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Microbiota-Directed Fibre Activates Both Targeted and 2 Secondary Metabolic Shifts in the Distal Gut 3 bioRxiv preprint doi: https://doi.org/10.1101/799023; this version posted August 14, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Microbiota-directed fibre activates both targeted and 2 secondary metabolic shifts in the distal gut 3 4 Leszek Michalak1, John Christian Gaby1, Leidy Lagos2, Sabina Leanti La Rosa1, Torgeir R. Hvidsten1, 5 Catherine Tétard-Jones3, William G.T. Willats3, Nicolas Terrapon4,5, Vincent Lombard4,5, Bernard 6 Henrissat4,5,6, Johannes Dröge7, Magnus Ø. Arntzen1, Live Heldal Hagen1, Margareth Øverland2, Phillip 7 B. Pope1,2*, Bjørge Westereng1* 8 9 1 Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, 1432 10 Ås, Norway 11 2 Faculty of Biosciences, Norwegian University of Life Sciences, 1432 Ås, Norway 12 3 School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, UK. 13 4 Centre National de la Recherche Scientifique, Aix-Marseille Université, UMR7257, France 14 5 Institut National de la Recherche Agronomique, USC1048 Architecture et Fonction des 15 Macromolécules Biologiques, Marseille, France 16 6 Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia 17 7 Department for Mathematical Sciences, Chalmers University of Technology, Gothenburg, Sweden 18 19 * Contributed equally 20 Corresponding authors: 21 Bjorge Westereng [email protected] 22 Phillip B. Pope [email protected] 23 John Christian Gaby [email protected] 1 bioRxiv preprint doi: https://doi.org/10.1101/799023; this version posted August 14, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 24 ABSTRACT 25 Beneficial modulation of the gut microbiome has high-impact implications not only in humans, 26 but also in livestock that sustain our current societal needs. In this context, we have tailored an 27 acetylated galactoglucomannan (AcGGM) fibre to match unique enzymatic capabilities of Roseburia 28 and Faecalibacterium species, both renowned butyrate-producing gut commensals. The accuracy of 29 AcGGM was tested within the complex endogenous gut microbiome of pigs, wherein we resolved 355 30 metagenome-assembled genomes together with quantitative metaproteomes. In AcGGM-fed pigs, 31 both target populations differentially expressed AcGGM-specific polysaccharide utilization loci, 32 including novel, mannan-specific esterases that are critical to its deconstruction. However, AcGGM- 33 inclusion also manifested a “butterfly effect”, whereby numerous metabolic changes and 34 interdependent cross-feeding pathways were detected in neighboring non-mannolytic populations 35 that produce short-chain fatty acids. Our findings show that intricate structural features and 36 acetylation patterns of dietary fibre can be customized to specific bacterial populations, with potential 37 to create greater modulatory effects at large. 38 39 MAIN TEXT 40 Microbiota-directed foods (MDFs) have emerged as a strategy to modulate the gut 41 microbiome, as diet has distinct and rapid effects on microbiome composition and function1,2. MDFs 42 by definition are not broadly metabolized, but rather elicit a targeted metabolic response in specific 43 indigenous microbiota that confers benefits to their host. This in itself presents a challenge; as many 44 newly identified MDF target organisms, such as beneficial butyrate-producing (i.e. butyrogenic) 45 Roseburia and Faecalibacterium spp.3,4, have broad metabolic capabilities that are shared with the 46 vast majority of fibre-fermenting microbiota in the gut ecosystem. Nevertheless, recent studies have 47 revealed intimate connections between the enzymatic and mechanistic features of microorganisms 48 and the glycan structures of the fibres they consume5,6, which creates new conceptual MDF targets. 2 bioRxiv preprint doi: https://doi.org/10.1101/799023; this version posted August 14, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 49 This is exemplified by discoveries of sophisticated polysaccharide-degrading apparatuses that enable 50 certain microbiota to consume fibre in a “selfish” manner, whereby complex glycan-structures (such 51 as β-mannans) are cleaved into large oligosaccharides at the cell surface, which are subsequently 52 transported into the cell and depolymerized into monomeric sugars5,7,8. Such a mechanism restricts 53 the release of sugars into the ecosystem for neighboring scavenging populations, thus giving a 54 selective metabolic advantage to the selfish-degrader in the presence of these highly complex glycans. 