Short-Chain Fatty Acids in the Microbiota–Gut–Brain Axis: Role in Neurodegenerative Disorders and Viral Infections

Majumdar, Atreye; Venkatesh, Indira Priya Siva; Basu, Anirban

doi:10.1021/acschemneuro.2c00803

Cited by 18 publications

(9 citation statements)

References 197 publications

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“…This study describes specific genes encoding SCFA production pathways in the genomes of fish gut microbiota. Microbial fatty acids serve as a key metabolite in gut-brain communication ( 89 ) and are a major source of available carbon for the host ( 90 ). SCFA pathway diversity is unexpectedly low for a system previously shown to contain high SCFA concentrations in vivo ( 16 ).…”

Section: Discussionmentioning

confidence: 99%

Enrichable consortia of microbial symbionts degrade macroalgal polysaccharides in Kyphosus fish

Oliver,

Podell,

Wegley Kelly

et al. 2024

mBio

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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 Kyphosus gastrointestinal microbial symbionts to collaboratively degrade and ferment polysaccharides from red, green, and brown macroalgae through in silico study of carbohydrate-active enzyme and sulfatase sequences. Recovery of metagenome-assembled genomes (MAGs) from previously described Kyphosus gut metagenomes and newly sequenced bioreactor enrichments reveals differences in enzymatic capabilities between the major microbial taxa in Kyphosus guts. The most versatile of the recovered MAGs were from the Bacteroidota phylum, whose MAGs house enzyme collections able to decompose a variety of algal polysaccharides. Unique enzymes and predicted degradative capacities of genomes from the Bacillota (genus Vallitalea ) and Verrucomicrobiota (order Kiritimatiellales ) 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 Kyphosus 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. 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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Section: Discussionmentioning

confidence: 99%

Enrichable consortia of microbial symbionts degrade macroalgal polysaccharides in Kyphosus fish

Oliver,

Podell,

Wegley Kelly

et al. 2024

mBio

View full text Add to dashboard Cite

show abstract

“…This study is the first to describe specific genes encoding SCFA production pathways in the genomes of fish gut microbiota. Microbial fatty acids serve as a key metabolite in gut-brain communication (84) and are a major source of available carbon for the host (85). SCFA pathway diversity is unexpectedly low for a system previously shown to contain high SCFA concentrations in vivo (16).…”

Section: Discussionmentioning

confidence: 99%

Enrichable consortia of microbial symbionts degrade macroalgal polysaccharides inKyphosusfish

Oliver,

Podell,

Kelly

et al. 2023

Preprint

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Coastal herbivorous fishes consume macroalgae, which is then degraded by microbes along their digestive tract. However, there is scarce foundational genomic work on the microbiota that perform this degradation. This study explores the potential ofKyphosusgastrointestinal microbial symbionts to collaboratively degrade and ferment polysaccharides from red, green, and brown macroalgae throughin silicostudy of carbohydrate-active enzyme and sulfatase sequences. Recovery of metagenome-assembled genomes (MAGs) reveals differences in enzymatic capabilities between the major microbial taxa inKyphosusguts. The most versatile of the recovered MAGs were from the Bacteroidota phylum, whose MAGs house enzymes able to decompose a variety of algal polysaccharides. Unique enzymes and predicted degradative capacities of genomes from theBacillota(genusVallitalea) andVerrucomicrobiota(order Kiritimatiellales) suggest the potential for microbial transfer between marine sediment andKyphosusdigestive tracts. 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 amongKyphosussymbionts 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.ImportanceSeaweed 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 genusKyphosusfeed on seaweed by leveraging gastrointestinal bacteria to degrade algal polysaccharides into simple sugars. This study is the first to build genomes for these gastrointestinal bacteria to enhance our understanding of herbivorous fish digestion and fermentation of algal sugars. Investigations at the gene level identifyKyphosusguts 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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“…SCFAs can improve the cognitive function and have neuroprotective and anti-inflammatory properties. Particularly butyrate has been demonstrated to support the cognitive health (Majumdar et al, 2023). The blood-brain barrier; a barrier that keeps the bloodstream and brain apart can be affected by the gutbrain axis (Raimondi et al, 2020).…”

Section: Cognitive Functionmentioning

confidence: 99%

From gut to brain: Deciphering the impact of gut microbiota on neurological health

R.,

M.,

et al. 2024

Novel Research in Microbiology Journal

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The Gut-Brain Axis is a complex and fascinating concept elucidating the two-way communication between gut microbiota and the central nervous system, encompassing diverse mechanisms with profound implications on neurological health. Situated in the gastrointestinal tract, the gut microbiota, a diverse bacterial community, which communicates with the brain through various processes, including neurotransmitter and neuropeptide synthesis, immune system modulation, and involvement of the vagus nerve. These interactions not only impact digestion but also influence emotions, cognition, and behavior. Recent research has revealed the significant influence of gut microbiota on the neurological health, establishing connections between alterations in the gut microbiota composition and the prevailing conditions such as depression and neurodegenerative diseases. This understanding sheds new light on the pathophysiology of neurological disorders, marking the gut-brain axis as an exciting frontier in neuroscience and medicine. The aims of this study were to investigate and elucidate the intricate interplay between the gut microbiota and neurological health, and exploring the mechanisms of communication along the gut-brain axis. As research progresses, the potential for groundbreaking strategies to prevent and treat the neurological disorders becomes increasingly apparent. This comprehensive review delves into the nuanced world of the gutbrain axis, providing insights into the intricate relationship between the gut and the brain. Additionally, this review delves into potential therapeutic implications, exploring the use of probiotics, prebiotics, and dietary interventions to modulate gut microbiota for enhancement of the neurological well-being.

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Short-Chain Fatty Acids in the Microbiota–Gut–Brain Axis: Role in Neurodegenerative Disorders and Viral Infections

Cited by 18 publications

References 197 publications

Enrichable consortia of microbial symbionts degrade macroalgal polysaccharides in Kyphosus fish

Enrichable consortia of microbial symbionts degrade macroalgal polysaccharides in Kyphosus fish

Enrichable consortia of microbial symbionts degrade macroalgal polysaccharides inKyphosusfish

From gut to brain: Deciphering the impact of gut microbiota on neurological health

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