Characterization of a Novel Cysteine Protease Inhibitor from Poultry Red Mites: Potential Vaccine for Chickens

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.

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Comparison of in vivo and in vitro survival and fecundity rates of the poultry red mite, Dermanyssus gallinae

Research in Veterinary Science ◽

10.1016/j.rvsc.2009.08.002 ◽

2010 ◽

Vol 88 (2) ◽

pp. 279-280 ◽

Cited By ~ 6

Author(s):

S. Arkle ◽

D.R. George ◽

J.H. Guy ◽

O.A.E. Sparagano

Keyword(s):

Dermanyssus Gallinae ◽

Poultry Red Mite ◽

In Vitro Survival

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Comparison of synthetic membranes in the development of an in vitro feeding system for Dermanyssus gallinae

Bulletin of Entomological Research ◽

10.1017/s0007485309006865 ◽

2009 ◽

Vol 100 (2) ◽

pp. 127-132 ◽

Cited By ~ 10

Author(s):

D.W.J. Harrington ◽

J.H. Guy ◽

K. Robinson ◽

O.A.E. Sparagano

Keyword(s):

Feeding Rate ◽

Storage Conditions ◽

Dermanyssus Gallinae ◽

Skin Extract ◽

Proof Of Concept ◽

Ethical Considerations ◽

Poultry Red Mite ◽

Synthetic Membranes ◽

In Vitro Feeding

AbstractAlthough artificial feeding models for the poultry red mite (Dermanyssus gallinae) most frequently use biological membranes consisting of day-old chick skin, there are ethical considerations associated with the use of skin. The few studies reported in the literature that have investigated the use of synthetic membranes to feed D. gallinae in vitro have reported limited success. The current study describes an investigation into the use of synthetic membranes made from either Nescofilm® or rayon and silicone, used either alone or in combination with different feather or skin extracts, as well as the use of capillary tubes. In all, 12 different treatments were used, and the feeding rate of D. gallinae was compared to that of day-old chick skin. Allowing mites to feed on a membrane consisting of Nescofilm with a skin extract resulted in the highest proportion of mites feeding (32.3%), which was not significantly different to the feeding rate of mites on day-old chick skin (38.8%). This study confirms that synthetic membranes can be used to feed D. gallinae artificially. Further optimization of the membrane and mite storage conditions is still necessary, but the study demonstrates a proof of concept.

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Ability of a proteinase inhibitor mixture to kill poultry red mite, Dermanyssus gallinae in an in vitro feeding system

Veterinary Parasitology ◽

10.1016/j.vetpar.2006.05.013 ◽

2006 ◽

Vol 141 (3-4) ◽

pp. 380-385 ◽

Cited By ~ 22

Author(s):

R. McDevitt ◽

A.J. Nisbet ◽

J.F. Huntley

Keyword(s):

Proteinase Inhibitor ◽

Dermanyssus Gallinae ◽

Feeding System ◽

Poultry Red Mite ◽

In Vitro Feeding

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Assessment of cathepsin D and L-like proteinases of poultry red mite, Dermanyssus gallinae (De Geer), as potential vaccine antigens

Parasitology ◽

10.1017/s0031182011002356 ◽

2012 ◽

Vol 139 (6) ◽

pp. 755-765 ◽

Cited By ~ 25

Author(s):

KATHRYN BARTLEY ◽

JOHN F. HUNTLEY ◽

HARRY W. WRIGHT ◽

MINTU NATH ◽

ALASDAIR J. NISBET

Keyword(s):

Amino Acid ◽

Cathepsin D ◽

Proportional Hazards ◽

Proportional Hazards Model ◽

Dermanyssus Gallinae ◽

Poultry Red Mite ◽

Acid Protein ◽

Vaccine Antigens ◽

Potential Vaccine ◽

Amino Acid Protein

SUMMARYVaccination is a feasible strategy for controlling the haematophagous poultry red mite Dermanyssus gallinae. A cDNA library enriched for genes upregulated after feeding was created to identify potential vaccine antigens. From this library, a gene (Dg-CatD-1) encoding a 383 amino acid protein (Dg-CatD-1) with homology to cathepsin D lysosomal aspartyl proteinases was identified as a potential vaccine candidate. A second gene (Dg-CatL-1) encoding a 341 amino acid protein (Dg-CatL-1) with homology to cathepsin L cysteine proteinases was also selected for further study. IgY obtained from naturally infested hens failed to detect Dg-CatD-1 suggesting that it is a concealed antigen. Conversely, Dg-CatL-1 was detected by IgY derived from natural-infestation, indicating that infested hens are exposed to Dg-CatL-1. Mortality rates 120 h after mites had been fed anti-Dg-CatD-1 were significantly higher than those fed control IgY (PF<0·01). In a survival analysis, fitting a proportional hazards model to the time of death of mites, anti-Dg-CatD-1 and anti-Dg-CatL-1 IgY had 4·42 and 2·13 times higher risks of dying compared with controls (PF<0·05). Dg-CatD-1 and L-1 both have potential as vaccine antigens as part of a multi-component vaccine and have the potential to be improved as vaccine antigens using alternative expression systems.

