Skip to main content

Advertisement

SpringerLink
Log in

Swine virome on rural backyard farms in Mexico: communities with different abundances of animal viruses and phages

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

    We’re sorry, something doesn't seem to be working properly.

    Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Abstract

Domestic swine have been introduced by humans into a wide diversity of environments and have been bred in different production systems. This has resulted in an increased risk for the occurrence and spread of diseases. Although viromes of swine in intensive farms have been described, little is known about the virus communities in backyard production systems around the world. The aim of this study was to describe the viral diversity of 23 healthy domestic swine maintained in rural backyards in Morelos, Mexico, through collection and analysis of nasal and rectal samples. Next-generation sequencing was used to identify viruses that are present in swine. Through homology search and bioinformatic analysis of reads and their assemblies, we found that rural backyard swine have a high degree of viral diversity, different from those reported in intensive production systems or under experimental conditions. There was a higher frequency of bacteriophages and lower diversity of animal viruses than reported previously. In addition, sapoviruses, bocaparvoviruses, and mamastroviruses that had not been reported previously in our country were identified. These findings were correlated with the health status of animals, their social interactions, and the breeding/rearing environment (which differed from intensive systems), providing baseline information about viral communities in backyard swine.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Availability of data and material

Sequences are available in GenBank with accession numbers MH490914, MH490915, MH490916, MH490912, MH490913, MH490911 and MH479904.

References

  1. Lambin EF, Turner BL, Geist HJ et al (2001) The causes of land-use and land-cover change : moving beyond the myths. Glob Environ Chang 11:261–269. https://doi.org/10.1016/S0959-3780(01)00007-3

    Article  Google Scholar 

  2. Patz JA, Daszak P, Tabor GM et al (2004) Unhealthy landscapes: policy recommendations on land use change and infectious disease emergence. Environ Health Perspect 112:1092–1098. https://doi.org/10.1289/EHP.6877

    Article  PubMed  PubMed Central  Google Scholar 

  3. Cohen ML (1998) Resurgent and emergent disease in a changing world. Br Med Bull 54:523–532. https://doi.org/10.1093/oxfordjournals.bmb.a011707

    Article  CAS  PubMed  Google Scholar 

  4. Schultz-Cherry S, Olsen CW, Easterday BC (2011) History of Swine Influenza. In: Current topics in microbiology and immunology. Curr Top Microbiol Immunol, pp 21–27

  5. Smith I, Wang LF (2013) Bats and their virome: an important source of emerging viruses capable of infecting humans. Curr Opin Virol 3:84–91. https://doi.org/10.1016/j.coviro.2012.11.006

    Article  PubMed  Google Scholar 

  6. Philbey AW, Kirkland PD, Ross AD et al (1998) An apparently new virus (family Paramyxoviridae) infectious for pigs, humans, and fruit bats. Emerg Infect Dis 4:269–271. https://doi.org/10.3201/eid0402.980214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Bowden TR, Westenberg M, Wang LF et al (2001) Molecular characterization of menangle virus, a novel paramyxovirus which infects pigs, fruit bats, and humans. Virology 283:358–373. https://doi.org/10.1006/viro.2001.0893

    Article  CAS  PubMed  Google Scholar 

  8. Wang LF, Hansson E, Yu M et al (2007) Full-length genome sequence and genetic relationship of two paramyxoviruses isolated from bat and pigs in the Americas. Arch Virol 152:1259–1271. https://doi.org/10.1007/s00705-007-0959-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Cuevas-Romero JS, Blomstrom AL, Berg M (2015) Molecular and epidemiological studies of Porcine rubulavirus infection—an overview. Infect Ecol Epidemiol 5:1–8. https://doi.org/10.3402/iee.v5.29602\r29602[pii]

    Article  Google Scholar 

  10. Yaiw KC, Crameri G, Wang L et al (2007) Serological evidence of possible human infection with tioman virus, a newly described paramyxovirus of bat origin. J Infect Dis 196:884–886. https://doi.org/10.1086/520817

    Article  PubMed  Google Scholar 

  11. Yaiw KC, Bingham J, Crameri G et al (2008) Tioman virus, a paramyxovirus of bat origin, causes mild disease in pigs and has a predilection for lymphoid tissues. J Virol 82:565–568. https://doi.org/10.1128/JVI.01660-07

    Article  CAS  PubMed  Google Scholar 

  12. Hause BM, Duff JW, Scheldt A, Anderson G (2016) Virus detection using metagenomic sequencing of swine nasal and rectal swabs. J Swine Heal Prod 24:304–308

    Google Scholar 

  13. Sachsenröder J, Twardziok S, Hammerl JA et al (2012) Simultaneous identification of DNA and RNA viruses present in pig faeces using process-controlled deep sequencing. PLoS One. https://doi.org/10.1371/journal.pone.0034631

