The bovine nasal fungal community and associations with bovine respiratory disease

Introduction Effective identification and treatment of bovine respiratory disease (BRD) is an ongoing health and economic issue for the dairy and beef cattle industries. Bacteria pathogens Pasteurellamultocida, Mycoplasmabovis, Mannheimia haemolytica, and Histophilus somni and the virus Bovine herpesvirus-1 (BHV-1), Bovine parainfluenza-3 virus (BPIV-3), Bovine respiratory syncytial virus (BRSV), Bovine adenovirus 3 (BAdV3), bovine coronavirus (BoCV) and Bovine viral diarrhea virus (BVDV) have commonly been identified in BRD cattle; however, no studies have investigated the fungal community and how it may also relate to BRD. Methods The objective of this study was to understand if the nasal mycobiome differs between a BRD-affected (n = 56) and visually healthy (n = 73) Holstein steers. Fungal nasal community was determined by using Internal Transcribed Spacer (ITS) sequencing. Results The phyla, Ascomycota and Basidiomycota, and the genera, Trichosporon and Issatchenkia, were the most abundant among all animals, regardless of health status. We identified differences between healthy and BRD animals in abundance of Trichosporon and Issatchenkia orientalis at a sub-species level that could be a potential indicator of BRD. No differences were observed in the nasal fungal alpha and beta diversity between BRD and healthy animals. However, the fungal community structure was affected based on season, specifically when comparing samples collected in the summer to the winter season. We then performed a random forest model, based on the fungal community and abundance of the BRD-pathobionts (qPCR data generated from a previous study using the same animals), to classify healthy and BRD animals and determine the agreement with visual diagnosis. Classification of BRD or healthy animals using ITS sequencing was low and agreed with the visual diagnosis with an accuracy of 51.9%. A portion of the ITS-predicted BRD animals were not predicted based on the abundance of BRD pathobionts. Lastly, fungal and bacterial co-occurrence were more common in BRD animals than healthy animals. Discussion The results from this novel study provide a baseline understanding of the fungal diversity and composition in the nasal cavity of BRD and healthy animals, upon which future interaction studies, including other nasal microbiome members to further understand and accurately diagnose BRD, can be designed.

[1]  Josiah Levi Davidson,et al.  Identification of bovine respiratory disease through the nasal microbiome , 2022, Animal microbiome.

[2]  J. Devlin,et al.  Crossing Kingdoms: How the Mycobiota and Fungal-Bacterial Interactions Impact Host Health and Disease , 2021, Infection and Immunity.

[3]  A. Hanaka,et al.  Mortierella Species as the Plant Growth-Promoting Fungi Present in the Agricultural Soils , 2020 .

[4]  M. Zeineldin,et al.  Meta-analysis of bovine respiratory microbiota: Link between respiratory microbiota and bovine respiratory health. , 2020, FEMS microbiology ecology.

[5]  R. Casagrande,et al.  Necrotizing Tracheobronchitis Caused by Aspergillus fumigatus in a Cow. , 2020, Journal of comparative pathology.

[6]  M. Workentine,et al.  Topography of the respiratory tract bacterial microbiota in cattle , 2020, Microbiome.

[7]  P. Capozza,et al.  Prevalence of Pathogens Related to Bovine Respiratory Disease Before and After Transportation in Beef Steers: Preliminary Results , 2019, Animals : an open access journal from MDPI.

[8]  Michael W Taylor,et al.  Longitudinal study of the bacterial and fungal microbiota in the human sinuses reveals seasonal and annual changes in diversity , 2019, Scientific Reports.

[9]  Lei Zhang,et al.  Current Challenges and Future Perspectives , 2019, Advanced Materials for Sodium Ion Storage.

[10]  Margaret Arnd-Caddigan,et al.  Current Knowledge and Perspectives , 2019, Intuition in Psychotherapy.

[11]  K. Orsel,et al.  Comparison of the nasopharyngeal bacterial microbiota of beef calves raised without the use of antimicrobials between healthy calves and those diagnosed with bovine respiratory disease. , 2019, Veterinary microbiology.

[12]  Kevin P. Byrne,et al.  Population genomics shows no distinction between pathogenic Candida krusei and environmental Pichia kudriavzevii: One species, four names , 2018, PLoS pathogens.

[13]  S. Seyedmousavi,et al.  Fungal infections in animals: a patchwork of different situations. , 2018, Medical mycology.

[14]  F. Cerutti,et al.  Characterization of the upper and lower respiratory tract microbiota in Piedmontese calves , 2017, Microbiome.

[15]  J. Lowe,et al.  Disparity in the nasopharyngeal microbiota between healthy cattle on feed, at entry processing and with respiratory disease. , 2017, Veterinary microbiology.

[16]  J. Keele,et al.  Evaluating the microbiome of two sampling locations in the nasal cavity of cattle with bovine respiratory disease complex (BRDC). , 2017, Journal of animal science.

