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Lactobacilli Probiotics As a Potential Control for Avian Intestinal Spirochaetosis

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Lactobacilli Probiotics As a Potential Control for Avian Intestinal Spirochaetosis Lactobacilli probiotics as a potential control for avian intestinal spirochaetosis A thesis submitted by Jade Louise Passey Submitted for the degree of Doctor of Philosophy School of Veterinary Medicine University of Surrey October 2018 Copyrightã Jade L Passey 2018 “It always seems impossible until it’s done” -unknown ii Declaration of Originality This thesis and the worK to which it refers are the results of my own efforts. Any ideas, data, images or text resulting from the worK of others (whether published or unpublished) are fully identified as such within the worK and attributed to their originator in the text, bibliography or in footnotes. This thesis has not been submitted in whole or in part for any other academic degree or professional Qualification. I agree that the University has the right to submit my worK to the plagiarism detection service TurnitinUK for originality checKs. Whether or not drafts have been so-assessed, the University reserves the right to reQuire an electronic version of the final document (as submitted) for assessment as above. Signed………………………………………….. iii Abstract Brachyspira are the causative agent of avian intestinal spirochaetosis, a gastrointestinal disease common in layer hens and broiler breeders. This disease costs the UK laying industry approximately £18 million per annum, resulting from reduced egg production and poor egg Quality. Prevalence of Brachyspira is increasing, and due to the poor understanding of this pathogen, mitigation strategies have been largely unsuccessful. Therefore, preventative measures are essential. These studies aimed to improve the understanding of Brachyspira pathobiology and investigate Lactobacillus probiotics as a suitable mitigation strategy. Brachyspira and Lactobacillus species were characterised using phenotypic and genotypic methods. Four Lactobacillus isolates were selected for their inhibition of Brachyspira in vitro and demonstrated inhibition by a number of mechanisms. Secreted metabolites in Lactobacillus cell free supernatant inhibited Brachyspira (p value £ 0.05) and metabolomic studies identified the production of organic acids to be a major contributor to inhibition. Protein denaturation in cell free supernatants significantly reduced Brachyspira inhibition (p value £ 0.05), suggesting the role of bacteriocins in inhibition. Furthermore, L. reuteri isolates co-aggregated with Brachyspira in vitro, reducing pathogen viability (p value £ 0.05). Pro-inflammatory responses to Brachyspira in HD11 avian macrophages were dominated by upregulation of IFNg (p value £ 0.01) and pre-treatment of cells with Lactobacillus significantly reduced this response (p value £ 0.0001), demonstrating the ability of probiotics to alter immune responses to Brachyspira. Galleria mellonella were utilised to study Brachyspira virulence and probiotic intervention. G. mellonella exhibited a varied response to Brachyspira iv infection and Lactobacillus isolates were able to protect against the mortality associated with Brachyspira isolates (p value £ 0.05). The studies here demonstrated that Lactobacillus probiotics are a suitable mitigation strategy against Brachyspira. A number of mechanisms were identified, however future studies are reQuired to explore these mechanisms in a more relevant in vivo chicken model. v Acknowledgements Firstly, I would liKe to extend my sincere gratitude to my supervisors Professor Roberto La Ragione, Professor Martin Woodward and Dr Jorge Gutierrez for their continued support and guidance over the last four years. ThanK you also to Dr Arnoud van Vliet who has helped me to overcome my fear of the command line and who’s advice and support with genomics was invaluable. A special thanKs to Duncan Grainger for his help and advice with histology sample preparation. ThanKs also to Dr Chris Palgrave for histological analysis of these samples. ThanK you to the British Egg MarKeting Board Research and Education Trust for funding this project and for all of the positive feedbacK over the last four years. A special thanKs to Ali Bone, her positivity always put a smile on my face and to Jeff Vergerson who has facilitated a number of trips to laying farms over the country which were an important insight into the industry. I am also extremely grateful for the help and guidance from Dr Caroline Le Roy who taught me everything I now Know about metabolomics and analysis NMR data. ThanKs also to Dr Jon Swann at Imperial College London for use of the NMR facilities. I’d liKe to extend my thanKs to Professor David Hampson and his research group, including Tom La and Nyree Phillips, the sharing of Brachyspira isolates made it possible initiate collaborations