1887

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Volume 102, Issue 10

Comparison of gut viral communities in diarrhoea and healthy dairy calves No Access

Abstract

Calf diarrhoea has been a major cause of economic losses in the global dairy industry. Many factors, including multiple pathogen infections, can directly or indirectly cause calf diarrhoea. This study compared the faecal virome between 15 healthy calves and 15 calves with diarrhoea. Significantly lower diversity of viruses was found in samples from animals with diarrhoea than those in the healthy ones, and this feature may also be related to the age of the calves. Viruses belonging to the families and that may cause diarrhoea in dairy calves have been characterized, which revealed that reads of caliciviruses and astroviruses in diarrhoea calves were much higher than those in healthy calves. Five complete genomic sequences closely related to have been identified, which may participate in the regulation of the gut virus community ecology of healthy hosts together with bacteriophages. This research provides a theoretical basis for further understanding of known or potential enteric pathogens related to calf diarrhoea.

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  • Accepted:
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Keyword(s): dairy calves , diarrhea , metagenomics , virome and virus diversity
© 2021 The Authors
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/content/journal/jgv/10.1099/jgv.0.001663
2021-10-29
2024-04-18
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References

  1. Izzo MM, Kirkland PD, Mohler VL, Perkins NR, Gunn AA et al. Prevalence of major enteric pathogens in australian dairy calves with diarrhoea. Aust Vet J 2011; 89:167–173 [View Article] [PubMed]
     [Google Scholar]
  2. Lee SH, Kim HY, Choi EW, Kim D. Causative agents and epidemiology of diarrhea in Korean native calves. J Vet Sci 2019; 20:e64 [View Article] [PubMed]
     [Google Scholar]
  3. Ling Y, Zhang X, Qi G, Yang S, Jingjiao L et al. Viral metagenomics reveals significant viruses in the genital tract of apparently healthy dairy cows. Arch Virol 2019; 164:1059–1067 [View Article] [PubMed]
     [Google Scholar]
  4. Bendali F, Bichet H, Schelcher F, Sanaa M. Pattern of diarrhoea in newborn beef calves in South-west France. Vet Res 1999; 30:61–74 [PubMed]
     [Google Scholar]
  5. Alfred N, Liu H, Li ML, Hong SF, Tang HB et al. Molecular epidemiology and phylogenetic analysis of diverse bovine astroviruses associated with diarrhea in cattle and water buffalo calves in China. J Vet Med Sci 2015; 77:643–651 [View Article] [PubMed]
     [Google Scholar]
  6. Smiley JR, Chang KO, Hayes J, Vinjé J, Saif LJ. Characterization of an enteropathogenic bovine calicivirus representing a potentially new calicivirus genus. J Virol 2002; 76:10089–10098 [View Article] [PubMed]
     [Google Scholar]
  7. Civra A, Altomare A, Francese R, Donalisio M, Aldini G et al. Colostrum from cows immunized with a veterinary vaccine against bovine rotavirus displays enhanced in vitro anti-human rotavirus activity. J Dairy Sci 2019; 102:4857–4869 [View Article] [PubMed]
     [Google Scholar]
  8. Dudleenamjil E, Lin C-Y, Dredge D, Murray BK, Robison RA et al. Bovine parvovirus uses clathrin-mediated endocytosis for cell entry. J Gen Virol 2010; 91:3032–3041 [View Article] [PubMed]
     [Google Scholar]
  9. Fahkrajang W, Sudaryatma PE, Mekata H, Hamabe S, Saito A et al. Bovine respiratory coronavirus enhances bacterial adherence by upregulating expression of cellular receptors on bovine respiratory epithelial cells. Vet Microbiol 2021; 255:109017 [View Article] [PubMed]
     [Google Scholar]
  10. Odeón AC, Risatti G, Kaiser GG, Leunda MR, Odriozola E et al. Bovine viral diarrhea virus genomic associations in mucosal disease, enteritis and generalized dermatitis outbreaks in Argentina. Vet Microbiol 2003; 96:133–144 [View Article] [PubMed]
     [Google Scholar]
