Skip to main content
Log in

Alterations in cecal microbiota of Jinhua piglets fostered by a Yorkshire sow

  • Article
  • Animal Genetics
  • Published:
Chinese Science Bulletin

Abstract

Gut microbiota play important roles in host health and diseases. Several factors, in particular antibiotics, affect the gut microbiota of pigs. Cross-fostering has been applied as a regular practice to equalize litter size, reduce pre-weaning mortality and increase body weight. However, the effect of cross-fostering on cecal microbiota is unclear. In this study, we fostered three Jinhua pigs to a Yorkshire sow. The fostered Jinhua piglets grew significantly faster than their biological siblings. To explore whether the cecal microbiota of piglets will alter during fostering, we characterized the cecal microbiota of all piglets by examining the V3 hypervariable region of 16S rDNA. We observed altered cecal microbiota in these piglets using the Illumina HiSeq 2000 platform, and this was accompanied with an increase in growth rate after fostering. The relative abundance of Bacteroidetes in the fostered Jinhua piglets was decreased compared with their biological siblings, although still higher in comparison with their new littermates. Beta-diversity analysis also showed that the cecal microbiota of the adopted Jinhua piglets differed from their biological siblings with a shift toward their step-siblings. Our data show that cecal microbiota of piglets were altered after cross-fostering while the growth rate increased.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Meurens F, Summerfield A, Nauwynck H et al (2012) The pig: a model for human infectious diseases. Trends Microbiol 20:50–57

    Article  Google Scholar 

  2. Hvistendahl M (2012) Pigs as stand-ins for microbiome studies. Science 336:1250

    Article  Google Scholar 

  3. Delgado CL, Courbois C, Rosegrant MW (1998) Global food demand and the contribution of livestock as we enter the new millennium. International Food Policy Research Institute (IFPRI), Washington, DC

  4. Straw BE, Burgi EJ, Dewey CE et al (1998) Effects of extensive crossfostering on performance of pigs on a farm. J Am Vet Med Assoc 212:855–856

    Google Scholar 

  5. Robert S, Martineau G (2001) Effects of repeated cross-fosterings on preweaning behavior and growth performance of piglets and on maternal behavior of sows. J Anim Sci 79:88–93

    Google Scholar 

  6. Rzasa A, Poznanski W, Akincza J et al (2002) The influence of primiparous sow litter standardization on their performance. Ann Anim Sci 2(Suppl):167–172

    Google Scholar 

  7. English PR, Smith WJ, MacLean A (1978) The sow-improving her efficiency. Farming Press, Ipswich

    Google Scholar 

  8. Heim G, Mellagi A, Bierhals T et al (2012) Effects of cross-fostering within 24 h after birth on pre-weaning behaviour, growth performance and survival rate of biological and adopted piglets. Livest Sci 150:121–127

    Article  Google Scholar 

  9. Ley RE, Backhed F, Turnbaugh P et al (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 102:11070–11075

    Article  Google Scholar 

  10. Ley RE, Turnbaugh PJ, Klein S et al (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444:1022–1023

    Article  Google Scholar 

  11. Turnbaugh PJ, Ley RE, Mahowald MA et al (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027–1031

    Article  Google Scholar 

  12. Jumpertz R, Le DS, Turnbaugh PJ et al (2011) Energy-balance studies reveal associations between gut microbes, caloric load, and nutrient absorption in humans. Am J Clin Nutr 94:58–65

    Article  Google Scholar 

  13. Round JL, Mazmanian SK (2009) The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9:313–323

    Article  Google Scholar 

  14. Chung H, Pamp SJ, Hill JA et al (2012) Gut immune maturation depends on colonization with a host-specific microbiota. Cell 149:1578–1593

    Article  Google Scholar 

  15. Diaz Heijtz R, Wang S, Anuar F et al (2011) Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci USA 108:3047–3052

    Article  Google Scholar 

  16. Marques TM, Wall R, Ross RP et al (2010) Programming infant gut microbiota: influence of dietary and environmental factors. Curr Opin Biotechnol 21:149–156

    Article  Google Scholar 

  17. Spor A, Koren O, Ley R (2011) Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol 9:279–290

    Article  Google Scholar 

  18. Lamendella R, Domingo JW, Ghosh S et al (2011) Comparative fecal metagenomics unveils unique functional capacity of the swine gut. BMC Microbiol 11:103