    Article  PubMed  PubMed Central  Google Scholar 

  14. Shan T, Li L, Simmonds P et al (2011) The fecal virome of pigs on a high-density farm. J Virol 85:11697–11708. https://doi.org/10.1128/JVI.05217-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Lager KM, Ng TF, Bayles DO et al (2012) Diversity of viruses detected by deep sequencing in pigs from a common background. J Vet Diagn Investig 24:1177–1179. https://doi.org/10.1177/1040638712463212

    Article  Google Scholar 

  16. Gallardo Nieto JL, Villamar Angula L, Barrera Wadgymar MA (2006) Situación actual y perspectiva de la producción de carne de porcino en México 2006

  17. Wiethoelter AK, Beltrán-Alcrudo D, Kock R, Mor SM (2015) Global trends in infectious diseases at the wildlife–livestock interface. Proc Natl Acad Sci 112:9662–9667. https://doi.org/10.1073/pnas.1422741112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. CEA (2014) Programa estatal hídrico de Morelos 2014 - 2018. 110

  19. INEGI IN de EG e I (2016) Mapa Digital de México. http://gaia.inegi.org.mx/mdm6/?v=bGF0OjE4LjYyNDAwLGxvbjotOTkuMDQ3Mjgsejo2LGw6YzQwN3xjNDE3fGMxMDJ8YzEwMHxjMzUw&layers=c401,c404,c407,c410,c417,c418. Accessed 21 Jun 2018

  20. Djikeng A, Halpin R, Kuzmickas R et al (2008) Viral genome sequencing by random priming methods. BMC Genomics 9:5. https://doi.org/10.1186/1471-2164-9-5

    Article  CAS  Google Scholar 

  21. Afgan E, Baker D, Batut B et al (2018) The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update. Nucleic Acids Res 46:W537–W544. https://doi.org/10.1093/nar/gky379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Zerbino DR (2011) Using the Velvet de novo assembler for short-read seqeuncig technologies. Curr Protoc Bioinform. https://doi.org/10.1002/0471250953.bi1105s31.Using

    Article  Google Scholar 

  23. Zerbino DR, Birney E (2008) Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829. https://doi.org/10.1101/gr.074492.107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Kumar S, Stecher G, Li M et al (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454

    Article  CAS  PubMed  Google Scholar 

  26. Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci 101:11030–11035. https://doi.org/10.1073/pnas.0404206101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Hsieh TC, Ma KH, Chao A (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol Evol 7:1451–1456. https://doi.org/10.1111/2041-210X.12613

    Article  Google Scholar 

  28. Chao A, Ma KH, Hsieh TC (2016) iNEXT (iNterpolation and EXTrapolation) Online. Program and User’s Guide published at http://chao.stat.nthu.edu.tw/wordpress/software_download/.30043:1–14. https://doi.org/10.13140/RG.2.2.25777.79200. Accessed 6 July 2018

  29. SAGARPA (2011) ACUERDO mediante el cual se dan a conocer en los Estados Unidos Mexicanos las enfermedades y plagas exóticas y endémicas de notificación obligatoria de los animales terrestres y acuáticos. D Of la Fed 38:38–85

    Google Scholar 

  30. Sachsenröder J, Twardziok SO, Scheuch M, Johne R (2014) The general composition of the faecal virome of pigs depends on age, but not on feeding with a probiotic bacterium. PLoS One 9:15–22. https://doi.org/10.1371/journal.pone.0088888

    Article  CAS  Google Scholar 

  31. Zhang B, Tang C, Yue H et al (2014) Viral metagenomics analysis demonstrates the diversity of viral flora in piglet diarrhoeic faeces in China. J Gen Virol 95:1603–1611. https://doi.org/10.1099/vir.0.063743-0

    Article  CAS  PubMed  Google Scholar 

  32. Wang D (2020) 5 challenges in understanding the role of the virome in health and disease. PLoS Pathog 16:e1008318. https://doi.org/10.1371/journal.ppat.1008318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Biggs PM (1985) Infectious animal disease and its control. Philos Trans R Soc Lond B Biol Sci 310:259–274

    Article  CAS  PubMed  Google Scholar 

  34. Tung J, Barreiro LB, Burns MB et al (2015) Social networks predict gut microbiome composition in wild baboons. Elife 2015:1–18. https://doi.org/10.7554/eLife.05224

    Article  Google Scholar 

  35. Amimo JO, El Zowalaty ME, Githae D et al (2016) Metagenomic analysis demonstrates the diversity of the fecal virome in asymptomatic pigs in East Africa. Arch Virol 161:887–897. https://doi.org/10.1007/s00705-016-2819-6