  11. Sandals WC, Povey RC, Meek AH. Prevalence of bovine parvovirus infection in Ontario dairy cattle. Can J Vet Res 1995; 59:81–86 [PubMed]
     [Google Scholar]
  12. Livingstone M, Aitchison K, Dagleish M, Longbottom D. De novo whole-genome sequencing and annotation of pathogenic bovine Pasteurella multocida type a:3 strains. Microbiol Resour Announc 2020; 9: [View Article] [PubMed]
     [Google Scholar]
  13. Pires PS, Santos RL, da Paixão TA, de Oliveira Bernardes LC, de Macêdo AA et al. Intracellular survival of clostridium chauvoei in bovine macrophages. Vet Microbiol 2017; 199:1–7 [View Article] [PubMed]
     [Google Scholar]
  14. Raheel IAER, Hassan WH, Salem SSR, Salam HSH. Biofilm forming potentiality of Escherichia coli isolated from bovine endometritis and their antibiotic resistance profiles. J Adv Vet Anim Res 2020; 7:442–451 [View Article] [PubMed]
     [Google Scholar]
  15. van Altena SEC, Peen MA, van der Linden FH, Parmentier HK, Savelkoul HFJ et al. Bovine natural antibodies in antibody-dependent bactericidal activity against Escherichia coli and Salmonella typhimurium and risk of mastitis. Vet Immunol Immunopathol 2016; 171:21–27 [View Article] [PubMed]
     [Google Scholar]
  16. Koutny H, Joachim A, Tichy A, Baumgartner W. Bovine Eimeria species in Austria. Parasitol Res 2012; 110:1893–1901 [View Article]
     [Google Scholar]
  17. Ryff KL, Bergstrom RC. Bovine coccidia in American bison. J Wildl Dis 1975; 11:412–414 [View Article] [PubMed]
     [Google Scholar]
  18. Taminelli V, Eckert J, Sydler T, Gottstein B, Corboz L et al. Experimental infection of calves and sheep with bovine giardia isolates. Schweiz Arch Tierheilkd 1989; 131:551–564 [PubMed]
     [Google Scholar]
  19. Yang Z, Fu Y, Gong P, Zheng J, Liu L et al. Bovine tlr2 and tlr4 mediate Cryptosporidium parvum recognition in bovine intestinal epithelial cells. Microb Pathog 2015; 85:29–34 [View Article] [PubMed]
     [Google Scholar]
  20. Crouch CF, Oliver S, Francis MJ. Serological, colostral and milk responses of cows vaccinated with a single dose of a combined vaccine against rotavirus, coronavirus and Escherichia coli F5 (K99. Vet Rec 2001; 149:105–108 [View Article] [PubMed]
     [Google Scholar]
  21. He X, Parenti M, Grip T, Lönnerdal B, Timby N et al. Fecal microbiome and metabolome of infants fed bovine mfgm supplemented formula or standard formula with breast-fed infants as reference: A randomized controlled trial. Sci Rep 2019; 9:11589 [View Article] [PubMed]
     [Google Scholar]
  22. Wang H, Ling Y, Shan T, Yang S, Xu H et al. Gut virome of mammals and birds reveals high genetic diversity of the family microviridae. Virus Evol 2019; 5:vez013 [View Article] [PubMed]
     [Google Scholar]
  23. Zhang W, Li L, Deng X, Kapusinszky B, Pesavento PA et al. Faecal Virome of cats in an animal shelter. J Gen Virol 2014; 95:2553–2564 [View Article] [PubMed]
     [Google Scholar]
  24. Deng X, Naccache SN, Ng T, Federman S, Li L et al. An ensemble strategy that significantly improves de novo assembly of microbial genomes from metagenomic next-generation sequencing data. Nucleic Acids Res 2015; 43:e46 [View Article] [PubMed]
     [Google Scholar]
  25. Skewes-Cox P, Sharpton TJ, Pollard KS, DeRisi JL. Profile hidden Markov models for the detection of viruses within metagenomic sequence data. PLoS One 2014; 9:e105067 [View Article] [PubMed]
     [Google Scholar]
  26. Eddy SR. A new generation of homology search tools based on probabilistic inference. Genome Inform 2009; 23:205–211 [PubMed]
     [Google Scholar]
  27. Finn RD, Clements J, Eddy SR. HMMER web server: Interactive sequence similarity searching. Nucleic Acids Res 2011; 39:W29–37 [View Article]
     [Google Scholar]
  28. Johnson LS, Eddy SR, Portugaly E. Hidden markov model speed heuristic and iterative HMM search procedure. BMC Bioinformatics 2010; 11:431 [View Article] [PubMed]
     [Google Scholar]
  29. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M et al. Geneious basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012; 28:1647–1649 [View Article] [PubMed]
