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Main Authors: Plominsky, Alvaro M, Oliver, Aaron, Henriquez-Castillo, Carlos, Podell, Sheila, Minich, Jeremiah J, Augyte, Simona, Lowell-Hawkins, Jennica, Sims, Neil A, Allen, Eric E
Format: Artículo científico
Language:en
Published: bioRxiv : the preprint server for biology 2025
Online Access:https://pubmed.ncbi.nlm.nih.gov/41279255/
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author Plominsky, Alvaro M
Oliver, Aaron
Henriquez-Castillo, Carlos
Podell, Sheila
Minich, Jeremiah J
Augyte, Simona
Lowell-Hawkins, Jennica
Sims, Neil A
Allen, Eric E
author_facet Plominsky, Alvaro M
Oliver, Aaron
Henriquez-Castillo, Carlos
Podell, Sheila
Minich, Jeremiah J
Augyte, Simona
Lowell-Hawkins, Jennica
Sims, Neil A
Allen, Eric E
Plominsky, Alvaro M
Oliver, Aaron
Henriquez-Castillo, Carlos
Podell, Sheila
Minich, Jeremiah J
Augyte, Simona
Lowell-Hawkins, Jennica
Sims, Neil A
Allen, Eric E
collection PubMed - marine biology
contents Detoxifying and depolymerizing microorganisms reveal intertwined guild collaborations in the gut microbiome of a generalist macro-algivorous fish. Plominsky, Alvaro M Oliver, Aaron Henriquez-Castillo, Carlos Podell, Sheila Minich, Jeremiah J Augyte, Simona Lowell-Hawkins, Jennica Sims, Neil A Allen, Eric E The biotransformation of macroalgal biomass represents a major catabolic challenge due to its structurally diverse polysaccharides and inhibitory polyphenols. Unlike terrestrial lignocellulosic substrates, macroalgae polysaccharides contain multiple monomer types, branching patterns, and sulfation states. Additionally, macroalgae polyphenols have been shown to inhibit both microbial growth and their catalytic enzymes. While herbivorous fishes have evolved specialized gut microbiota to process these substrates, the enzymatic pathways remain poorly characterized, with few experimentally validated polysaccharide utilization loci or biochemically defined marine sulfatases, and limited understanding of polyphenol degradation. Here, we developed microcosms, based on the gut microbiome of the generalist macro-algivorous fish , to temporally resolve the activity of the microbial guilds involved in macroalgal polysaccharide and polyphenol transformation. First, parallel cDNA/DNA amplicon sequencing were employed to distinguish the natural active fraction from transient gut microbiome taxa. Four media combinations were able to propagate between 96% to 99% of the active hindgut microbial families, reproducing the cooperative degradation dynamics observed . Metagenomic and metatranscriptomic profiling of these four optimized microcosms served as models to assess the stepwise functional successions occurring in the natural gut microbiome. Early Gammaproteobacteria expressed enzymes linked to polyphenol detoxification and alginate degradation, followed by Bacillota, Bacteroidota, and Verrucomicrobiota guilds targeting more recalcitrant sulfated polysaccharides and polyphenols. Together, these results identified temporal and taxonomic coordination as key features of macroalgal biomass deconstruction, providing an experimentally tractable model for discovering novel carbohydrate-active enzymes and elucidating poorly understood pathways of marine polyphenol degradation.
format Artículo científico
id pubmed_41279255
institution PubMed
language en
publishDate 2025
publisher bioRxiv : the preprint server for biology
record_format pubmed
spellingShingle Detoxifying and depolymerizing microorganisms reveal intertwined guild collaborations in the gut microbiome of a generalist macro-algivorous fish.
Plominsky, Alvaro M
Oliver, Aaron
Henriquez-Castillo, Carlos
Podell, Sheila
Minich, Jeremiah J
Augyte, Simona
Lowell-Hawkins, Jennica
Sims, Neil A
Allen, Eric E
Detoxifying and depolymerizing microorganisms reveal intertwined guild collaborations in the gut microbiome of a generalist macro-algivorous fish. Plominsky, Alvaro M Oliver, Aaron Henriquez-Castillo, Carlos Podell, Sheila Minich, Jeremiah J Augyte, Simona Lowell-Hawkins, Jennica Sims, Neil A Allen, Eric E The biotransformation of macroalgal biomass represents a major catabolic challenge due to its structurally diverse polysaccharides and inhibitory polyphenols. Unlike terrestrial lignocellulosic substrates, macroalgae polysaccharides contain multiple monomer types, branching patterns, and sulfation states. Additionally, macroalgae polyphenols have been shown to inhibit both microbial growth and their catalytic enzymes. While herbivorous fishes have evolved specialized gut microbiota to process these substrates, the enzymatic pathways remain poorly characterized, with few experimentally validated polysaccharide utilization loci or biochemically defined marine sulfatases, and limited understanding of polyphenol degradation. Here, we developed microcosms, based on the gut microbiome of the generalist macro-algivorous fish , to temporally resolve the activity of the microbial guilds involved in macroalgal polysaccharide and polyphenol transformation. First, parallel cDNA/DNA amplicon sequencing were employed to distinguish the natural active fraction from transient gut microbiome taxa. Four media combinations were able to propagate between 96% to 99% of the active hindgut microbial families, reproducing the cooperative degradation dynamics observed . Metagenomic and metatranscriptomic profiling of these four optimized microcosms served as models to assess the stepwise functional successions occurring in the natural gut microbiome. Early Gammaproteobacteria expressed enzymes linked to polyphenol detoxification and alginate degradation, followed by Bacillota, Bacteroidota, and Verrucomicrobiota guilds targeting more recalcitrant sulfated polysaccharides and polyphenols. Together, these results identified temporal and taxonomic coordination as key features of macroalgal biomass deconstruction, providing an experimentally tractable model for discovering novel carbohydrate-active enzymes and elucidating poorly understood pathways of marine polyphenol degradation.
title Detoxifying and depolymerizing microorganisms reveal intertwined guild collaborations in the gut microbiome of a generalist macro-algivorous fish.
url https://pubmed.ncbi.nlm.nih.gov/41279255/