Extensive Transfer of Genes for Edible Seaweed Digestion from Marine to Human Gut Bacteria

Pudlo, Nicholas A.; Pereira, Gabriel Vasconcelos; Parnami, Jaagni; Cid, Melissa; Markert, Stephanie; Tingley, Jeffrey P.; Unfried, Frank; Ali, Ahmed; Campbell, Austin; Urs, Karthik; Xiao, Yao; Adams, Ryan P.; Martin, Duña; Bolam, David N.; Becher, Dörte; Schmidt, Thomas M.; Abbott, D. Wade; Schweder, Thomas; Hehemann, Jan Hendrik; Martens, Eric C.

doi:10.2139/ssrn.3739936

Cited by 4 publications

(6 citation statements)

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“…For example, Kearney et al [ 156 ] demonstrated that reversible engraftment of porphyran-utilising Bacteroides plebeius is possible with the addition of 1% porphyran to the diet of mice. Similar trials by Shepherd et al [ 157 ] and Pudlo et al [ 154 ] found that mammalian gut bacteria could be transferred by gavage to mice and successfully colonise their gut.…”

Section: Discussionsupporting

confidence: 55%

“…It is hypothesised that these utilisation loci were acquired by human gut bacteria via horizontal transfer over thousands of years of seaweed consumption [ 149 , 153 ]. Pudlo et al [ 154 ] surveyed a global culture collection of 354 human and animal gut bacteria and identified marine bacteria-derived genes involved in seaweed polysaccharide catabolism in 22 species of human gut Bacteroides. These genes were present to a significantly greater extent in Japanese and Chinese subjects, where seaweed forms a regular part of the diet, compared to Northern American and European subjects.…”

Section: Discussionmentioning

confidence: 99%

“…A similar geographic distribution was reported by Pluvinage et al [ 155 ] for the presence of genes relating to agarose and porphyran utilisation in human-associated Bacteroides. The study also found that genes involved in laminarin-degrading enzymes (capable of hydrolysing the bonds between β (1,3)-linked glucose units) were most abundant [ 154 ]. This prevalence of genes related to the metabolism of laminarin, more so than porphyran, alginate, and carrageenan, may be due to the fact that structurally similar β -linked glucans occur extensively in many plants and fungi consumed by humans.…”

Section: Discussionmentioning

confidence: 99%

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The Prebiotic Effect of Australian Seaweeds on Commensal Bacteria and Short Chain Fatty Acid Production in a Simulated Gut Model

2022

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Diet is known to affect the composition and metabolite production of the human gut microbial community, which in turn is linked with the health and immune status of the host. Whole seaweeds (WH) and their extracts contain prebiotic components such as polysaccharides (PS) and polyphenols (PP). In this study, the Australian seaweeds, Phyllospora comosa, Ecklonia radiata, Ulva ohnoi, and their PS and PP extracts were assessed for potential prebiotic activities using an in vitro gut model that included fresh human faecal inoculum. 16S rRNA sequencing post gut simulation treatment revealed that the abundance of several taxa of commensal bacteria within the phylum Firmicutes linked with short chain fatty acid (SCFA) production, and gut and immune function, including the lactic acid producing order Lactobacillales and the chief butyrate-producing genera Faecalibacteria, Roseburia, Blautia, and Butyricicoccus were significantly enhanced by the inclusion of WH, PS and PP extracts. After 24 h fermentation, the abundance of total Firmicutes ranged from 57.35–81.55% in the WH, PS and PP samples, which was significantly greater (p ≤ 0.01) than the inulin (INU) polysaccharide control (32.50%) and the epigallocatechingallate (EGCG) polyphenol control (67.13%); with the exception of P. comosa PP (57.35%), which was significantly greater than INU only. However, all WH, PS and PP samples also increased the abundance of the phylum Proteobacteria; while the abundance of the phylum Actinobacteria was decreased by WH and PS samples. After 24 h incubation, the total and individual SCFAs present, including butyric, acetic and propionic acids produced by bacteria fermented with E. radiata and U. ohnoi, were significantly greater than the SCFAs identified in the INU and EGCG controls. Most notably, total SCFAs in the E. radiata PS and U. ohnoi WH samples were 227.53 and 208.68 µmol/mL, respectively, compared to only 71.05 µmol/mL in INU and 7.76 µmol/mL in the EGCG samples. This study demonstrates that whole seaweeds and their extracts have potential as functional food ingredients to support normal gut and immune function.

