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Insect Larvae Meal As a Feed Ingredient for Atlantic Salmon (Salmo Salar): Effects on Intestinal Function, Health, and Microbiota

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Insect Larvae Meal As a Feed Ingredient for Atlantic Salmon (Salmo Salar): Effects on Intestinal Function, Health, and Microbiota Insect larvae meal as a feed ingredient for Atlantic salmon (Salmo salar): Effects on intestinal function, health, and microbiota Mel av insektlarver som ingrediens i fôr til Atlantisk laks (Salmo salar): Effekter på tarmens funksjon, helse og mikrobiota Philosophiae Doctor (PhD) Thesis Yanxian Li Norwegian University of Life Sciences Faculty of Veterinary Medicine Department of Paraclinical Sciences Ås (2021) Thesis number 2021:75 ISSN 1894-6402 ISBN 978-82-575-1851-6 “When you are studying any matter, or considering any philosophy, ask yourself only what are the facts and what is the truth that the facts bear out. Never let yourself be diverted, either by what you wish to believe, or by what you think would have beneficent social effects if it were believed. But look only, and solely, at what are the facts.” —Bertrand Russell TABLE OF CONTENTS Acknowledgements ............................................................................................................................................... 1 List of abbreviations ............................................................................................................................................. 3 Summary ................................................................................................................................................................... 4 Summary in Norwegian (sammendrag) ....................................................................................................... 6 List of papers ........................................................................................................................................................... 8 Introduction ............................................................................................................................................................. 9 General background ...................................................................................................................................... 10 Plant feedstuffs as main ingredients used in Norwegian salmon feeds ............................. 10 Insect larvae meal as an alternative feed ingredient for salmon aquaculture................. 11 Intestinal health problems associated with alternative feed ingredients ......................... 12 The multifunctional intestine ................................................................................................................... 15 Histomorphology ...................................................................................................................................... 15 Digestive function ..................................................................................................................................... 16 Immune function ....................................................................................................................................... 17 Barrier function ......................................................................................................................................... 21 Xenobiotic metabolism ........................................................................................................................... 22 Intestinal microbiota .................................................................................................................................... 23 Microbiota and intestinal health ......................................................................................................... 24 Interplays between intestinal microbiota and diet ..................................................................... 25 Temporal and spatial variation of Atlantic salmon intestinal microbiota ........................ 26 Aims of the study ................................................................................................................................................ 28 Hypotheses ............................................................................................................................................................ 29 Summary of results ............................................................................................................................................ 30 Discussion: materials and methods ............................................................................................................ 34 Materials ............................................................................................................................................................ 34 Methodological considerations for microbiota profiling .............................................................. 34 Experimental design ................................................................................................................................ 34 Sample collection ...................................................................................................................................... 37 DNA extraction ........................................................................................................................................... 38 Amplicon PCR ............................................................................................................................................. 38 Bioinformatics ............................................................................................................................................ 39 Statistics ........................................................................................................................................................ 41 Methodological limitations ................................................................................................................... 43 Discussions: main findings ............................................................................................................................. 46 Insect meal diets do not impair the intestinal health in Atlantic salmon ............................... 46 Insect meal diets ameliorate the intestinal steatosis in Atlantic salmon ................................ 47 Temporal and spatial variations of the Atlantic salmon intestinal microbiota.................... 47 Insect meal diets modulate the Atlantic salmon intestinal microbiota ................................... 49 Main conclusions ................................................................................................................................................ 51 Conclusions on methodology .................................................................................................................... 51 Conclusions on main findings ................................................................................................................... 52 Future perspectives ........................................................................................................................................... 53 References ............................................................................................................................................................. 54 Appendix: papers I-IV ....................................................................................................................................... 78 ACKNOWLEDGEMENTS The work presented in this thesis was performed at the Nutrition and Health Unit, Faculty of Veterinary Medicine, NMBU, from 2015 to 2021. Funding for the studies came from the AquFly project financed by the Research Council of Norway. In addition, I was granted a scholarship from the China Scholarship Council (CSC) to pursue my Ph.D. degree in Norway. Six years in the making. I would not have made it this far without supports from my supervisors, colleagues, friends, and family. I am proud of the knowledge and skills that I have acquired from my Ph.D. training under the supervision of Professor Åshild Krogdahl and Associate Professor Trond Kortner. I am grateful for your mentorship and supports, both in academia and in my personal life. Thank you, Åshild, for the shrimp treat in the summer at Hvitsten and the game meat fest during the Christmas season, both of which were incredible cultural experiences for me. You inspire me to be a better person through your compassion and dedication to science and your sympathy and kindness to people around you. Thank you, Trond, for the casual talks on science and life when we shared the office space. You inspire me to be an independent scientist through your pedagogic style of training on molecular biology. “Know what you are doing” is the best piece of advice I took from you. The lovely and kind colleagues at the Nutrition and Health Unit have certainly made this journey easier and enjoyable for me. Thank you, Karina and Alex, for your training on the microbiota wet-lab works, for the excellent time we spent together optimizing the microbiota workflow, and for the great advice on work-life balance. Thank you, Leonardo, for your friendship and the excellent collaboration on the microbiota work. Thank you, Ellen, the one who knows all at the lab, for your instructions on enzymatic analysis and not the least, for answering various questions that I had on living in Norway. Thank you, Elvis, for your training on histology and the fun chit-chat we had when we shared the office at Adamstuen. Thank you, Anne, for the ski trip to your cabin and the tour guide around Oslo. Thank you, Kirsti, for kindly driving us to collect the bikes and assemble them at your home. Thank you, Sissel, for the kindness
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