Assembly and synthesis of the extracellular matrix in brown algae

Mazéas, Lisa; Yonamine, Rina; Barbeyron, Tristan; Henrissat, Bernard; Drula, Élodie; Terrapon, Nicolas; Nagasato, Chikako; Hervé, Cécile

doi:10.1016/j.semcdb.2022.03.005

Cited by 19 publications

(27 citation statements)

References 84 publications

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“…This diversification has resulted in organisms with a broad range of morphological complexity ranging from filamentous to complex parenchymatous thalli, with the more complex thalli containing a greater number of different cell types (Figures 1 and S9A). Additional highly variable characteristics of the brown algae include the structures of their life cycles, their diverse reproductive strategies and their metabolic pathways 28,29,70,71 . The Phaeoexplorer dataset was analysed to search for genomic features associated with these diverse phenotypic characteristics.…”

Section: Resultsmentioning

confidence: 99%

Evolutionary genomics of the emergence of brown algae as key components of coastal ecosystems

Denoeud,

Godfroy,

Cruaud

et al. 2024

Preprint

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SUMMARYBrown seaweeds are keystone species of coastal ecosystems, often forming extensive underwater forests, that are under considerable threat from climate change. Despite their ecological and evolutionary importance, this phylogenetic group, which is very distantly related to animals and land plants, is still poorly characterised at the genome level. Here we analyse 60 new genomes that include species from all the major brown algal orders. Comparative analysis of these genomes indicated the occurrence of several major events coinciding approximately with the emergence of the brown algal lineage. These included marked gain of new orthologous gene families, enhanced protein domain rearrangement, horizontal gene transfer events and the acquisition of novel signalling molecules and metabolic pathways. The latter include enzymes implicated in processes emblematic of the brown algae such as biosynthesis of the alginate-based extracellular matrix, and halogen and phlorotannin biosynthesis. These early genomic innovations enabled the adaptation of brown algae to their intertidal habitats. The subsequent diversification of the brown algal orders tended to involve loss of gene families, and genomic features were identified that correlated with the emergence of differences in life cycle strategy, flagellar structure and halogen metabolism. We show that integration of large viral genomes has had a significant impact on brown algal genome content and propose that this process has persisted throughout the evolutionary history of the lineage. Finally, analysis of microevolutionary patterns within the genusEctocarpusindicated that deep gene flow between species may be an important factor in genome evolution on more recent timescales.

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Section: Resultsmentioning

confidence: 99%

Evolutionary genomics of the emergence of brown algae as key components of coastal ecosystems

Denoeud,

Godfroy,

Cruaud

et al. 2024

Preprint

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“…The FCSPs are likely initially polymerized in the state of neutral glycans by GTs, prior to their sulfation by STs. GTs and STs form large multigenic families in brown algae and brown algal STs can be clustered into at least 15 clades [12]. In order to investigate the origin of brown algal STs within the Stramenopiles, we analysed the ST gene content of all the Phaeoexplorer brown algal and sister taxa genomes, along with genomes of other Stramenopiles.…”

Section: Prediction Of Candidate Genes For the Synthesis Of Sulfated ...mentioning

confidence: 99%

Evolutionary history of the main extracellular matrix polysaccharides in brown algae

Hervé,

Bouguerba-Collin,

Cock

et al. 2024

Preprint

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Background: Brown algae belong to the Stramenopiles phylum and are phylogenetically distant from plants and other multicellular organisms. This independent evolutionary history has shaped brown algae with numerous metabolic characteristics specific to this group, including the synthesis of peculiar polysaccharides contained in their extracellular matrix (ECM). Alginates and fucose-containing sulphated polysaccharides (FCSP), the latter including fucans, are the main components of ECMs. However, the metabolic pathways of these polysaccharides remain poorly described due to a lack of genomic data. Results: An extensive genomic dataset has been recently released for brown algae and their close sister species. We performed an expert annotation of key genes involved in ECM-carbohydrate metabolisms, combined with comparative genomics, phylogenetics analyses, and protein modelling. Our analysis indicates that the gene families involved in both the synthesis and degradation of alginate were acquired by the common ancestor of brown algae and their closest sister species Schizocladia ischiensis, and subsequently expanded in brown algae. The pathway for the biosynthesis of fucans still remains biochemically unresolved and we also identify the most likely fucosyltransferase genes that may harbour a fucan synthase activity in brown algae. Conclusions: The expansion of specific families related to alginate metabolism may have represented an important prerequisite for the evolution of developmental complexity in brown algae. Our analysis questions the possible occurrence of FCSPs outside brown algae, notably within their closest sister taxon and in other Stramenopiles such as diatoms. Filling this knowledge gap in the future will help determine the origin and evolutionary history of fucan synthesis in eukaryotes. Access to the present large genomic resource allowed us to identify putative glycosyltransferases (GTs) involved in fucan synthesis and elongation, and members of the GT23 family appear to be very interesting candidates for functional validation.

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“…Only second follows innovation to increase carbon dioxide removal and storage capacity 7 . Diatoms 2 and brown algae synthesize an extracellular matrix 8 that contains fucoidan, a sulfated fucan with antibacterial 9 , antiviral 10 and antifouling activity 11,12 . Algal blooms accumulate dissolved and particulate fucan.…”

Section: Mainmentioning

confidence: 99%

Phosphate starvation stops bacteria digesting algal fucan that sequesters carbon

Xu,

Schultz-Johansen,

Yao

et al. 2024

Preprint

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Algae provide a solar powered pathway to capture and sequester carbon by injecting stable fucan made from carbon dioxide into the ocean1–4. Stability of the pathway is at odds with the presence of marine bacteria with genes of enzymes that can digest fucan and release the carbon dioxide5. Biochemical explanations for stable fucan remain hypothetical6. We assembled a biological carbon cycle model and found phosphate limitation enhanced fucan synthesis by algae, stopped digestion by bacteria and thereby stabilized the fucan carbon sequestration pathway. Marine microalgaeGlossomastixsp. PLY432 increased synthesis of fucan, a part of its extracellular matrix, under nutrient-growth limiting conditions. Rate and extent of fucan digestion by a marine, isolated bacterium of theAkkermansiaceaefamily decreased with decreasing phosphate concentration. Phosphate starvation restricted bacterial growth rate, biomass yield and in turn increased the amount of stable fucan. Phosphate is universally required for growth but rare relative to glycan carbon in photosynthesis-derived ecosystems. The fact that phosphate is required for replication, transcription and translation explains why bacteria can digest gigatons of laminarin with a few enzymes, but not fucan during nutrient limited algal blooms. We conclude phosphate starvation constrains the ability of bacteria to digest fucan, which evolves to maintain stability around algal cells and consequentially also to keep carbon dioxide in the ocean.

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Assembly and synthesis of the extracellular matrix in brown algae

Cited by 19 publications

References 84 publications

Evolutionary genomics of the emergence of brown algae as key components of coastal ecosystems

Evolutionary genomics of the emergence of brown algae as key components of coastal ecosystems

Evolutionary history of the main extracellular matrix polysaccharides in brown algae

Phosphate starvation stops bacteria digesting algal fucan that sequesters carbon

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