and improve my genomics studies. An enormous thanK you to all of the incredible people I have met throughout my PhD. A special thanKs to Dr Jai Mehat, Lucy Rhys-Davies and Dr BecKy ClarKe, their unwavering friendship and support got me through some of the toughest days! ThanK you also to the rest vi of my research group: Dr Jono Betts, Dr MoniKa TchorzewsKa, Dr Joy Leng, Dr MiKe Hornsey and Dr Susan McNally for their positivity and advice over the years. Finally, the last four years would not have been possible without the support of my family. Mum, you have supported me and believed in me when I didn’t believe in myself. You have given me encouragement my whole life and I wouldn’t be the person I am today or have achieved the things I have achieved without you being there every step of the way. Dad, we have faced some difficult times over the last three years, but we made it out the other side with smiles on our faces. Your positivity and sense of humour in the toughest of times is inspiring and you never fail to encourage me and make me smile. Steve, thanK you for your unwavering support for so many years. You’ve always been there to listen to me and offer words of encouragement no matter what. Nan, you’re always there to listen, make me laugh and offer (mostly) sensible advice. Last but by no means least, I would liKe to thanK Gavin, your love, patience and understanding have been second to none and I couldn’t have done my PhD without you by my side. vii Publications, Conference papers and Awards Le Roy, C.I., Passey, J.L., Woodward, M.J., La Ragione, R.M., Claus, S.P. Metabonomics-based analysis of Brachyspira pilosicoli's response to tiamulin reveals metabolic activity despite significant growth inhibition. Anaerobe 45, (2017). Lactobacillus probiotics as a novel control for avian intestinal spirochaetosis International Probiotics and Antimicrobial Proteins conference- First poster prize. Barcelona, Spain 2017. Lactobacillus probiotics as a novel control for avian intestinal spirochaetosis Veterinary Research Council- Oral presentation, Walter and Dorothy Plowright prize runner-up. Surrey, UK 2017. Lactobacillus probiotics as a novel control for avian intestinal spirochaetosis World Poultry Association Congress- Poster presentation. Edinburgh, UK 2017. Lactobacillus probiotics as a novel control for avian intestinal spirochaetosis Microbiology Society annual conference- Poster presentation. Edinburgh, UK 2017. Lactobacillus probiotics as a novel control for avian intestinal spirochaetosis International Spirochaete Conference- Fellstrom poster prize. Hanover, Germany 2016. Lactobacillus probiotics as a novel control for avian intestinal spirochaetosis University of Surrey Festival of Research- First poster prize. Surrey, UK 2016. viii Table of Contents Declaration of Originality ................................................................................................. iii Abstract ........................................................................................................................... iv Acknowledgements .......................................................................................................... vi Publications, Conference papers and Awards .................................................................. viii Table of Contents ............................................................................................................. ix List of Figures .................................................................................................................. xiv List of Tables ................................................................................................................... xvi List of Abbreviations ...................................................................................................... xviii Chapter 1: Introduction ..................................................................................................... 1 1.1 Brachyspira .................................................................................................................... 1 1.1.1 History of Brachyspira Taxonomy .................................................................................................. 1 1.1.2 The genus Brachyspira ................................................................................................................... 2 1.1.3 Phenotypic characteristics of Brachyspira ..................................................................................... 4 1.1.3.1 Cell morphology and cultural characteristics ....................................................................... 4 1.1.3.2 Biochemical properties of Brachyspira ................................................................................. 7 1.1.3.3 Metabolic properties of Brachyspira ...................................................................................
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