[17]  Irina Leonardi,et al.  Fungal dysbiosis: immunity and interactions at mucosal barriers , 2017, Nature Reviews Immunology.

[18]  C. Manichanh,et al.  The microbiome in respiratory medicine: current challenges and future perspectives , 2017, European Respiratory Journal.

[19]  E. Ganda,et al.  Deciphering upper respiratory tract microbiota complexity in healthy calves and calves that develop respiratory disease using shotgun metagenomics. , 2017, Journal of dairy science.

[20]  C. Murray,et al.  The use of PCR/Electrospray Ionization-Time-of-Flight-Mass Spectrometry (PCR/ESI-TOF-MS) to detect bacterial and fungal colonization in healthy military service members , 2016, BMC Infectious Diseases.

[21]  Paul J. McMurdie,et al.  DADA2: High resolution sample inference from Illumina amplicon data , 2016, Nature Methods.

[22]  Daniel M. Griffith,et al.  cooccur: Probabilistic Species Co-Occurrence Analysis in R , 2016 .

[23]  M. Bakhshaee,et al.  Nasal and Indoors Fungal Contamination in Healthy Subjects , 2016 .

[24]  Edouard Timsit,et al.  A Systematic Review of Bovine Respiratory Disease Diagnosis Focused on Diagnostic Confirmation, Early Detection, and Prediction of Unfavorable Outcomes in Feedlot Cattle. , 2015, The Veterinary clinics of North America. Food animal practice.

[25]  E. Timsit,et al.  The nasopharyngeal microbiota of feedlot cattle , 2015, Scientific Reports.

[26]  E. Topp,et al.  The nasopharyngeal microbiota of feedlot cattle that develop bovine respiratory disease. , 2015, Veterinary microbiology.

[27]  E. Mylonakis,et al.  Fungal–bacterial interactions and their relevance in health , 2015, Cellular microbiology.

[28]  Philippe Lejeune,et al.  Canopy Gap Mapping from Airborne Laser Scanning: An Assessment of the Positional and Geometrical Accuracy , 2015, Remote. Sens..

[29]  Alison L. Van Eenennaam,et al.  A Metagenomics and Case-Control Study To Identify Viruses Associated with Bovine Respiratory Disease , 2015, Journal of Virology.

[30]  J. Klironomos,et al.  Relationships of fungal spore concentrations in the air and meteorological factors , 2015 .

[31]  D. Newman,et al.  Anaerobic Bacteria Grow within Candida albicans Biofilms and Induce Biofilm Formation in Suspension Cultures , 2014, Current Biology.

[32]  Luisa Delgado-Serrano,et al.  Respiratory tract clinical sample selection for microbiota analysis in patients with pulmonary tuberculosis , 2014, Microbiome.

[33]  D. Underhill,et al.  The mycobiota: interactions between commensal fungi and the host immune system , 2014, Nature Reviews Immunology.

[34]  G. Herrler,et al.  Three viruses of the bovine respiratory disease complex apply different strategies to initiate infection , 2014, Veterinary Research.

[35]  R. Zaheer,et al.  Pathogens of Bovine Respiratory Disease in North American Feedlots Conferring Multidrug Resistance via Integrative Conjugative Elements , 2013, Journal of Clinical Microbiology.

[36]  D. Castelo-Branco,et al.  Species of Candida as a component of the nasal microbiota of healthy horses. , 2013, Medical mycology.

[37]  E. Ghedin,et al.  The human mycobiome in health and disease , 2013, Genome Medicine.

[38]  Mark V Brown,et al.  Microbial community responses to anthropogenically induced environmental change: towards a systems approach. , 2013, Ecology letters.

[39]  G. S. de Hoog,et al.  A comprehensive molecular phylogeny of the Mortierellales (Mortierellomycotina) based on nuclear ribosomal DNA , 2013, Persoonia.

[40]  S. Leroy,et al.  The Airway Microbiota in Cystic Fibrosis: A Complex Fungal and Bacterial Community—Implications for Therapeutic Management , 2012, PloS one.

[41]  H. Seegers,et al.  Visually undetected fever episodes in newly received beef bulls at a fattening operation: occurrence, duration, and impact on performance. , 2011, Journal of animal science.

[42]  A. Strzelczak,et al.  The relationships between air pollutants, meteorological parameters and concentration of airborne fungal spores. , 2011, Environmental pollution.

[43]  D. Renter,et al.  Temporal distributions of respiratory disease events within cohorts of feedlot cattle and associations with cattle health and performance indices. , 2010, Preventive veterinary medicine.

[44]  A. Confer,et al.  The epidemiology of bovine respiratory disease: What is the evidence for predisposing factors? , 2010, The Canadian veterinary journal = La revue veterinaire canadienne.

[45]  D. S. McVey,et al.  Bacterial pathogens of the bovine respiratory disease complex. , 2010, The Veterinary clinics of North America. Food animal practice.