    Article  Google Scholar 

  19. Kim HB, Borewicz K, White BA et al (2011) Longitudinal investigation of the age-related bacterial diversity in the feces of commercial pigs. Vet Microbiol 153:124–133

    Article  Google Scholar 

  20. Looft T, Johnson TA, Allen HK et al (2012) In-feed antibiotic effects on the swine intestinal microbiome. Proc Natl Acad Sci USA 109:1691–1696

    Article  Google Scholar 

  21. Kim HB, Borewicz K, White BA et al (2012) Microbial shifts in the swine distal gut in response to the treatment with antimicrobial growth promoter, tylosin. Proc Natl Acad Sci USA 109:15485–15490

    Article  Google Scholar 

  22. Poole T, Suchodolski J, Callaway T et al (2013) The effect of chlortetracycline on faecal microbial populations in growing swine. J Glob Antimicrob Resist 3:171–174

    Article  Google Scholar 

  23. Rettedal E, Vilain S, Lindblom S et al (2009) Alteration of the ileal microbiota of weanling piglets by the growth-promoting antibiotic chlortetracycline. Appl Environ Microbiol 75:5489–5495

    Article  Google Scholar 

  24. Poroyko V, White JR, Wang M et al (2010) Gut microbial gene expression in mother-fed and formula-fed piglets. PLoS One 5:e12459

    Article  Google Scholar 

  25. Pieper R, Janczyk P, Zeyner A et al (2008) Ecophysiology of the developing total bacterial and lactobacillus communities in the terminal small intestine of weaning piglets. Microb Ecol 56:474–483

    Article  Google Scholar 

  26. Jacobson M, Hård af Segerstad C, Gunnarsson A et al (2003) Diarrhoea in the growing pig—a comparison of clinical, morphological and microbial findings between animals from good and poor performance herds. Res Vet Sci 74:163–169

    Article  Google Scholar 

  27. Miao ZG, Wang LJ, Xu ZR et al (2009) Developmental changes of carcass composition, meat quality and organs in the Jinhua pig and Landrace. Animal 3:468–473

    Article  Google Scholar 

  28. Yang F, Wang Q, Wang M et al (2012) Associations between gene polymorphisms in two crucial metabolic pathways and growth traits in pigs. Chin Sci Bull 57:2733–2740

    Article  Google Scholar 

  29. Huse SM, Dethlefsen L, Huber JA et al (2008) Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genetics 4:e1000255

    Article  Google Scholar 

  30. Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  Google Scholar 

  31. Kozich JJ, Westcott SL, Baxter NT et al (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120

    Article  Google Scholar 

  32. Chao A, Shen T-J (2003) Nonparametric estimation of Shannon’s index of diversity when there are unseen species in sample. Environ Ecol Stat 10:429–443

    Article  Google Scholar 

  33. Segata N, Izard J, Waldron L et al (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60

    Article  Google Scholar 

  34. Zou S, McLaren D, Hurley W (1992) Pig colostrum and milk composition: comparisons between Chinese Meishan and US breeds. Livest Product Sci 30:115–127

    Article  Google Scholar 

  35. Ramanau A, Kluge H, Spilke J et al (2004) Supplementation of sows with L-carnitine during pregnancy and lactation improves growth of the piglets during the suckling period through increased milk production. J Nutr 134:86–92

    Google Scholar 

  36. Averette LA, Odle J, Monaco MH et al (1999) Dietary fat during pregnancy and lactation increases milk fat and insulin-like growth factor I concentrations and improves neonatal growth rates in swine. J Nutr 129:2123–2129

    Google Scholar 

  37. Gill SR, Pop M, Deboy RT et al (2006) Metagenomic analysis of the human distal gut microbiome. Science 312:1355–1359

    Article  Google Scholar 

  38. Backhed F, Ding H, Wang T et al (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 101:15718–15723

    Article  Google Scholar 

  39. Backhed F, Manchester JK, Semenkovich CF et al (2007) Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc Natl Acad Sci USA 104:979–984

    Article  Google Scholar 

  40. Martin FP, Dumas ME, Wang Y et al (2007) A top-down systems biology view of microbiome-mammalian metabolic interactions in a mouse model. Mol Syst Biol 3:112

