Enrichable consortia of microbial symbionts degrade macroalgal polysaccharides in Kyphosus fish

Oliver, Aaron; Podell, Sheila; Wegley Kelly, Linda; Sparagon, Wesley J.; Plominsky, Alvaro M.; Nelson, Robert S.; Laurens, Lieve M. L.; Augyte, Simona; Sims, Neil A.; Nelson, Craig E.; Allen, Eric E.; Martiny, ed., Jennifer B. H.

doi:10.1128/mbio.00496-24

Enrichable consortia of microbial symbionts degrade macroalgal polysaccharides in Kyphosus fish

Journal Article · Wed May 08 00:00:00 EDT 2024 · mBio (Online)

DOI:https://doi.org/10.1128/mbio.00496-24· OSTI ID:2329343

^[1]; ^[1]; Wegley Kelly, Linda ^[2]; ^[3]; Plominsky, Alvaro M. ^[2]; Nelson, Robert S. ^[4]; Laurens, Lieve M. L. ^[4]; Augyte, Simona ^[5]; Sims, Neil A. ^[5]; Nelson, Craig E. ^[3]; ^[6]; Martiny, ed., Jennifer B. H.

Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California San Diego, La Jolla, California, USA
Marine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, California, USA
Daniel K. Inouye Center for Microbial Oceanography: Research and Education, School of Ocean and Earth Science and Technology, University of Hawai’i at Mānoa, Honolulu, Hawaii, USA
National Renewable Energy Laboratory, Golden, Colorado, USA
Ocean-Era Inc., Kailua-Kona, Hawaii, USA
Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California San Diego, La Jolla, California, USA, Center for Microbiome Innovation, University of California San Diego, La Jolla, California, USA, Department of Molecular Biology, School of Biological Sciences, University of California San Diego, La Jolla, California, USA

ABSTRACT <p> Coastal herbivorous fishes consume macroalgae, which is then degraded by microbes along their digestive tract. However, there is scarce genomic information about the microbiota that perform this degradation. This study explores the potential of <italic>Kyphosus</italic> gastrointestinal microbial symbionts to collaboratively degrade and ferment polysaccharides from red, green, and brown macroalgae through <italic>in silico</italic> study of carbohydrate-active enzyme and sulfatase sequences. Recovery of metagenome-assembled genomes (MAGs) from previously described <italic>Kyphosus</italic> gut metagenomes and newly sequenced bioreactor enrichments reveals differences in enzymatic capabilities between the major microbial taxa in <italic>Kyphosus</italic> guts. The most versatile of the recovered MAGs were from the <italic>Bacteroidota</italic> phylum, whose MAGs house enzyme collections able to decompose a variety of algal polysaccharides. Unique enzymes and predicted degradative capacities of genomes from the <italic>Bacillota</italic> (genus <italic>Vallitalea</italic> ) and <italic>Verrucomicrobiota</italic> (order <italic>Kiritimatiellales</italic> ) highlight the importance of metabolic contributions from multiple phyla to broaden polysaccharide degradation capabilities. Few genomes contain the required enzymes to fully degrade any complex sulfated algal polysaccharide alone. The distribution of suitable enzymes between MAGs originating from different taxa, along with the widespread detection of signal peptides in candidate enzymes, is consistent with cooperative extracellular degradation of these carbohydrates. This study leverages genomic evidence to reveal an untapped diversity at the enzyme and strain level among <italic>Kyphosus</italic> symbionts and their contributions to macroalgae decomposition. Bioreactor enrichments provide a genomic foundation for degradative and fermentative processes central to translating the knowledge gained from this system to the aquaculture and bioenergy sectors. </p> <sec> <title>IMPORTANCE

Seaweed has long been considered a promising source of sustainable biomass for bioenergy and aquaculture feed, but scalable industrial methods for decomposing terrestrial compounds can struggle to break down seaweed polysaccharides efficiently due to their unique sulfated structures. Fish of the genus Kyphosus feed on seaweed by leveraging gastrointestinal bacteria to degrade algal polysaccharides into simple sugars. This study reconstructs metagenome-assembled genomes for these gastrointestinal bacteria to enhance our understanding of herbivorous fish digestion and fermentation of algal sugars. Investigations at the gene level identify Kyphosus guts as an untapped source of seaweed-degrading enzymes ripe for further characterization. These discoveries set the stage for future work incorporating marine enzymes and microbial communities in the industrial degradation of algal polysaccharides.

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Research Organization:: National Renewable Energy Laboratory (NREL), Golden, CO (United States)

Sponsoring Organization:: National Science Foundation (NSF) , National Institutes of Health (NIH); USDOE Advanced Research Projects Agency - Energy (ARPA-E)

Grant/Contract Number:: AC36-08GO28308

OSTI ID:: 2329343

Alternate ID(s):: OSTI ID: 2344979

Report Number(s):: NREL/JA--2700-89762; e00496-24

Journal Information:: mBio (Online), Journal Name: mBio (Online) Journal Issue: 5 Vol. 15; ISSN 2150-7511

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Herbivorous Fish Microbiome Adaptations to Sulfated Dietary Polysaccharides

Journal Article · Tue May 02 20:00:00 EDT 2023 · Applied and Environmental Microbiology · OSTI ID:1974998

Fine scale transitions of the microbiota and metabolome along the gastrointestinal tract of herbivorous fishes

Journal Article · Sun May 22 20:00:00 EDT 2022 · Animal Microbiome · OSTI ID:1869484

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59 BASIC BIOLOGICAL SCIENCES
60 APPLIED LIFE SCIENCES
Kyphosus
fish gut microbiome
macroalgal polysaccharides
sulfatase

Enrichable consortia of microbial symbionts degrade macroalgal polysaccharides in Kyphosus fish

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