It is shown that fucoidans are degraded through synergistic interactions between specialized bacteria with complementary metabolic functions, providing a mechanistic framework for understanding carbon cycling in the ocean and for engineering synthetic microbial consortia to degrade recalcitrant polysaccharides.
Abstract
Fucoidans, a class of complex polysaccharides produced by brown algae and diatoms, contribute to long-term carbon sequestration owing to their resistance to microbial degradation1,2. Although individual microorganisms can break down portions of these polysaccharides3-5, it remains unclear whether complete breakdown is possible in nature and, if so, by what mechanisms. Here we show that fucoidans are degraded through synergistic interactions between specialized bacteria with complementary metabolic functions. Using metabolomic analysis of a reconstructed marine consortium, we uncovered metabolic guilds of bacteria that preferentially degrade either the sulfated fucose backbone or the side branches of rare monomers. This functional division of labour leads to an unexpectedly high number of synergistic interactions between different degraders that enhanced degradation efficiency up to 97.1%. Despite varying fucoidan structures across different types of algae6, the metabolic functions of degraders remained conserved, enabling quantitative prediction of degradation outcomes based on community and substrate composition. The frequent co-occurrence of functionally complementary fucoidan degraders in ocean metagenomes suggests that synergistic degradation is a globally relevant strategy. Our findings suggest that the environmental turnover of complex biopolymers depends not only on individual metabolic capabilities of degraders but also on ecological interactions shaped by substrate architecture. This work provides a mechanistic framework for understanding carbon cycling in the ocean and for engineering synthetic microbial consortia to degrade recalcitrant polysaccharides.
Macroalgae secrete complex carbohydrate polymers, their extracellular matrix, as protection against microbial degradation. By resisting breakdown, these carbohydrates can contribute to marine carbon sequestration, though mechanisms, extent, and timescales remain unknown. Using ship-based sampling and experiments, we found that brown macroalgae release 1.7-4.2% of carbon fixation as fucoidan, equivalent to 0.32-0.88 mg fucoidan per gram of dry seaweed tissue per day. A Bayesian model trained on our empirical data, coupled with Monte Carlo simulations suggests an annual global release of 13-37 megatons fucoidan carbon. Moreover, degradation resistance combined with surface-activity enabled fucoidan to act as glue that cross-linked allochthonous organic carbon including microbes and proteins into marine snow. Notably, substantial fucoidan exudation was universally conserved across all tested species and regions. Thus, any brown macroalgal species can be used e.g. via aquafarming to enhance the formation of marine snow.
Inga Hellige, H. Buck-Wiese, M. Bligh et al.· bioRxiv· 0 citations
Fucoidans, also known as fucose-containing sulfated polysaccharides (FCSPs), are abundant and structurally complex glycans found in the cell wall of brown algae. These compounds have been shown to have fundamental roles in the development and physiology of these organisms, to provide a major contribution to marine carbon sequestration, and to exhibit numerous bioactivities. Despite this, we currently have a limited understanding of the metabolic pathways and enzymes involved in synthesis and remodelling of fucoidans, their spatial and temporal dynamics in brown algae and in the marine environment, and how their structure and composition influence their bioactivities. Here, we highlight some of the challenges that have hindered progress on fucoidan research. We then moved on to underline some of the recent technical progress and new resources that would contribute to alleviate these challenges when combined together. This includes new technical approaches in analytical chemistry and glycobiology, as well the extension of genomic resources and genetics tools for brown algae. Finally, we suggest how progress in fucoidan research should contribute to advance understanding on brown algae biology, while supporting current and developing new aspects in fucoidan applications and seaweed biotechnology as part of the growing blue bioeconomy.
T. Tonon, F. Aachmann, Vincent Ferrières et al.· The Cell Surface· 0 citations
A wide range of microorganisms produce storage biopolymer polyhydroxyalkanoates (sPHAs) as carbon and energy reserves. However, only bacteria and fungi are known to degrade microbial sPHAs, using enzymes called polyhydroxyalkanoate depolymerases (PHADs). Here we show that some animals also have PHADs that can degrade sPHAs. We discovered a PHAD in the gutless oligochaete Olavius algarvensis, a marine worm that gains nutrition by digesting bacterial symbionts, including a dominant symbiont in which sPHAs account for up to 42% of cellular carbon stores. Enzyme assays, combined with mass spectrometry, confirmed that heterologously expressed O. algarvensis PHAD degraded sPHAs into hydroxyalkanoate monomers that can enter conserved metabolic pathways. Imaging of mRNA showed that PHAD was expressed in the oligochaete epidermis, the site of symbiont digestion. We further identified PHADs in more than 66 gut-bearing animal species from nine phyla and 19 protist species from three major supergroups, suggesting that the last common ancestor of metazoans possessed PHADs. Functional assays confirmed that PHADs from phylogenetically distant animal lineages spanning aquatic and terrestrial environments degrade sPHAs. These findings reveal a previously unrecognized pathway by which protists and animals can access microbial carbon reserves, with broad relevance given the widespread occurrence of sPHAs across ecosystems.
Caroline Zeidler, Harald R Gruber-Vodicka, D. Michellod et al.· Nature Ecology & Evolution· 0 citations
Bacteroides thetaiotaomicron (Bt) degrades dietary glycans via carbohydrate-active enzymes (CAZymes), but their spatial distribution and functional coordination remain unclear. In this study, we characterized the "labor division" during glycan degradation across four bacterial fractions: cytoplasm, outer membrane, extracellular vesicles, and supernatant. All fractions displayed hydrolytic activity. Proteomic analysis identified abundant glycoside hydrolases, mainly GH32 enzymes encoded by PUL22, and their components varied greatly. Untargeted metabolomics identified 45 shared differential metabolites (e.g., carbohydrates and short-chain fatty acids), indicating distinct hydrolytic capacities among fractions. Notably, cross-feeding experiments confirmed that Bt EVs-mediated degradation can support the growth of recipient bacteria. Collectively, our results reveal a synergistic multicomponent strategy for glycan degradation in Bacteroides, offering new insights into glycan utilization and laying a foundation for developing postbiotics and functional microbial products.
Ying He, Ziyang Yu, Qiqiong Li et al.· Journal of Agricultural and...· 0 citations
The enrichment and expression of polyphenol degradation pathways define a previously underappreciated metabolic niche for SAR116 and provides new evidence emphasizing the importance of polyphenol metabolism in the marine carbon cycle.
Jordan T. Coelho, M. Borton, J. Thrash· bioRxiv· 0 citations
It is revealed that a globally distributed clade of symbiotic SRB has a conserved core metabolism that diverges from free-living relatives, and these endosymbionts retain key traits of SRB such as sulfate reduction, complete oxidation of acetate to CO2, amino acid degradation for nitrogen acquisition, and transport of essential nutrients.
G. D'Angelo, Manuel Kleiner, A. Mankowski et al.· The ISME Journal· 0 citations