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An improved method for in vitro feeding of adult female Dermanyssus gallinae (poultry red mite) using Baudruche membrane (goldbeater’s skin)

Parasites & Vectors ◽

10.1186/s13071-020-04471-x ◽

2020 ◽

Vol 13 (1) ◽

Author(s):

Francesca Nunn ◽

Jessica Baganz ◽

Kathryn Bartley ◽

Sarah Hall ◽

Stewart Burgess ◽

...

Keyword(s):

Adult Female ◽

Egg Laying ◽

Blood Type ◽

Dermanyssus Gallinae ◽

Feeding Rates ◽

Poultry Red Mite ◽

Polyester Mesh ◽

In Vitro Feeding

Abstract Background Dermanyssus gallinae, or poultry red mite (PRM), is an important ectoparasite in laying hen, having a significant effect on animal welfare and potentially causing economic loss. Testing novel control compounds typically involves in vitro methodologies before in vivo assessments. Historically, in vitro methods have involved PRM feeding on hen blood through a membrane. The use of hen blood requires multiple procedures (bleeds) to provide sufficient material, and the use of a larger species (e.g. goose) could serve as a refinement in the use of animals in research. Methods The in vitro feeding device used was that which currently employs a Parafilm™ M membrane (Bartley et al.: Int J Parasitol. 45:819–830, 2015). Adult female PMR were used to investigate any differences in mite feeding, egg laying and mortality when fed goose or hen blood. Effects on these parameters when PRM were fed through either the Parafilm™ M membrane or the Baudruche membrane alone or through a combination of the membrane with an overlaid polyester mesh were tested using goose blood. Results Poultry red mites fed equally well on goose or hen blood through the Parafilm™ M membrane, and there were no significant differences in mortality of PRM fed with either blood type. A significant increase (t test: t = 3.467, df = 4, P = 0.03) in the number of eggs laid per fed mite was observed when goose blood was used. A 70% increase in PRM feeding was observed when the mites were fed on goose blood through a Baudruche membrane compared to when they were fed goose blood through the Parafilm™ M membrane. The addition of an overlaid polyester mesh did not improve feeding rates. A significant increase (analysis of variance: F(3, 20) = 3.193, P = 0.04) in PRM egg laying was observed in mites fed on goose blood through the Baudruche membrane compared to those fed goose blood through the Parafilm™ M membrane. A mean of 1.22 (standard error of the mean ± 0.04) eggs per fed mite was obtained using the Baudruche feeding device compared to only 0.87 (SEM ± 0.3) eggs per fed mite using the Parafilm™ M device when neither was combined with a polyester mesh overlay. Conclusion The in vitro feeding of adult female PRM can be readily facilitated through the use of goose blood in feeding devices with the Baudruche membrane.

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Characterization, mode of action, and efficacy of twelve silica-based acaricides against poultry red mite (Dermanyssus gallinae) in vitro

Parasitology Research ◽

10.1007/s00436-014-3978-6 ◽

2014 ◽

Vol 113 (9) ◽

pp. 3167-3175 ◽

Cited By ~ 14

Author(s):

Johanna Schulz ◽

Jutta Berk ◽

Johanna Suhl ◽

Lars Schrader ◽

Stefan Kaufhold ◽

...

Keyword(s):

Mode Of Action ◽

Dermanyssus Gallinae ◽

Poultry Red Mite

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In vitro efficacies of oils, silicas and plant preparations against the poultry red mite Dermanyssus gallinae

Experimental and Applied Acarology ◽

10.1007/s10493-009-9254-2 ◽

2009 ◽

Vol 48 (1-2) ◽

pp. 31-41 ◽

Cited By ~ 32

Author(s):

Veronika Maurer ◽

Erika Perler ◽

Felix Heckendorn

Keyword(s):

Dermanyssus Gallinae ◽

Poultry Red Mite

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

10.1101/2021.04.14.439672 ◽

2021 ◽

Author(s):

Daniel R. G. Price ◽

Kathryn Bartley ◽

Damer P. Blake ◽

Eleanor Karp-Tatham ◽

Francesca Nunn ◽

...

Keyword(s):

Vitamin B1 ◽

Blood Feeding ◽

B Vitamins ◽

Dermanyssus Gallinae ◽

Poultry Red Mite ◽

Protein Coding ◽

Pathway Reconstruction ◽

Blood Sucking ◽

Metabolic Pathway Reconstruction ◽

B Vitamin

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.

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A Rickettsiella Endosymbiont Is a Potential Source of Essential B-Vitamins for the Poultry Red Mite, Dermanyssus gallinae

Frontiers in Microbiology ◽

10.3389/fmicb.2021.695346 ◽

2021 ◽

Vol 12 ◽

Author(s):

Daniel R. G. Price ◽

Kathryn Bartley ◽

Damer P. Blake ◽

Eleanor Karp-Tatham ◽

Francesca Nunn ◽

...

Keyword(s):

Amino Acids ◽

Egg Quality ◽

Vitamin B1 ◽

Blood Feeding ◽

B Vitamins ◽

Dermanyssus Gallinae ◽

Poultry Red Mite ◽

Pathway Reconstruction ◽

Blood Sucking ◽

B Vitamin

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.

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