Brown algae are important players in the global carbon cycle by fixing carbon dioxide into 1 Gt of biomass annually, yet the fate of fucoidan—their major cell wall polysaccharide—remains poorly understood. Microbial degradation of fucoidans is slower than that of other polysaccharides, suggesting that fucoidans are more recalcitrant and may sequester carbon in the ocean. This may be due to the complex, branched and highly sulfated structure of fucoidans, which also varies among species of brown algae. Here, we show that ‘Lentimonas’ sp. CC4, belonging to the Verrucomicrobia, acquired a remarkably complex machinery for the degradation of six different fucoidans. The strain accumulated 284 putative fucoidanases, including glycoside hydrolases, sulfatases and carbohydrate esterases, which are primarily located on a 0.89-megabase pair plasmid. Proteomics reveals that these enzymes assemble into substrate-specific pathways requiring about 100 enzymes per fucoidan from different species of brown algae. These enzymes depolymerize fucoidan into fucose, which is metabolized in a proteome-costly bacterial microcompartment that spatially constrains the metabolism of the toxic intermediate lactaldehyde. Marine metagenomes and microbial genomes show that Verrucomicrobia including ‘Lentimonas’ are abundant and highly specialized degraders of fucoidans and other complex polysaccharides. Overall, the complexity of the pathways underscores why fucoidans are probably recalcitrant and more slowly degraded, since only highly specialized organisms can effectively degrade them in the ocean.

褐藻通过每年将二氧化碳固定到 1 Gt 的生物质中而成为全球碳循环的重要参与者，但褐藻糖胶（它们的主要细胞壁多糖）的命运仍然知之甚少。褐藻糖胶的微生物降解速度比其他多糖慢，这表明褐藻糖胶更顽固，可能会螯合海洋中的碳。这可能是由于褐藻糖胶的复杂、支化和高度硫酸化的结构，褐藻的种类也不同。在这里，我们展示了 ' Lentimonas' sp。CC4 属于 Verrucomicrobia，获得了一种非常复杂的机制来降解六种不同的褐藻糖胶。该菌株积累了 284 种假定的岩藻依聚糖酶，包括糖苷水解酶、硫酸酯酶和碳水化合物酯酶，它们主要位于 0.89 兆碱基对的质粒上。蛋白质组学表明，这些酶组装成底物特异性途径，每个褐藻糖胶需要来自不同种类褐藻的约 100 种酶。这些酶将岩藻依聚糖解聚成岩藻糖，岩藻糖在蛋白质组成本高的细菌微区室中代谢，在空间上限制了有毒中间体乳醛的代谢。海洋宏基因组和微生物基因组显示，疣微菌包括 ' Lentimonas' 是褐藻糖胶和其他复杂多糖的丰富且高度专业化的降解剂。总体而言，这些途径的复杂性强调了为什么褐藻糖胶可能是顽固的并且降解更慢，因为只有高度专业化的生物才能在海洋中有效地降解它们。