     [Google Scholar]
  30. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article]
     [Google Scholar]
  31. Kuraku S, Zmasek CM, Nishimura O, Katoh K. Aleaves facilitates on-demand exploration of metazoan gene family trees on MAFFT sequence alignment server with enhanced interactivity. Nucleic Acids Res 2013; 41:W22–8 [View Article] [PubMed]
     [Google Scholar]
  32. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A et al. Mrbayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 2012; 61:539–542 [View Article] [PubMed]
     [Google Scholar]
  33. Leung DYM, Calatroni A, Zaramela LS, LeBeau PK, Dyjack N et al. The nonlesional skin surface distinguishes atopic dermatitis with food allergy as a unique endotype. Sci Transl Med 2019; 11: [View Article] [PubMed]
     [Google Scholar]
  34. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L et al. Metagenomic Biomarker discovery and explanation. Genome Biol 2011; 12:R60 [View Article] [PubMed]
     [Google Scholar]
  35. Fernández-Correa I, Truchado DA, Gomez-Lucia E, Doménech A, Pérez-Tris J et al. A novel group of avian astroviruses from neotropical passerine birds broaden the diversity and host range of astroviridae. Sci Rep 2019; 9:9513 [View Article] [PubMed]
     [Google Scholar]
  36. Donato C, Vijaykrishna D. The broad host range and genetic diversity of mammalian and avian astroviruses. Viruses 2017; 9: [View Article] [PubMed]
     [Google Scholar]
  37. Krishnan T. Novel human astroviruses: challenges for developing countries. Virusdisease 2014; 25:208–214 [View Article] [PubMed]
     [Google Scholar]
  38. Appleton H, Higgins PG. Letter: Viruses and gastroenteritis in infants. Lancet 1975; 1:1297 [View Article] [PubMed]
     [Google Scholar]
  39. Bouzalas IG, Wüthrich D, Walland J, Drögemüller C, Zurbriggen A et al. Neurotropic astrovirus in cattle with nonsuppurative encephalitis in Europe. J Clin Microbiol 2014; 52:3318–3324 [View Article] [PubMed]
     [Google Scholar]
  40. Pfaff F, Schlottau K, Scholes S, Courtenay A, Hoffmann B et al. A novel astrovirus associated with encephalitis and ganglionitis in domestic sheep. Transbound Emerg Dis 2017; 64:677–682 [View Article] [PubMed]
     [Google Scholar]
  41. Opriessnig T, Xiao CT, Halbur PG. Porcine astrovirus type 5-associated enteritis in pigs. J Comp Pathol 2020; 181:38–46 [View Article] [PubMed]
     [Google Scholar]
  42. De Benedictis P, Schultz-Cherry S, Burnham A, Cattoli G. astrovirus infections in humans and animals - molecular biology, genetic diversity, and interspecies transmissions. Infect Genet Evol 2011; 11:1529–1544 [View Article] [PubMed]
     [Google Scholar]
  43. Alkan F, Karayel İ, Catella C, Bodnar L, Lanave G et al. Identification of a bovine enteric calicivirus, kırklareli virus, distantly related to neboviruses, in calves with enteritis in Turkey. J Clin Microbiol 2015; 53:3614–3617 [View Article] [PubMed]
     [Google Scholar]
  44. de Souza WM, Fumagalli MJ, de Araujo J, Ometto T, Modha S et al. Discovery of novel astrovirus and calicivirus identified in Ruddy turnstones in Brazil. Sci Rep 2019; 9:5556 [View Article] [PubMed]
     [Google Scholar]
  45. Wang F, Wang M, Dong Y, Zhang B, Zhang D. Genetic characterization of a novel calicivirus from a goose. Arch Virol 2017; 162:2115–2118 [View Article] [PubMed]
     [Google Scholar]
  46. Mor SK, Phelps NBD, Ng TFF, Subramaniam K, Primus A et al. Genomic characterization of a novel calicivirus, FHMCV-2012, from baitfish in the USA. Arch Virol 2017; 162:3619–3627 [View Article] [PubMed]
     [Google Scholar]
  47. Tan le V, van Doorn HR, Nghia HD, Chau TT, Tu le TP et al. Identification of a new cyclovirus in cerebrospinal fluid of patients with acute central nervous system infections. mBio 2013; 4:e00231
     [Google Scholar]
  48. Garigliany M-M, Börstler J, Jöst H, Badusche M, Desmecht D et al. Characterization of a novel circo-like virus in Aedes vexans mosquitoes from Germany: Evidence for a new genus within the family Circoviridae. J Gen Virol 2015; 96:915–920 [View Article] [PubMed]