    Article  Google Scholar 

  41. Dominguez-Bello MG, Costello EK, Contreras M et al (2010) Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA 107:11971–11975

    Article  Google Scholar 

  42. Turnbaugh PJ, Ridaura VK, Faith JJ et al (2009) The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 1:6ra14

    Article  Google Scholar 

  43. Wu GD, Chen J, Hoffmann C et al (2011) Linking long-term dietary patterns with gut microbial enterotypes. Science 334:105–108

    Article  Google Scholar 

  44. Ley RE, Peterson DA, Gordon JI (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124:837–848

    Article  Google Scholar 

  45. Song SJ, Lauber C, Costello EK et al (2013) Cohabiting family members share microbiota with one another and with their dogs. eLife 2:e00458

    Google Scholar 

  46. Thompson CL, Wang B, Holmes AJ (2008) The immediate environment during postnatal development has long-term impact on gut community structure in pigs. ISME J 2:739–748

    Article  Google Scholar 

  47. Zoetendal EG, Akkermans AD, Akkermans-van Vliet WM et al (2001) The host genotype affects the bacterial community in the human gastronintestinal tract. Microb Ecol Health Dis 13:129–134

    Article  Google Scholar 

  48. Martín R, Langa S, Reviriego C et al (2003) Human milk is a source of lactic acid bacteria for the infant gut. J Pediatrics 143:754–758

    Article  Google Scholar 

  49. Jimenez E, Delgado S, Maldonado A et al (2008) Staphylococcus epidermidis: a differential trait of the fecal microbiota of breast-fed infants. BMC Microbiol 8:143

    Article  Google Scholar 

  50. Adlerberth I, Wold AE (2009) Establishment of the gut microbiota in Western infants. Acta Paediatr 98:229–238

    Article  Google Scholar 

  51. O’Toole PW, Claesson MJ (2010) Gut microbiota: changes throughout the lifespan from infancy to elderly. Int Dairy J 20:281–291

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to Pinger Lou and Xiaoli Zhang for assistance with sample collections. We also thank Xingyong Ma for critically reading this manuscript. This work was supported by the National Special Foundation for Transgenic Species of China (2014ZX0800950B, 2011ZX08006-003), the Specialized Research Fund of Ministry of Agriculture of China (NYCYTX-009), the Fund of Fok Ying-Tung Education Foundation (141117), the Fund for Distinguished Young Scientists of Sichuan Province (2013JQ0013), the Program for Changjiang Scholars and Innovative Research Team in University (IRT13083) to Mingzhou Li and Xuewei Li, and the “100-Talent Program” in Sichuan Science Foundation for Youths of Sichuan Province to Ying Li.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Mingzhou Li or Xuewei Li.

Additional information

Lingjin Xian, Ying Li and Zhi Jiang contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

11434_2014_532_MOESM1_ESM.xls

The electronic supplementary material is available online at csb.scichina.com and www.springerlink.com. The supporting materials are published as submitted, without typesetting or editing. The responsibility for scientific accuracy and content remains entirely with the authors (XLS 23 kb)

11434_2014_532_MOESM2_ESM.xls

The electronic supplementary material is available online at csb.scichina.com and www.springerlink.com. The supporting materials are published as submitted, without typesetting or editing. The responsibility for scientific accuracy and content remains entirely with the authors (XLS 26 kb)

11434_2014_532_MOESM3_ESM.xls

The electronic supplementary material is available online at csb.scichina.com and www.springerlink.com. The supporting materials are published as submitted, without typesetting or editing. The responsibility for scientific accuracy and content remains entirely with the authors (XLS 29 kb)

11434_2014_532_MOESM4_ESM.tif

The electronic supplementary material is available online at csb.scichina.com and www.springerlink.com. The supporting materials are published as submitted, without typesetting or editing. The responsibility for scientific accuracy and content remains entirely with the authors (TIFF 2784 kb)

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xian, L., Li, Y., Jiang, Z. et al. Alterations in cecal microbiota of Jinhua piglets fostered by a Yorkshire sow. Chin. Sci. Bull. 59, 4304–4311 (2014). https://doi.org/10.1007/s11434-014-0532-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11434-014-0532-y

Keywords

Navigation