut symbionts and subsequently examine the insect's transcriptional response following symbiont elimination. In line with bioassays demonstrating the symbionts' contribution towards host fitness through the supplementation of B vitamins, comparative transcriptomic analyses of genes involved in import and processing of B vitamins revealed an upregulation of gene expression in aposymbiotic (symbiont-free) compared with symbiotic individuals; an expression pattern that is indicative of B vitamin deficiency in animals. Normal expression levels of these genes, however, can be restored by either artificial supplementation of B vitamins into the insect's diet or reinfection with the actinobacterial symbionts. Furthermore, the functional characterization of the differentially expressed thiamine transporter 2 through heterologous expression in Xenopus laevis oocytes confirms its role in cellular uptake of vitamin B1. These findings demonstrate that despite an extracellular localization, beneficial gut microbes can be integral to the host's metabolic homeostasis, reminiscent of bacteriome-localized intracellular mutualists.


2021 ◽  
Vol 14 (1) ◽  
Author(s):  
Ivo Petersen ◽  
Katharina Johannhörster ◽  
Eric Pagot ◽  
Damian Escribano ◽  
Eva Zschiesche ◽  
...  

Abstract Background Poultry red mite (PRM) (Dermanyssus gallinae) infestations are a cause of anaemia, impaired productivity and stress-related behaviours linked to reduced hen welfare. A study investigated the potential health, welfare and productivity benefits following fluralaner treatment to eliminate PRM from infested hens. Methods A PRM-infested layer house was selected on a free-range farm (5400 hens) and an aviary farm (42,400 hens). Fluralaner (Exzolt®; 0.5 mg/kg body weight) was administered twice, 7 days apart (Weeks 0 and 1), via drinking water. Mite populations were monitored by traps. Cameras recorded nighttime hen behaviours weekly, pre- and post-treatment. On the free-range farm, daytime behaviours were also recorded weekly. For pre- and post-treatment corticosterone assessments, eggs were randomly collected on both farms, and blood samples were collected from 50 randomly selected aviary farm hens. Production parameters were assessed using farm records. Results Throughout the post-treatment period, fluralaner efficacy against PRM was > 99% on both farms. On the aviary and free-range farms, treatment was followed by significant nighttime increases in the proportion of resting hens (P < 0.0001; P = 0.0175, respectively). Significant post-treatment versus pre-treatment nighttime reductions were observed in head shaking (aviary, P < 0.0001; free-range P = 0.0233) and preening (P = 0.0032; P = 0.0018) and on the aviary farm in bouts of body shaking (P = 0.0108), vertical wing shaking (P = 0.0002), head scratching (P = 0.0335), and gentle feather pecking (P < 0.0001). On the free-range farm there were significant daytime reductions in head scratching (P < 0.0001), head shaking (P = 0.0492) and preening (P = 0.0012). Relative to standard production parameters, no differences were detected on the aviary farm, but on the free-range farm the laying rate decline with increasing age was less than expected and the increase in egg weight greater than expected. Post-treatment increases in egg and plasma corticosterone were suggestive of stress factors in addition to mite infestation. Red blood cell counts and haematocrit increased following treatment. Conclusion Fluralaner treatment eliminated mite challenge, leading to improved hen welfare and health, based on reductions in stress-related behaviours and restoration of the anaemia-inducing effects of mite blood feeding.


2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Biswajit Bhowmick ◽  
Yu Tang ◽  
Fang Lin ◽  
Øivind Øines ◽  
Jianguo Zhao ◽  
...  

Abstract Detection of chemical cues via chemosensory receptor proteins are essential for most animals, and underlies critical behaviors, including location and discrimination of food resources, identification of sexual partners and avoidance of predators. The current knowledge of how chemical cues are detected is based primarily on data acquired from studies on insects, while our understanding of the molecular basis for chemoreception in acari, mites in particular, remains limited. The poultry red mite (PRM), Dermanyssus gallinae, is one of the most important blood-feeding ectoparasites of poultry. PRM are active at night which suck the birds' blood during periods of darkness and hide themselves in all kinds of gaps and cracks during the daytime. The diversity in habitat usage, as well as the demonstrated host finding and avoidance behaviors suggest that PRM relies on their sense of smell to orchestrate complex behavioral decisions. Comparative transcriptome analyses revealed the presence of candidate variant ionotropic receptors, odorant binding proteins, niemann-pick proteins type C2 and sensory neuron membrane proteins. Some of these proteins were highly and differentially expressed in the forelegs of PRM. Rhodopsin-like G protein-coupled receptors were also identified, while insect-specific odorant receptors and odorant co-receptors were not detected. Furthermore, using scanning electron microscopy, the tarsomeres of all leg pairs were shown to be equipped with sensilla chaetica with or without tip pores, while wall-pored olfactory sensilla chaetica were restricted to the distal-most tarsomeres of the forelegs. This study is the first to describe the presence of chemosensory genes in any Dermanyssidae family. Our findings make a significant step forward in understanding the chemosensory abilities of D. gallinae.


