Ancient acquisition of “alginate utilization loci” by human gut microbiota

Abstract

In bacteria from the phylum Bacteroidetes, the genes coding for enzymes involved in polysaccharide degradation are often colocalized and coregulated in so-called “polysaccharide utilization loci” (PULs). PULs dedicated to the degradation of marine polysaccharides (e.g. laminaran, ulvan, alginate and porphyran) have been characterized in marine bacteria. Interestingly, the gut microbiome of Japanese individuals acquired, by lateral transfer from marine bacteria, the genes involved in the breakdown of porphyran, the cell wall polysaccharide of the red seaweed used in maki. Sequence similarity analyses predict that the human gut microbiome also encodes enzymes for the degradation of alginate, the main cell wall polysaccharide of brown algae. We undertook the functional characterization of diverse polysaccharide lyases from family PL17, frequently found in marine bacteria as well as those of human gut bacteria. We demonstrate here that this family is polyspecific. Our phylogenetic analysis of family PL17 reveals that all alginate lyases, which have all the same specificity and mode of action, cluster together in a very distinct subfamily. The alginate lyases found in human gut bacteria group together in a single clade which is rooted deeply in the PL17 tree. These enzymes were found in PULs containing PL6 enzymes, which also clustered together in the phylogenetic tree of PL6. Together, biochemical and bioinformatics analyses suggest that acquisition of this system appears ancient and, because only traces of two successful transfers were detected upon inspection of PL6 and PL17 families, the pace of acquisition of marine polysaccharide degradation system is probably very slow.

Extensive transfer of genes for edible seaweed digestion from marine to human gut bacteria

“…1B) . Among strains that grew on alginate, all for which a sequenced genome was available contained known alginate utilization genes 6,7 and loci from representatives in each species were upregulated >100-fold in response to growth on alginate ( Extended Data 1 ). Growth on the remaining polysaccharides was even less prevalent, with only the single, previously known isolate of Bacteroides plebeius from a Japanese adult showing growth on porphyran and individual isolates belonging to two different species, B. thetaiotaomicron and B. ovatus , growing on carrageenan (a mixture of κ, λ isomers).…”

“…As with nearly all dietary fibers, humans lack these enzymes and therefore rely on colonic bacteria for the ability to digest them. Previous studies have documented a few examples in which symbiotic bacteria belonging to Bacteroides— a dominant genus in humans—possess genes for degrading seaweed-derived porphyran 3,4 , agarose 5 , alginate 6,7 and laminarin 8 . In the first three cases, the genes involved often have closest homologs in marine Bacteroidetes, which are physiologically different from gut Bacteroides but share similar mechanisms for polysaccharide degradation 9 .…”

Potential impacts of horizontal gene transfer on human health and physiology and how anthropogenic activity can affect it

“…Acquired genes allow the digestion of carbohydrates present in seaweeds that constitute an important fraction of the daily diet in this human population. Recently, Mathieu et al [32] have postulated the ancient acquisition of alginate (the main polysaccharide in the cell wall of brown algae) metabolism genes coming from marine Bacteroidetes by bacteria of the human gut microbiome. Despite in this case the acquisition is not restricted to Japanese people; authors suggest a similar scenario of acquisition via consumption of marine algae associated with occasional marine bacteria.…”

Saved by seaweeds: phyconomic contributions in times of crises

“…Medicinal uses of seaweeds, as well as potential health benefits of consuming seaweeds, or seaweed-derived products have been extensively reviewed in the scientific literature and are indicative of their importance and growing applications, both in general (Fleurence and Levine 2016 ; Déléris et al 2016 ), as well as in specific cases, such as heart- and coronary diseases (Cornish et al 2015 ; Cardoso et al 2015 ; Murai et al 2019 ), brain and neural development and diseases (Cornish et al 2017 ; Guo et al 2019 ; Schepers et al 2020 ; Hannan et al 2020 ), irritable bowel syndrome and the human microbiome (Mathieu et al 2018 ; Cornish et al 2019 ), prevention and treatment of various cancers (Mamvar et al 2013 ; Jiang and Shi 2018 ), viral infections (Domínguez 2013 ; Mazalovska and Kouokam 2018 ), and parasite infections (Shafiq et al 2018 ), as well as diabetes and obesity (Sharifuddin et al 2015 ; Husni 2018 ; Attjioui et al 2020 ; Bermanoa et al 2020 ). Furthermore, various bioactive compounds of seaweed origin, such as secondary metabolites (Holdt and Kraan 2011 ; Kim 2012 ; Collins et al 2016 ; Rosa et al 2020 ), nutraceuticals (Domínguez 2013 ; Shannon and Abu-Ghannam 2019 ) and other functional ingredients (Peñalver et al 2020 ), have been suggested for judicious use as prophylactics and interventions in disease prevention.…”