Role of Staphylococcus agnetis and Staphylococcus hyicus in the Pathogenesis of Buffalo Fly Skin Lesions in Cattle

ABSTRACT Buffalo flies (Haematobia irritans exigua) are hematophagous ectoparasites of cattle causing production and welfare impacts in northern Australian herds. Skin lesions associated with buffalo fly infestation and Stephanofilaria nematode infection are manifested as focal dermatitis or ulcerat...

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Main Authors: Muhammad Noman Naseem, Conny Turni, Rosalind Gilbert, Ali Raza, Rachel Allavena, Michael McGowan, Constantin Constantinoiu, Chian Teng Ong, Ala E. Tabor, Peter James
Format: Article
Language:English
Published: American Society for Microbiology 2022-08-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.00873-22
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author Muhammad Noman Naseem
Conny Turni
Rosalind Gilbert
Ali Raza
Rachel Allavena
Michael McGowan
Constantin Constantinoiu
Chian Teng Ong
Ala E. Tabor
Peter James
author_facet Muhammad Noman Naseem
Conny Turni
Rosalind Gilbert
Ali Raza
Rachel Allavena
Michael McGowan
Constantin Constantinoiu
Chian Teng Ong
Ala E. Tabor
Peter James
author_sort Muhammad Noman Naseem
collection DOAJ
description ABSTRACT Buffalo flies (Haematobia irritans exigua) are hematophagous ectoparasites of cattle causing production and welfare impacts in northern Australian herds. Skin lesions associated with buffalo fly infestation and Stephanofilaria nematode infection are manifested as focal dermatitis or ulcerated areas, most commonly on the medial canthus of the eye, along the lateral and ventral neck, and on the abdomen of cattle. For closely related horn flies (Haematobia irritans irritans), Staphylococcus aureus has been suggested as a contributing factor in the development of lesions. To investigate the potential role of bacterial infection in the pathogenesis of buffalo fly lesions, swabs were taken from lesions and normal skin, and bacteria were also isolated from surface washings of buffalo flies and surface-sterilized homogenized flies. Bacterial identification was conducted by matrix-assisted laser desorption ionization–time of flight (MALDI-TOF) and strain typing by repetitive sequence-based PCR (rep-PCR) and DNA sequencing to determine species similarity and virulence factors. Of 50 bacterial isolates collected from lesions, 38 were identified as Staphylococcus agnetis and 12 as Staphylococcus hyicus, whereas four isolates from normal skin were S. hyicus and one was Mammaliicoccus sciuri. Of the Staphylococcus isolates isolated from buffalo flies, five were identified as S. agnetis and three as S. hyicus. Fifty percent of the buffalo fly isolates had rep-PCR genotypic patterns identical to those of the lesion isolates. Genome sequencing of 16 S. agnetis and four S. hyicus isolates revealed closely similar virulence factor profiles, with all isolates possessing exfoliative toxin A and C genes. The findings from this study suggest the involvement of S. agnetis and S. hyicus in buffalo fly lesion pathogenesis. This should be taken into account in the development of effective treatment and control strategies for lesions. IMPORTANCE Skin lesions in cattle associated with feeding by Haematobia fly species are a significant welfare issue in Australia, North and South America, and Europe. The development of these lesions has been attributed to a number of causal factors, but the exact etiology and pathogenesis were unclear. This study characterized Staphylococcus agnetis and Staphylococcus hyicus strains from cattle skin lesions and in vector flies and demonstrated their role in the pathogenesis of these lesions. These findings will aid the development of targeted and more effective treatment and control strategies for lesions associated with fly infestation in cattle.
