Microbial alginate foraging is conserved in geographically and taxonomically distinct ruminant microbiomes

Ferrillo, A.; Tingley, J. P.; King, M. L.; Sagaye, A.; Bajwa, B.; Xing, X.; Johannessen, T.; Lysberg, A.; Mydland, L. T.; Overland, M.; Reintjes, G.; Shearer, A. Y.; Klassen, L.; Low, K. E.; Patel, T. R.; Terry, S.; Pope, P. B.; Abbott, D. W.; Hagen, L. H.

doi:10.1101/2024.12.17.628917

bioRxiv · 10.1101/2024.12.17.628917

Microbial alginate foraging is conserved in geographically and taxonomically distinct ruminant microbiomes

Ferrillo, A.·Tingley, J. P.·King, M. L.·Sagaye, A.·Bajwa, B.·Xing, X.·Johannessen, T.·Lysberg, A.·Mydland, L. T.·Overland, M.·Reintjes, G.·Shearer, A. Y.·Klassen, L.·Low, K. E.·Patel, T. R.·Terry, S.·Pope, P. B.·Abbott, D. W.·Hagen, L. H.

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Abstract

Seaweed plays a crucial role in carbon cycling and is expected to be a valuable resource for sustainable biomass, with applications in biofuel production, human nutrition, and animal feed. Although seaweed has historically been used as a feed source for livestock grazing near coastlines, the process by which it is digested in the rumen remains unknown. Here, we show how the brown algae Saccharina latissima is catabolized in the rumen ecosystem of two different species using in vivo and in vitro experimental systems. We determined that the ruminal decomposition of alginate, a prominent component of the brown algae cell wall, requires microbial catabolic pathways complete with alginate lyases and transport proteins. Evidence of digestion was obtained through a combination of animal models, bacterial imaging, multilayered meta-omics, and enzyme biochemistry. The evolution of and implications for acquisition of alginate utilization loci within geographically and taxonomically distinct ruminants are considered. Graphical abstractSaccharina latissima is a brown alga commonly found in the North Atlantic, Arctic and Pacific oceans. S. latissima was collected from the west coast and Canada and Norway for microbiome studies. Alginate constitutes a substantial portion of the cell wall of S. latissima (SL), and its digestion requires a specific set of enzymes, alginate lyases. We investigated if and how S. latissima is metabolized in geographically distinct rumen ecosystems through in vivo lamb feeding experiments (2.5 and 5% inclusion, DM basis) and in vitro cattle-based rumen simulation technique, RUSITEC, experiments (up to 50% inclusion). Evidence supporting ruminal degradation of alginate was explored using a combination of multilayered meta-omics, physiology (fluorescently labelled S. latissima hot water extracts (FLA-SLAT)) and biochemical characterization of PL6 alginate lyases. O_FIG O_LINKSMALLFIG WIDTH=161 HEIGHT=200 SRC="FIGDIR/small/628917v1_ufig1.gif" ALT="Figure 1"> View larger version (43K): org.highwire.dtl.DTLVardef@eebe40org.highwire.dtl.DTLVardef@c6fb8org.highwire.dtl.DTLVardef@7a9b1borg.highwire.dtl.DTLVardef@15d30d7_HPS_FORMAT_FIGEXP M_FIG C_FIG

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Ferrillo, A., Tingley, J. P., King, M. L., Sagaye, A., Bajwa, B., Xing, X., Johannessen, T., Lysberg, A., Mydland, L. T., Overland, M., Reintjes, G., Shearer, A. Y., Klassen, L., Low, K. E., Patel, T. R., Terry, S., Pope, P. B., Abbott, D. W., Hagen, L. H.. 2024-12-18. Microbial alginate foraging is conserved in geographically and taxonomically distinct ruminant microbiomes. https://doi.org/10.1101/2024.12.17.628917

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