    Article  CAS  PubMed  Google Scholar 

  36. Colbère-Garapin F, Martin-Latil S, Blondel B et al (2007) Prevention and treatment of enteric viral infections: possible benefits of probiotic bacteria. Microbes Infect 9:1623–1631. https://doi.org/10.1016/j.micinf.2007.09.016

    Article  CAS  PubMed  Google Scholar 

  37. Modi SR, Lee HH, Spina CS, Collins JJ (2013) Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome. Nature 499:219–222. https://doi.org/10.1038/nature12212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Ogilvie LA, Bowler LD, Caplin J et al (2013) Genome signature-based dissection of human gut metagenomes to extract subliminal viral sequences. Nat Commun 4:2420. https://doi.org/10.1038/ncomms3420

    Article  CAS  PubMed  Google Scholar 

  39. Chiappetta CM, Cibulski SP, Lima FES et al (2017) Molecular detection of circovirus and adenovirus in feces of fur seals (Arctocephalus spp.). EcoHealth 14:69–77. https://doi.org/10.1007/s10393-016-1195-8

    Article  PubMed  Google Scholar 

  40. Oba M, Katayama Y, Naoi Y et al (2017) Discovery of fur seal feces-associated circular DNA virus in swine feces in Japan. J Vet Med Sci 79:1664–1666. https://doi.org/10.1292/jvms.16-0642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Breitbart M, Delwart E, Rosario K et al (2017) ICTV virus taxonomy profile: circoviridae. J Gen Virol 98:1997–1998. https://doi.org/10.1099/jgv.0.000871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Ge X, Li J, Peng C et al (2011) Genetic diversity of novel circular ssDNA viruses in bats in China. J Gen Virol 92:2646–2653. https://doi.org/10.1099/vir.0.034108-0

    Article  CAS  PubMed  Google Scholar 

  43. Wang H, Li S, Mahmood A et al (2018) Plasma virome of cattle from forest region revealed diverse small circular ssDNA viral genomes. Virol J 15:11. https://doi.org/10.1186/s12985-018-0923-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Li L, Kapoor A, Slikas B et al (2010) Multiple diverse circoviruses infect farm animals and are commonly found in human and chimpanzee feces. J Virol 84:1674–1682. https://doi.org/10.1128/JVI.02109-09

    Article  CAS  PubMed  Google Scholar 

  45. Chiba S, Sakuma Y, Kogasaka R et al (1979) An outbreak of gastroenteritis associated with calicivirus in an infant home. J Med Virol 4:249–254

    Article  CAS  PubMed  Google Scholar 

  46. Reuter G, Zimsek-Mijovski J, Poljsak-Prijatelj M et al (2010) Incidence, diversity, and molecular epidemiology of sapoviruses in swine across Europe. J Clin Microbiol 48:363–368. https://doi.org/10.1128/JCM.01279-09

    Article  CAS  PubMed  Google Scholar 

  47. Green KY, Ando T, Balayan MS et al (2000) Taxonomy of the caliciviruses. J Infect Dis 181(Suppl):S322–S330. https://doi.org/10.1086/315591

    Article  PubMed  Google Scholar 

  48. Scheuer KA, Oka T, Hoet AE et al (2013) Prevalence of porcine Noroviruses, molecular characterization of emerging porcine sapoviruses from finisher swine in the United States, and unified classification scheme for sapoviruses. J Clin Microbiol 51:2344–2353. https://doi.org/10.1128/JCM.00865-13

    Article  PubMed  PubMed Central  Google Scholar 

  49. Wang QH, Han MG, Funk JA et al (2005) Genetic diversity and recombination of porcine sapoviruses. J Clin Microbiol 43:5963–5972. https://doi.org/10.1128/JCM.43.12.5963-5972.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Martella V, Lorusso E, Banyai K et al (2008) Identification of a porcine calicivirus related genetically to human sapoviruses. J Clin Microbiol 46:1907–1913. https://doi.org/10.1128/JCM.00341-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Zhou F, Sun H, Wang Y (2014) Porcine bocavirus: Achievements in the past five years. Viruses 6:4946–4960. https://doi.org/10.3390/v6124946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Luo Z, Roi S, Dastor M et al (2011) Multiple novel and prevalent astroviruses in pigs. Vet Microbiol 149:316–323. https://doi.org/10.1016/j.vetmic.2010.11.026