     [Google Scholar]
  49. Ge X, Li J, Peng C, Wu L, Yang X et al. Genetic diversity of novel circular ssdna viruses in bats in China. J Gen Virol 2011; 92:2646–2653 [View Article] [PubMed]
     [Google Scholar]
  50. Ikegami M, Yazaki K, Honda Y, Iwaki M, Fujii H et al. Single-stranded dna in mung bean yellow Mosaic virus. Microbiol Immunol 1985; 29:783–789 [View Article] [PubMed]
     [Google Scholar]
  51. Kraberger S, Stainton D, Dayaram A, Zawar-Reza P, Gomez C et al. Discovery of Sclerotinia sclerotiorum Hypovirulence-associated virus-1 in urban river sediments of heathCote and Styx Rivers in Christchurch City, New Zealand. Genome Announc 2013; 1: [View Article] [PubMed]
     [Google Scholar]
  52. Woode GN, Bridger JC. Isolation of small viruses resembling astroviruses and caliciviruses from acute enteritis of calves. J Med Microbiol 1978; 11:441–452 [View Article] [PubMed]
     [Google Scholar]
  53. Woode GN, Gourley NE, Pohlenz JF, Liebler EM, Mathews SL et al. Serotypes of bovine astrovirus. J Clin Microbiol 1985; 22:668–670 [View Article] [PubMed]
     [Google Scholar]
  54. Martella V, Catella C, Capozza P, Diakoudi G, Camero M et al. Identification of astroviruses in bovine and buffalo calves with enteritis. Res Vet Sci 2020; 131:59–68 [View Article] [PubMed]
     [Google Scholar]
  55. Nagai M, Omatsu T, Aoki H, Otomaru K, Uto T et al. Full genome analysis of bovine astrovirus from fecal samples of cattle in Japan: Identification of possible interspecies transmission of bovine astrovirus. Arch Virol 2015; 160:2491–2501 [View Article] [PubMed]
     [Google Scholar]
  56. Tse H, Chan W-M, Tsoi H-W, Fan RYY, Lau CCY et al. Rediscovery and genomic characterization of bovine astroviruses. J Gen Virol 2011; 92:1888–1898 [View Article] [PubMed]
     [Google Scholar]
  57. Myrmel M. Development of a strand specific SYBRGreen RT-PCR for a GIII.2 bovine Norovirus. J Virol Methods 2013; 190:17–19 [View Article] [PubMed]
     [Google Scholar]
  58. Guo Z, He Q, Zhang B, Yue H, Tang C. Detection and molecular characteristics of neboviruses in dairy cows in China. J Gen Virol 2019; 100:35–45 [View Article] [PubMed]
     [Google Scholar]
  59. Liu BL, Lambden PR, Günther H, Otto P, Elschner M et al. Molecular characterization of a bovine enteric calicivirus: Relationship to the norwalk-like viruses. J Virol 1999; 73:819–825 [View Article] [PubMed]
     [Google Scholar]
  60. Sikorski A, Arguello-Astorga GR, Dayaram A, Dobson RC, Varsani A. Discovery of a novel circular single-stranded DNA virus from porcine faeces. Arch Virol 2013; 158:283–289 [View Article] [PubMed]
     [Google Scholar]
  61. Krupovic M, Varsani A, Kazlauskas D, Breitbart M, Delwart E et al. Cressdnaviricota: a virus phylum unifying seven families of rep-encoding viruses with single-stranded, circular DNA genomes. J Virol 2020; 94:
     [Google Scholar]
  62. Steel O, Kraberger S, Sikorski A, Young LM, Catchpole RJ et al. Circular replication-associated protein encoding DNA viruses identified in the faecal matter of various animals in New Zealand. Infect Genet Evol 2016; 43:151–164 [View Article] [PubMed]
     [Google Scholar]
  63. Kinsella CM, Bart A, Deijs M, Broekhuizen P, Kaczorowska J et al. Entamoeba and Giardia parasites implicated as hosts of CRESS viruses. Nat Commun 2020; 11:4620 [View Article] [PubMed]
     [Google Scholar]
  64. O’Dea MA, Kabay MJ, Carr J, Wilcox GE, Richards RB. Porcine circovirus-associated disease in weaner pigs in Western Australia. Aust Vet J 2011; 89:122–130 [View Article] [PubMed]
     [Google Scholar]
  65. Biagini P. Human circoviruses. Vet Microbiol 2004; 98:95–101 [View Article] [PubMed]
     [Google Scholar]
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Comparison of gut viral communities in diarrhoea and healthy dairy calves
J. Gen. Virol. 102, 001663 (2021); https://doi.org/10.1099/jgv.0.001663
/content/journal/jgv/10.1099/jgv.0.001663
/content/journal/jgv/10.1099/jgv.0.001663
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