2020 ◽  
Author(s):  
Weipeng Zhang ◽  
Shunan Cao ◽  
Wei Ding ◽  
Meng Wang ◽  
Shen Fan ◽  
...  

Abstract Background: The Arctic and Antarctic are the two most geographically distant bioregions on earth. Recent sampling efforts and following metagenomics have shed light on the global ocean microbial diversity and function, yet the microbiota of polar regions has not been included in such global analyses. Results: Here a metagenomic study of seawater samples (n = 60) collected from different depths at 28 locations in the Arctic and Antarctic zones was performed, together with metagenomes from the Tara Oceans. More than 7,500 (19%) polar seawater-derived operational taxonomic units could not be identified in the Tara Oceans datasets, and more than 3,900,000 protein-coding gene orthologs had no hits in the Ocean Microbial Reference Gene Catalog. Analysis of 214 metagenome assembled genomes (MAGs) , recovered from the polar seawater microbiomes, revealed strains that are prevalent in the polar regions while nearly undetectable in temperate seawater. Metabolic pathway reconstruction for these microbes suggested versatility for saccharide and lipids biosynthesis, nitrate and sulfate reduction, and CO2 fixation. Comparison between the Arctic and Antarctic microbiomes revealed that antibiotic resistance genes were enriched in the Arctic while functions like DNA recombination were enriched in the Antarctic. Conclusions: Our data highlight the occurrence of dominant and locally enriched microbes in the Arctic and Antarctic seawater with unique functional traits for environmental adaption, and provide a foundation for analyzing the global ocean microbiome in a more complete perspective.


Vaccines ◽  
2021 ◽  
Vol 9 (12) ◽  
pp. 1472
Author(s):  
Sotaro Fujisawa ◽  
Shiro Murata ◽  
Masayoshi Isezaki ◽  
Takuma Ariizumi ◽  
Takumi Sato ◽  
...  

Poultry red mite (PRM; Dermanyssus gallinae) is a hazardous, blood-sucking ectoparasite of birds that constitutes a threat to poultry farming worldwide. Acaricides, commonly used in poultry farms to prevent PRMs, are not effective because of the rapid emergence of acaricide-resistant PRMs. However, vaccination may be a promising strategy to control PRM. We identified a novel cystatin-like molecule in PRMs: Dg-Cys. Dg-Cys mRNA expression was detected in the midgut and ovaries, in all stages of life. The PRM nymphs that were artificially fed with the plasma from chickens that were immunized with Dg-Cys in vitro had a significantly reduced reproductive capacity and survival rate. Moreover, combination of Dg-Cys with other antigen candidates, like copper transporter 1 or adipocyte plasma membrane-associated protein, enhanced vaccine efficacies. vaccination and its application as an antigen for cocktail vaccines could be an effective strategy to reduce the damage caused by PRMs in poultry farming.


Author(s):  
Biswajit Bhowmick ◽  
Yu Tang ◽  
Fang Lin ◽  
Øivind Øines ◽  
Jianguo Zhao ◽  
...  

AbstractDetection of chemical cues via chemosensory receptor proteins are essential for most animals, and underlies critical behaviors, including location and discrimination of food resources, identification of sexual partners and avoidance of predators. The current knowledge of how chemical cues are detected is based primarily on data acquired from studies on insects, while our understanding of the molecular basis for chemoreception in acari, mites in particular, remains limited. The poultry red mite (PRM), Dermanyssus gallinae, is one of the most important blood-feeding ectoparasites of poultry. Unlike other ectoparasites on animals, PRM feeds mainly at night. During daytime, these animals hide themselves in crevices around the poultry house. The diversity in habitat usage, as well as the demonstrated host finding and avoidance behaviors suggest that PRM relies on their sense of smell to orchestrate complex behavioral decisions. Comparative transcriptome analyses revealed the presence of candidate variant ionotropic receptors (IRs), odorant binding proteins (OBPs), niemann-pick proteins type C2 (NPC2) and sensory neuron membrane proteins (SNMPs). Some of these proteins were highly and differentially expressed in the forelegs of PRM. Rhodopsin-like G protein-coupled receptors (GPCRs) were also identified, while insect-specific odorant receptors (ORs) and odorant co-receptors (ORcos) were not detected. Furthermore, using scanning electron microscopy (SEM), the tarsomeres of all legs pairs were shown to be equipped with sensilla chaetica with or without tip pores, while wall-pored olfactory sensilla chaetica were restricted to the distal-most tarsomeres of the forelegs. Further, using the conserved odorant binding protein (OBP) as a test case, the results showed that RNA interference (RNAi) can be induced in D. gallinae chemosensory tissues. This study is the first to describe the presence of chemosensory genes in any Dermanyssidae family. It is also the first report of chemosensory gene knockdown by RNAi in any mite species and demonstrate that their diminutive size, less than 1 mm, is not a major impediment when applying gene knockdown approaches. Our findings make a significant step forward in understanding the chemosensory abilities of D. gallinae.


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