    Article  PubMed  Google Scholar 

  53. Blomström A-L, Widén F, Hammer A-S et al (2010) Detection of a novel astrovirus in brain tissue of mink suffering from shaking mink syndrome by use of viral metagenomics. J Clin Microbiol 48:4392–4396. https://doi.org/10.1128/JCM.01040-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Quan P-L, Wagner TA, Briese T et al (2010) Astrovirus ENCEPHALITIS IN BOY WITH X-LINKED AGAMMAGLOBULINEMIA. Emerg Infect Dis 16:918–925. https://doi.org/10.3201/eid1606.091536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Hause BM, Padmanabhan A, Pedersen K, Gidlewski T (2016) Feral swine virome is dominated by single-stranded DNA viruses and contains a novel Orthopneumovirus which circulates both in feral and domestic swine. J Gen Virol 97:2090–2095. https://doi.org/10.1099/jgv.0.000554

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Omar Ríos Bello, Omar Maldonado Pineda, José López Reyeros, Julio José Barrón Rodríguez, and Francisco A. Rosas Rodríguez for their help in field work. We also thank Carlos Cabello and José Eduardo Márquez García for their support during the sequencing work at the INER, and Jairo Betancourt for his help in translation of this text.

Funding

This work was supported by the National Institute of Research in Forestry, Agriculture and Livestock (INIFAP) and the Mexican Council for Science and Technology (CONACyT) [scholarship 219623].

Author information

Authors and Affiliations

  1. Laboratorio de Biotecnología en Salud Animal, Centro Nacional de Investigación Disciplinaria en Microbiología Animal (CENID-Microbiología), Instituto Nacional de Investigaciones Forestales Agrícolas y Pecuarias (INIFAP), carretera federal México-Toluca km 15.5, colonia palo Alto, Cuajimalpa, P.C. 05110, Mexico City, Mexico

    Rodrigo Jesús Barrón-Rodríguez, Edith Rojas-Anaya & Elizabeth Loza-Rubio

  2. Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de México (UNAM), Avenida Universidad 3000, colonia Ciudad universitaria, Coyoacán, P.C. 04510, Mexico City, Mexico

    Rodrigo Jesús Barrón-Rodríguez & Gary García-Espinosa

  3. Idix S.A. de C.V., Sonterra 3035 interior 26, Fraccionamiento Sonterra, P.C. 76230, Santiago de Querétaro, Querétaro, Mexico

    Jorge Tonatiuh Ayala-Sumuano

  4. Laboratorio de Virología, Instituto Nacional de Enfermedades Respiratorias (INER), Calzada de Tlalpan 4502, Del. Tlalpan, colonia Sección XVI, Tlalpan, P.C. 14080, Mexico City, Mexico

    José Ángel Iván Romero-Espinosa & Joel Armando Vázquez-Pérez

  5. Centro Nacional de Recursoso Genéticos (CNRG), Instituto Nacional de Investigaciones Forestales Agrícolas y Pecuarias (INIFAP), Boulevard de la biodiversidad 400, Rancho las Cruces, P.C. 47600, Tepatitlán de Morelos, Jalisco, Mexico

    Moisés Cortés-Cruz

Authors
  1. Rodrigo Jesús Barrón-Rodríguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Edith Rojas-Anaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jorge Tonatiuh Ayala-Sumuano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. José Ángel Iván Romero-Espinosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Joel Armando Vázquez-Pérez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Moisés Cortés-Cruz
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gary García-Espinosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Elizabeth Loza-Rubio
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceived by Rodrigo J. Barrón-Rodríguez and Elizabeht Loza-Rubio. Performed research: Rodrigo J. Barrón-Rodríguez, Edith Rojas-Anaya, José A.I. Romero-Espinosa, Joel A. Vázquez-Pérez and Moisés Cortés-Cruz. Analyzed the data: Rodrigo J. Barrón-Rodríguez, Jorge T. Ayala-Sumuano, Gary García-Espinosa. Wrote the paper: Rodrigo J. Barrón-Rodríguez, Elizabeth Loza-Rubio, Moisés Cortés-Cruz and Gary García-Espinosa.

Corresponding author

Correspondence to Elizabeth Loza-Rubio.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval

The care, handling and sampling of animals for this study were conducted in accordance with the guidelines issued by the Secretary of Agriculture and Rural Development (Spanish acronym, SADER). The experiment was approved by the Institutional Committee for Care and Use of Experimental Animals (Spanish acronym, CICUAE) of the Faculty of Veterinary Medicine and Animal Science at the Universidad Nacional Autónoma de México (UNAM) by protocol DC-2016/2-2.

Code availability

Available upon request from the authors.

Additional information

Handling Editor: Ana Cristina Bratanich.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Barrón-Rodríguez, R.J., Rojas-Anaya, E., Ayala-Sumuano, J.T. et al. Swine virome on rural backyard farms in Mexico: communities with different abundances of animal viruses and phages. Arch Virol 166, 475–489 (2021). https://doi.org/10.1007/s00705-020-04894-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-020-04894-y

Search

Navigation