55 Beta-mannans are present in human and livestock diets, and depending on their plant origins, can 56 be heavily decorated with varying amounts of acetylation that protect the fibre from enzymatic 57 degradation9. We recently demonstrated that the human gut commensal Roseburia intestinalis 58 encodes a mannan-specific polysaccharide utilization locus (PUL), and “selfishly” converts highly 59 complex mannan substrates to butyrate5. Within this mannan PUL, a carbohydrate esterase (CE) family 60 2 (RiCE2) removes 3-O-, and 6-O- acetylations on mannan, whereas a novel CE family 17 (RiCE17) 61 removes the axially oriented 2-O-hydroxyl acetylations9, which are distinctive features found in limited 62 mannan moieties and inaccessible to most of the characterized bacterial esterases present in the gut 63 microbiome. Closer genome examinations have revealed that putative CE2/CE17-containing mannan 64 PULs are in fact prominent within many butyrate-producers including Roseburia spp., 65 Faecalibacterium prausnitzii, Ruminococcus gnavus, Coprococcus eutactus and Butyrivibrio 66 fibrisolvens5,10. It is well known that the metabolic attributes of these populations are highly desirable 67 in the gastrointestinal tract, and that their depletion is implicated in colorectal cancer, Crohn’s disease, 68 inflammatory bowel syndrome, ulcerative colitis, forms of dermatitis and several other diseases11,12. 69 These collective findings thus raised the question: could a custom MDF fibre that was tailored to match 70 these specialized enzymatic capabilities selectively engage butyrate-producers in a complex 71 microbiome ecosystem? 72 2-O-acetylated mannans are found in a limited number of characterized western dietary fibre 73 sources (i.e. tomatoes13 and coffee5), however 2-O-acetylations are present in acetylated 3 bioRxiv preprint doi: https://doi.org/10.1101/799023; this version posted August 14, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 74 galactoglucomannan (AcGGM), which is the main hemicellulose in the secondary cell wall of Norway 75 spruce (Picea abies)14. Here, we have utilized controlled steam explosion (SE), followed by 76 ultrafiltration (UF) fractionation to extract complex AcGGM from spruce wood. Processing conditions 77 were selected to tailor the fibre with a high degree of galactose branching’s and 2-O-, 3-O- and 6-O- 78 acetylations15, which is amenable to inclusion as an MDF in animal feed production. Previously, the 79 MDF concept has matched polysaccharides with Bacteroides-encoded PULs to demonstrate the 80 creation of exclusive metabolic niches1,16. In particular, Shepherd et al engrafted exogenous strains in 81 mice via their rare PUL-encoded enzymatic capabilites16, whereas Patnode et al1 illustrated that 82 bioactive carbohydrates were found to target particular Bacteroides species in a defined consortium 83 of 20 human gut microbial species in gnotobiotic mice. However, what is less understood from MDF 84 studies to date, is (1) can the MDF concept be applied to target indigenous populations within a 85 complex endogenous microbiome, and (2) what are the broader secondary community effects if a 86 targeted population is stimulated, i.e. are new niches created and/or existing ones closed? 87 Here, we tested whether our AcGGM fibre could specifically target beneficial Firmicutes 88 species Roseburia and Faecalibacterium within a “real-world” gut ecosystem that consists of 100- 89 1000’s of different species. To do this, we fed weaned piglets diets containing varying AcGGM levels 90 over a 28-day period that extended from their first meal after sow separation until an adapted, fibre- 91 degrading microbiome was established. Temporal changes in the microbiome were monitored using 92 metagenomics, which phylogenetically and functionally resolved the genomes of indigenous 93 microbiota. Finally, quantitative metaproteomic analysis and carbohydrate microarrays were used to 94 visualize the metabolic and enzymatic responses of the different microbiota to the varying AcGGM 95 exposure. This approach demonstrates how the activity of specific beneficial microbiota can be 96 directly stimulated while simultaneously deciphering the secondary, trophic effects on other 97 populations and metabolic
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