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Section: Discussionsupporting

confidence: 55%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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The Prebiotic Effect of Australian Seaweeds on Commensal Bacteria and Short Chain Fatty Acid Production in a Simulated Gut Model

2022

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“…The enzymes encoded by these loci are also highly similar to carrageenanases and are able to convert high MW carrageenans into carrageenan oligosaccharides. Furthermore, B. thetaiotaomicron , when cocultured with high MW carrageenans up to 70 h, degrades native carrageenans into poligeenan in a time dependent manner (Pudlo et al., 2020). The average colonic transit time is approximately 14–75 h in healthy adults (Bai et al., 2016), which suggests that there is ample time for carrageenans in the hindgut to be utilized or converted by these bacteria.…”

Section: Mechanisms By Which Carrageenans Exert Their Biological Effectsmentioning

confidence: 99%

“…Conventional wisdom suggests that carrageenanases are only expressed in marine bacterial species, mainly in the phyla Proteobacteria and Bacteroidetes (Chauhan & Saxena, 2016; Ghanbarzadeh et al., 2018). However, several recent studies have demonstrated that many species from the genus Bacteroides isolated from the human gut microbiome grow strongly in carrageenan‐containing media (Figure 2) (Hehemann et al., 2012; Pudlo et al., 2020). These carrageenan‐utilizing species possess polysaccharide utilization loci in their genomes, similar to those identified in marine counterparts.…”

Section: Mechanisms By Which Carrageenans Exert Their Biological Effectsmentioning

confidence: 99%

Food‐grade carrageenans and their implications in health and disease

Liu

Hou

Zhang

et al. 2021

Comp Rev Food Sci Food Safe

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Food additives, often used to guarantee the texture, shelf‐life, taste, and appearance of processed foods, have gained widespread attention due to their increased link to the growing incidence of chronic diseases. As one of the most common additives, carrageenans have been used in human diets for hundreds of years. While classified as generally recognized as safe (GRAS) for human consumption, numerous studies since the 1980s have suggested that carrageenans, particularly those with random coil conformations, may have adverse effects on gastrointestinal health, including aggravating intestinal inflammation. While these studies have provided some evidence of adverse effects, the topic is still controversial. Some have suggested that the negative consequence of the consumption of carrageenans may be structure dependent. Furthermore, pre‐existing conditions may predispose individuals to varied outcomes of carrageenan intake. In this review, structure–function relationships of various carrageenans in the context of food safety are discussed. We reviewed the molecular mechanisms by which carrageenans exert their biological effects. We summarized the findings associated with carrageenan intake in animal models and clinical trials. Moreover, we examined the interactions between carrageenans and the gut microbiome in the pathogenesis of gastrointestinal disorders. This review argues for personalized guidance on carrageenan intake based on individuals’ health status. Future research efforts that aim to close the knowledge gap on the effect of low‐dose and chronic carrageenan intake as well as interactions among food additives should be conducive to the improved safety profile of carrageenans in processed food products.

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Mammalian gut metabolomes mirror microbiome composition and host phylogeny

et al. 2021

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In the past decade, studies on the mammalian gut microbiome have revealed that different animal species have distinct gut microbial compositions. The functional ramifications of this variation in microbial composition remain unclear: do these taxonomic differences indicate microbial adaptations to host-specific functionality, or are these diverse microbial communities essentially functionally redundant, as has been indicated by previous metagenomics studies? Here, we examine the metabolic content of mammalian gut microbiomes as a direct window into ecosystem function, using an untargeted metabolomics platform to analyze 101 fecal samples from a range of 25 exotic mammalian species in collaboration with a zoological center. We find that mammalian metabolomes are chemically diverse and strongly linked to microbiome composition, and that metabolome composition is further correlated to the phylogeny of the mammalian host. Specific metabolites enriched in different animal species included modified and degraded host and dietary compounds such as bile acids and triterpenoids, as well as fermentation products such as lactate and short-chain fatty acids. Our results suggest that differences in microbial taxonomic composition are indeed translated to host-specific metabolism, indicating that taxonomically distant microbiomes are more functionally diverse than redundant.

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Extensive Transfer of Genes for Edible Seaweed Digestion from Marine to Human Gut Bacteria

Cited by 4 publications

References 0 publications

The Prebiotic Effect of Australian Seaweeds on Commensal Bacteria and Short Chain Fatty Acid Production in a Simulated Gut Model

The Prebiotic Effect of Australian Seaweeds on Commensal Bacteria and Short Chain Fatty Acid Production in a Simulated Gut Model

Food‐grade carrageenans and their implications in health and disease

Mammalian gut metabolomes mirror microbiome composition and host phylogeny

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