Transient and Prolonged Response of Chicken Cecum Mucosa to Colonization with Different Gut Microbiota

Jiri Volf,Lenka Gerzova,Vladimir Babak,Ondrej Polansky,Zuzana Sekelova,Matej Medvecky,Karolina Varmuzova,Bernd Kaspers,Marcela Faldynova,Philippe Velge,Ivan Rychlik,Adrian L Smith

doi:10.1371/journal.pone.0163932

Abstract

In this study we determined protein and gene expression in the caeca of newly hatched chickens inoculated with cecal contents sourced from hens of different ages. Over 250 proteins exhibited modified expression levels in response to microbiota inoculation. The most significant inductions were observed for ISG12-2, OASL, ES1, LYG2, DMBT1-L, CDD, ANGPTL6, B2M, CUZD1, IgM and Ig lambda chain. Of these, ISG12-2, ES1 and both immunoglobulins were expressed at lower levels in germ-free chickens compared to conventional chickens. In contrast, CELA2A, BRT-2, ALDH1A1, ADH1C, AKR1B1L, HEXB, ALDH2, ALDOB, CALB1 and TTR were expressed at lower levels following inoculation of microbiota. When chicks were given microbiota preparations from different age donors, the recipients mounted differential responses to the inoculation which also differed from the response profile in naturally colonised birds. For example, B2M, CUZD1 and CELA2A responded differently to the inoculation with microbiota of 4- or 40-week-old hens. The increased or decreased gene expression could be recorded 6 weeks after the inoculation of newly hatched chickens. To characterise the proteins that may directly interact with the microbiota we characterised chicken proteins that co-purified with the microbiota and identified a range of host proteins including CDD, ANGPTL6, DMBT1-L, MEP1A and Ig lambda. We propose that induction of ISG12-2 results in reduced apoptosis of host cells exposed to the colonizing commensal microbiota and that CDD, ANGPTL6, DMBT1-L, MEP1A and Ig lambda reduce contact of luminal microbiota with the gut epithelium thereby reducing the inflammatory response.

Highlights

Vertebrates are hatched or born with a sterile intestinal tract and colonization is initiated as early as during hatch or delivery
To characterise the proteins that may directly interact with the microbiota we characterised chicken proteins that co-purified with the microbiota and identified a range of host proteins including cytidine deaminase (CDD), angiopoetin related protein 6 (ANGPTL6), deleted in malignant brain tumor 1-like (DMBT1-L), meprin 1A (MEP1A) and Ig lambda
We propose that induction of ISG12-2 results in reduced apoptosis of host cells exposed to the colonizing commensal microbiota and that CDD, ANGPTL6, deleted in malignant brain tumor 1 (DMBT1)-L, MEP1A and Ig lambda reduce contact of luminal microbiota with the gut epithelium thereby reducing the inflammatory response

Summary

Introduction

Vertebrates are hatched or born with a sterile intestinal tract and colonization is initiated as early as during hatch or delivery. The gut microbiota develops further with the most dynamic changes in young animals and lower fluctuations in healthy adults. We recently characterized the life-time microbiota dynamics in egg laying hens [1] identifying an overall pattern of change that, except for a relative lack of Actinobacteria due to the absence of breast feeding in the chickens, resembles other animal species including humans [2,3]. The intestinal tract of any host responds to colonization with natural microbiota. Immunoglobulin production in the intestinal tract is dependent on the presence of microbiota since germ-free animals do not produce antibodies [4,5]. The processes leading to the development of this protective layer during the initial phases of microbial colonization are not known

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Conclusion