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spelling doaj.art-cfb7c83518164d51b85dec368411854a2022-12-22T04:19:14ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-08-0110410.1128/spectrum.00873-22Role of Staphylococcus agnetis and Staphylococcus hyicus in the Pathogenesis of Buffalo Fly Skin Lesions in CattleMuhammad Noman Naseem0Conny Turni1Rosalind Gilbert2Ali Raza3Rachel Allavena4Michael McGowan5Constantin Constantinoiu6Chian Teng Ong7Ala E. Tabor8Peter James9The University of Queensland, Queensland Alliance for Agriculture and Food Innovation, Centre for Animal Science, St. Lucia, Queensland, AustraliaThe University of Queensland, Queensland Alliance for Agriculture and Food Innovation, Centre for Animal Science, St. Lucia, Queensland, AustraliaThe University of Queensland, Queensland Alliance for Agriculture and Food Innovation, Centre for Animal Science, St. Lucia, Queensland, AustraliaThe University of Queensland, Queensland Alliance for Agriculture and Food Innovation, Centre for Animal Science, St. Lucia, Queensland, AustraliaThe University of Queensland, School of Veterinary Science, Gatton, Queensland, AustraliaThe University of Queensland, School of Veterinary Science, Gatton, Queensland, AustraliaJames Cook University, College of Public Health, Medical & Veterinary Sciences, Townsville, Queensland, AustraliaThe University of Queensland, Queensland Alliance for Agriculture and Food Innovation, Centre for Animal Science, St. Lucia, Queensland, AustraliaThe University of Queensland, Queensland Alliance for Agriculture and Food Innovation, Centre for Animal Science, St. Lucia, Queensland, AustraliaThe University of Queensland, Queensland Alliance for Agriculture and Food Innovation, Centre for Animal Science, St. Lucia, Queensland, AustraliaABSTRACT Buffalo flies (Haematobia irritans exigua) are hematophagous ectoparasites of cattle causing production and welfare impacts in northern Australian herds. Skin lesions associated with buffalo fly infestation and Stephanofilaria nematode infection are manifested as focal dermatitis or ulcerated areas, most commonly on the medial canthus of the eye, along the lateral and ventral neck, and on the abdomen of cattle. For closely related horn flies (Haematobia irritans irritans), Staphylococcus aureus has been suggested as a contributing factor in the development of lesions. To investigate the potential role of bacterial infection in the pathogenesis of buffalo fly lesions, swabs were taken from lesions and normal skin, and bacteria were also isolated from surface washings of buffalo flies and surface-sterilized homogenized flies. Bacterial identification was conducted by matrix-assisted laser desorption ionization–time of flight (MALDI-TOF) and strain typing by repetitive sequence-based PCR (rep-PCR) and DNA sequencing to determine species similarity and virulence factors. Of 50 bacterial isolates collected from lesions, 38 were identified as Staphylococcus agnetis and 12 as Staphylococcus hyicus, whereas four isolates from normal skin were S. hyicus and one was Mammaliicoccus sciuri. Of the Staphylococcus isolates isolated from buffalo flies, five were identified as S. agnetis and three as S. hyicus. Fifty percent of the buffalo fly isolates had rep-PCR genotypic patterns identical to those of the lesion isolates. Genome sequencing of 16 S. agnetis and four S. hyicus isolates revealed closely similar virulence factor profiles, with all isolates possessing exfoliative toxin A and C genes. The findings from this study suggest the involvement of S. agnetis and S. hyicus in buffalo fly lesion pathogenesis. This should be taken into account in the development of effective treatment and control strategies for lesions. IMPORTANCE Skin lesions in cattle associated with feeding by Haematobia fly species are a significant welfare issue in Australia, North and South America, and Europe. The development of these lesions has been attributed to a number of causal factors, but the exact etiology and pathogenesis were unclear. This study characterized Staphylococcus agnetis and Staphylococcus hyicus strains from cattle skin lesions and in vector flies and demonstrated their role in the pathogenesis of these lesions. These findings will aid the development of targeted and more effective treatment and control strategies for lesions associated with fly infestation in cattle.https://journals.asm.org/doi/10.1128/spectrum.00873-22Staphylococcus agnetisStaphylococcus hyicusHaematobiabuffalo fly lesionscattleexfoliative toxin
spellingShingle Muhammad Noman Naseem
Conny Turni
Rosalind Gilbert
Ali Raza
Rachel Allavena
Michael McGowan
Constantin Constantinoiu
Chian Teng Ong
Ala E. Tabor
Peter James
Role of Staphylococcus agnetis and Staphylococcus hyicus in the Pathogenesis of Buffalo Fly Skin Lesions in Cattle
Microbiology Spectrum
Staphylococcus agnetis
Staphylococcus hyicus
Haematobia
buffalo fly lesions
cattle
exfoliative toxin
title Role of Staphylococcus agnetis and Staphylococcus hyicus in the Pathogenesis of Buffalo Fly Skin Lesions in Cattle
title_full Role of Staphylococcus agnetis and Staphylococcus hyicus in the Pathogenesis of Buffalo Fly Skin Lesions in Cattle
title_fullStr Role of Staphylococcus agnetis and Staphylococcus hyicus in the Pathogenesis of Buffalo Fly Skin Lesions in Cattle
title_full_unstemmed Role of Staphylococcus agnetis and Staphylococcus hyicus in the Pathogenesis of Buffalo Fly Skin Lesions in Cattle
title_short Role of Staphylococcus agnetis and Staphylococcus hyicus in the Pathogenesis of Buffalo Fly Skin Lesions in Cattle
title_sort role of staphylococcus agnetis and staphylococcus hyicus in the pathogenesis of buffalo fly skin lesions in cattle
topic Staphylococcus agnetis
Staphylococcus hyicus
Haematobia
buffalo fly lesions
cattle
exfoliative toxin
url https://journals.asm.org/doi/10.1128/spectrum.00873-22
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