Herbivorous Fish Microbiome Adaptations to Sulfated Dietary Polysaccharides

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

doi:10.1128/aem.02154-22

Title: Herbivorous Fish Microbiome Adaptations to Sulfated Dietary Polysaccharides

Journal Article · 02 May 2023 · Applied and Environmental Microbiology

DOI: https://doi.org/10.1128/aem.02154-22 · OSTI ID:1974998

^[1]; Oliver, Aaron ^[1]; Kelly, Linda Wegley ^[1];

^[2]; Plominsky, Alvaro M. ^[1]; Nelson, Robert S. ^[3];

^[3]; Augyte, Simona ^[4]; Sims, Neil A. ^[4]; Nelson, Craig E. ^[2];

^[1]

Univ. of California, San Diego, La Jolla, CA (United States). Scripps Inst. of Oceanography
Univ. of Hawaii at Manoa, Honolulu, HI (United States)
National Renewable Energy Laboratory (NREL), Golden, CO (United States)
Ocean-Era, Inc., Kailua-Kona, Hawaii (United States)

Marine herbivorous fish that feed primarily on macroalgae, such as those from the genus Kyphosus, are essential for maintaining coral health and abundance on tropical reefs. Here, deep metagenomic sequencing and assembly of gut compartment-specific samples from three sympatric, macroalgivorous Hawaiian kyphosid species have been used to connect host gut microbial taxa with predicted protein functional capacities likely to contribute to efficient macroalgal digestion. Bacterial community compositions, algal dietary sources, and predicted enzyme functionalities were analyzed in parallel for 16 metagenomes spanning the mid- and hindgut digestive regions of wild-caught fishes. Gene colocalization patterns of expanded carbohydrate (CAZy) and sulfatase (SulfAtlas) digestive enzyme families on assembled contigs were used to identify likely polysaccharide utilization locus associations and to visualize potential cooperative networks of extracellularly exported proteins targeting complex sulfated polysaccharides. These insights into the gut microbiota of herbivorous marine fish and their functional capabilities improve our understanding of the enzymes and microorganisms involved in digesting complex macroalgal sulfated polysaccharides.

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

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

Grant/Contract Number:: AC36-08GO28308

OSTI ID:: 1974998

Report Number(s):: NREL/JA-2700-86337; MainId:87110; UUID:ab19d6c9-577f-4da1-ab85-c69aceecfeb0; MainAdminID:69569

Journal Information:: Applied and Environmental Microbiology, Journal Name: Applied and Environmental Microbiology Journal Issue: 5 Vol. 89; ISSN 0099-2240

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Fasta format protein sequences from 391 ruminant gut MAGs Podell, Sheila Zenodo https://doi.org/10.5281/zenodo.6635166	dataset	January 2023
Characterizing the resident, fermentative microbial consortium in the hindgut of the temperate-zone herbivorous fish, Hermosilla azurea (Teleostei: Kyphosidae) Fidopiastis, Pat M.; Bezdek, Daniel J.; Horn, Michael H. Marine Biology, Vol. 148, Issue 3 https://doi.org/10.1007/s00227-005-0106-2	journal	October 2005
SulfAtlas, the sulfatase database: state of the art and new developments Stam, Mark; Lelièvre, Pernelle; Hoebeke, Mark Nucleic Acids Research, Vol. 51, Issue D1 https://doi.org/10.1093/nar/gkac977	journal	November 2022
The Biogeochemistry of Marine Polysaccharides: Sources, Inventories, and Bacterial Drivers of the Carbohydrate Cycle Arnosti, C.; Wietz, M.; Brinkhoff, T. Annual Review of Marine Science, Vol. 13, Issue 1 https://doi.org/10.1146/annurev-marine-032020-012810	journal	January 2021

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