Skip to main content

Porcine Epidemic Diarrhea Virus Infection Induced the Unbalance of Gut Microbiota in Piglets

Current Microbiology volume 71, pages 643–649 (2015)Cite this article

Abstract

Porcine epidemic diarrhea (PED) is a devastating disease in livestock industry. Most of the previous studies related to the PED were focused on the pathology and etiology of porcine epidemic diarrhea virus (PEDV). A little was known regarding the status of gut microbiota after piglets infected by PEDV. In this study, aided by metagenome sequencing technology, gut microbiota profiles in feces of viral diarrhea (VD) and viral control (VC) piglets were investigated. The results showed that the abundance of four dominant phyla (Fusobacteria, Actinobacteria, Verrucomicrobia, and Proteobacteria) in feces was affected greatly by porcine epidemic diarrhea. Especially, the abundance of Fusobacteria was higher in VD piglets (36 %) than in VC piglets (5 %). On the contrary, the Verrucomicrobia was detected in lower distribution proportion in VD piglets (around 0 %) than in VC piglets (20 %). Furthermore, 25 genera were significantly different between VC and VD piglets at the genus level. Among the 25 genera, Leptotrichia belonging to Fusobacteria was remarkably lower in VC piglets than in VD piglets. Akkermansia belonging to Verrucomicrobia was higher in VC piglets than in VD piglets. Our findings implicated that the gut microbiota associated with PED significantly provided an insight into the pathology and physiology of PED.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y, Cheng GH, Yamasaki S, Saito T, Ohba Y, Taniguchi T, Takeda K, Hori S, Ivanov II, Umesaki Y, Itoh K, Honda K (2011) Induction of colonic regulatory T cells by indigenous clostridium species. Science 331(6015):337–341. doi:10.1126/science.1198469

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  2. Candela M, Perna F, Carnevali P, Vitali B, Ciati R, Gionchetti P, Rizzello F, Campieri M, Brigidi P (2008) Interaction of probiotic Lactobacillus and Bifidobacterium strains with human intestinal epithelial cells: adhesion properties, competition against enteropathogens and modulation of IL-8 production. Int J Food Microbiol 125(3):286–292. doi:10.1016/j.ijfoodmicro.2008.04.012

    CAS  Article  PubMed  Google Scholar 

  3. Cani PD, Geurts L, Matamoros S, Plovier H, Duparc T (2014) Glucose metabolism: focus on gut microbiota, the endocannabinoid system and beyond. Diabetes Metab 40(4):246–257. doi:10.1016/j.diabet.2014.02.004

    CAS  Article  PubMed  Google Scholar 

  4. Fernandez MF, Boris S, Barbes C (2003) Probiotic properties of human lactobacilli strains to be used in the gastrointestinal tract. J Appl Microbiol 94(3):449–455. doi:10.1046/j.1365-2672.2003.01850.x

    CAS  Article  PubMed  Google Scholar 

  5. Gordon JI, Hooper LV, McNevin MS, Wong M, Bry L (1997) Epithelial cell growth and differentiation. 3. Promoting diversity in the intestine: conversations between the microflora, epithelium, and diffuse GALT. Am J Physiol 273(3):565–570

    Google Scholar 

  6. Goto M, Hitomi S, Ishii T (2007) Bacterial arthritis caused by Leptotrichia amnionii. J Clin Microbiol 45(6):2082–2083. doi:10.1128/jcm.02441-06

    PubMed Central  Article  PubMed  Google Scholar 

  7. Hagland HR, Soreide K (2015) Cellular metabolism in colorectal carcinogenesis: influence of lifestyle, gut microbiome and metabolic pathways. Cancer Lett 356(2):273–280. doi:10.1016/j.canlet.2014.02.026

    CAS  Article  PubMed  Google Scholar 

  8. Han YPW, Fardini Y, Chen C, Iacampo KG, Peraino VA, Shamonki JM, Redline RW (2010) Term stillbirth caused by oral Fusobacterium nucleatum. Obstet Gynecol 115(2):442–445

    PubMed Central  Article  PubMed  Google Scholar 

  9. Han YW, Shen T, Chung P, Buhimschi IA, Buhimschi CS (2009) Uncultivated bacteria as etiologic agents of intra-amniotic inflammation leading to preterm birth. J Clin Microbiol 47(1):38–47. doi:10.1128/jcm.01206-08

    PubMed Central  Article  PubMed  Google Scholar 

  10. Jimenez E, Sanchez B, Farina A, Margolles A, Rodriguez JM (2014) Characterization of the bile and gall bladder microbiota of healthy pigs. Microbiologyopen 3(6):937–949. doi:10.1002/mbo3.218

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  11. Kostic AD, Chun EY, Robertson L, Glickman JN, Gallini CA, Michaud M, Clancy TE, Chung DC, Lochhead P, Hold GL, El-Omar EM, Brenner D, Fuchs CS, Meyerson M, Garrett WS (2013) Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe 14(2):207–215. doi:10.1016/j.chom.2013.07.007

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  12. Langfeldt D, Neulinger SC, Stiesch M, Stumpp N, Bang C, Schmitz RA, Eberhard J (2014) Health- and disease-associated species clusters in complex natural biofilms determine the innate immune response in oral epithelial cells during biofilm maturation. FEMS Microbiol Lett 360(2):137–143. doi:10.1111/1574-6968.12596

    CAS  Article  PubMed  Google Scholar 

  13. Levesque CL, Hooda S, Swanson KS, de Lange K (2014) Alterations in ileal mucosa bacteria related to diet complexity and growth performance in young pigs. PLoS One 9(9):e108472. doi:10.1371/journal.pone.0108472