[46]  Ning Ma,et al.  BLAST+: architecture and applications , 2009, BMC Bioinformatics.

[47]  R. Fulton Viral Diseases of the Bovine Respiratory Tract , 2009, Food Animal Practice.

[48]  David G Renter,et al.  Bayesian Estimation of the Performance of Using Clinical Observations and Harvest Lung Lesions for Diagnosing Bovine Respiratory Disease in Post-weaned Beef Calves , 2009, Journal of veterinary diagnostic investigation : official publication of the American Association of Veterinary Laboratory Diagnosticians, Inc.

[49]  A. Confer,et al.  Pasteurella multocida and bovine respiratory disease , 2007, Animal Health Research Reviews.

[50]  D. Hodgins,et al.  Mannheimia haemolytica and bovine respiratory disease , 2007, Animal Health Research Reviews.

[51]  Hayato Yamana,et al.  Improvement in accuracy of multiple sequence alignment using novel group-to-group sequence alignment algorithm with piecewise linear gap cost , 2006, BMC Bioinformatics.

[52]  L D Van Vleck,et al.  Bovine respiratory disease in feedlot cattle: environmental, genetic, and economic factors. , 2006, Journal of animal science.

[53]  R. Knight,et al.  UniFrac: a New Phylogenetic Method for Comparing Microbial Communities , 2005, Applied and Environmental Microbiology.

[54]  D. Desmecht,et al.  How Mannheimia haemolytica defeats host defence through a kiss of death mechanism. , 2005, Veterinary research.

[55]  J. G. Kirkpatrick,et al.  Respiratory tract infections in dairy calves from birth to breeding age , 2005, The Bovine Practitioner.

[56]  K. Katoh,et al.  MAFFT version 5: improvement in accuracy of multiple sequence alignment , 2005, Nucleic acids research.

[57]  S. Srivastava,et al.  Prevalent Serotypes of Pasteurella multocida Isolated from Different Animal and Avian Species in India , 2004, Veterinary Research Communications.

[58]  H. Alexandre,et al.  Saccharomyces cerevisiae-Oenococcus oeni interactions in wine: current knowledge and perspectives. , 2004, International journal of food microbiology.

[59]  P. Nicholson,et al.  Development of PCR assays for the detection and differentiation of Fusarium sporotrichioides and Fusarium langsethiae. , 2004, FEMS microbiology letters.

[60]  M. Payton,et al.  Evaluation of health status of calves and the impact on feedlot performance: assessment of a retained ownership program for postweaning calves. , 2002, Canadian journal of veterinary research = Revue canadienne de recherche veterinaire.

[61]  L. W. Greene,et al.  Dietary zinc and manganese sources administered from the fetal stage onwards affect immune response of transit stressed and virus infected offspring steer calves , 2001 .

[62]  A. Hasegawa,et al.  Isolation of Candida krusei from a case of bovine bronchopneumonia in a one-year-old heifer , 2001, Veterinary Record.

[63]  A. Bottalico FUSARIUM DISEASES OF CEREALS: SPECIES COMPLEX AND RELATED MYCOTOXIN PROFILES, IN EUROPE , 1998 .

[64]  A. Edwards Respiratory diseases of feedlot cattle in central USA , 1996, The Bovine Practitioner.

[65]  H. Schønheyder,et al.  Bovine mycotic abortion--a comparative study of diagnostic methods. , 1991, Zentralblatt fur Veterinarmedizin. Reihe B. Journal of veterinary medicine. Series B.

[66]  H. Jensen,et al.  Mycosis in the Stomach Compartments of Cattle , 1989, Acta Veterinaria Scandinavica.

[67]  Philip H. Ramsey Nonparametric Statistical Methods , 1974, Technometrics.

[68]  D. Bauer Constructing Confidence Sets Using Rank Statistics , 1972 .

[69]  E. C. Pielou The measurement of diversity in different types of biological collections , 1966 .

[70]  A. Saini,et al.  Fungal and Parasitic CNS Infections , 2017, The Indian Journal of Pediatrics.

[71]  Daniel M. Griffith,et al.  Probabilistic Species Co-Occurrence Analysis in R , 2016 .

[72]  Manuela Oliveira,et al.  The effects of meteorological factors on airborne fungal spore concentration in two areas differing in urbanisation level , 2009, International journal of biometeorology.

[73]  G. Torpier,et al.  Preliminary results , 2007 .

[74]  D. Hodgins,et al.  Respiratory Viruses and Bacteria in Cattle , 2002 .

[75]  P. Shewen,et al.  Bovine respiratory disease: commercial vaccines currently available in Canada. , 2000, The Canadian veterinary journal = La revue veterinaire canadienne.

[76]  D. Faith Conservation evaluation and phylogenetic diversity , 1992 .

[77]  A. Chao Nonparametric estimation of the number of classes in a population , 1984 .