    PubMed Central  Article  PubMed  Google Scholar 

  14. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R, Gordon JI (2008) Evolution of mammals and their gut microbes. Sci 320(5883):1647–1651. doi:10.1126/science.1155725

    CAS  Article  Google Scholar 

  15. Mole B (2013) Deadly pig virus slips through US borders. Nature 499(7459):388

    CAS  Article  PubMed  Google Scholar 

  16. Olszak T, An DD, Zeissig S, Vera MP, Richter J, Franke A, Glickman JN, Siebert R, Baron RM, Kasper DL, Blumberg RS (2012) Microbial exposure during early life has persistent effects on natural killer t cell function. Sci 336(6080):489–493. doi:10.1126/science.1219328

    CAS  Article  Google Scholar 

  17. Pensaert M, Callebaut P, DeBouck P (1982) Porcine epidemic diarrhea (PED) caused by a coronavirus. Present knowledge. Proc Congr Int Pig Vet Soc 7:52

    Google Scholar 

  18. Rist VTS, Eklund M, Bauer E, Sauer N, Mosenthin R (2012) Effect of feeding level on the composition of the intestinal microbiota in weaned piglets. J Anim Sci 90:19–21. doi:10.2527/jas52642

    Article  PubMed  Google Scholar 

  19. Rubinstein MR, Wang XW, Liu WD, Hao YJ, Cai GF, Han YPW (2013) Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/beta-catenin signaling via its FadA adhesin. Cell Host Microbe 14(2):195–206. doi:10.1016/j.chom.2013.07.012

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  20. Scher JU, Ubeda C, Artacho A, Attur M, Isaac S, Reddy SM, Marmon S, Neimann A, Brusca S, Patel T, Manasson J, Pamer EG, Littman DR, Abramson SB (2015) Decreased bacterial diversity characterizes the altered gut microbiota in patients with psoriatic arthritis, resembling dysbiosis in inflammatory bowel disease. Arthritis Rheumatol 67(1):128–139. doi:10.1002/art.38892

    CAS  Article  PubMed  Google Scholar 

  21. Shin NR, Lee JC, Lee HY, Kim MS, Whon TW, Lee MS, Bae JW (2014) An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice. Gut 63(5):727–735. doi:10.1136/gutjnl-2012-303839

    CAS  Article  PubMed  Google Scholar 

  22. Song D, Park B (2012) Porcine epidemic diarrhoea virus: a comprehensive review of molecular epidemiology, diagnosis, and vaccines. Virus Genes 44(2):167–175. doi:10.1007/s11262-012-0713-1

    CAS  Article  PubMed  Google Scholar 

  23. Sun RQ, Cai RJ, Chen YQ, Liang PS, Chen DK, Song CX (2012) Outbreak of porcine epidemic diarrhea in suckling piglets, China. Emerg Infect Dis 18(1):161–163. doi:10.3201/eid1801.111259

    PubMed Central  Article  PubMed  Google Scholar 

  24. Swidsinski A, Doerffel Y, Loening-Baucke V, Theissig F, Rueckert JC, Ismail M, Rau WA, Gaschler D, Weizenegger M, Kuehn S, Schilling J, Doerffel WV (2011) Acute appendicitis is characterised by local invasion with Fusobacterium nucleatum/necrophorum. Gut 60(1):34–40. doi:10.1136/gut.2009.191320

    Article  PubMed  Google Scholar 

  25. Thilesen CM, Nicolaidis M, Lökebo JE, Falsen E (2007) Leptotrichia amnionii, an emerging pathogen of the female urogenital tract. J Clin Microbiol 45(7):2344–2347

    PubMed Central  Article  PubMed  Google Scholar 

  26. Yoneda S, Loeser B, Feng J, Dmytryk J, Qi F, Merritt J (2014) Ubiquitous sialometabolism present among oral fusobacteria. PLoS One 9(6):e99263. doi:10.1371/journal.pone.0099263

    PubMed Central  Article  PubMed  Google Scholar 

  27. Zhao W, Wang Y, Liu S, Huang J, Zhai Z, He C, Ding J, Wang J, Wang H, Fan W, Zhao J, Meng H (2015) The dynamic distribution of porcine microbiota across different ages and gastrointestinal tract segments. PLoS One 10(2):e0117441. doi:10.1371/journal.pone.0117441

    PubMed Central  Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National High Technology Research and Development Program of China (Grant No. 2011AA100901), the National Science Foundation of China (Grant No. 31272430), and Agriculture Development through Science and Technology Key Project of Shanghai (Grant No. 2012,2-3).

Author information

Affiliations

  1. Shanghai Key Laboratory of Veterinary Biotechnology, Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, 800 Dongchuan Road, Shanghai, 200240, People’s Republic of China

    Shuyun Liu, Zhengxiao Zhai, Wenjing Zhao, Jinmei Ding, Ronghua Dai, Tao Sun & He Meng

  2. Shanghai Animal Disease Control Center, Shanghai, 201103, People’s Republic of China

    Lele Zhao

Authors
  1. Shuyun Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lele Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhengxiao Zhai
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wenjing Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jinmei Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ronghua Dai
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tao Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. He Meng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Tao Sun or He Meng.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Liu, S., Zhao, L., Zhai, Z. et al. Porcine Epidemic Diarrhea Virus Infection Induced the Unbalance of Gut Microbiota in Piglets. Curr Microbiol 71, 643–649 (2015). https://doi.org/10.1007/s00284-015-0895-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-015-0895-6

Keywords

  • Appendicitis
  • Proteobacteria
  • Firmicutes
  • Bacteroidetes
  • Porcine Epidemic Diarrhea Virus