Hyper-specialized Bacteroidetes selfishly compete for laminarin in microalgal blooms

Laminarin is a major storage polysaccharide in phytoplankton and an important carbon and energy source for marine microbes. How microbes compete for this labile polysaccharide in nature remains unclear. Here we investigated metaproteomes and metagenomes of bacterioplankton during four consecutive algal blooms in the North Sea to determine key laminarin consumers. We identified two specialized laminarin degraders of the Bacteroidetes group, which reached high abundances year after year. We found that these genomically streamlined bacteria of the genus Formosa have an expanded set of laminarin hydrolases, sensors and transporters that belonged to the most abundant proteins in the blooms. The respective genes are organized in three polysaccharide utilization loci. Proteomic and biochemical analyses revealed surface tethered enzymes and a laminarinase recombined with a membrane-spanning transporter, which act as a disassembly line and efficiently integrate substrate degradation and uptake in the highly diffusive, aquatic environment. We also show that the bloom bacteria couple laminarin utilization with uptake of cellular building blocks such as amino acids. This study suggests that in addition to genome reduction, enzyme fusions, transporter and enzyme expansion also the tight coupling of the carbon and nitrogen uptake make Formosa spp. efficient laminarin utilizers.

褐藻淀粉（Laminarin）是浮游植物（phytoplankton）中的主要储存性多糖，亦是海洋微生物关键的碳源与能源物质。目前学界尚未明确微生物在自然环境中如何竞争利用这类易分解多糖。本研究针对北海连续四次藻华期间的浮游细菌（bacterioplankton）宏蛋白质组（metaproteome）与宏基因组（metagenome）展开系统分析，旨在明确褐藻淀粉的核心消耗类群。我们鉴定出拟杆菌门（Bacteroidetes）下两类特化的褐藻淀粉降解菌，它们连续多个藻华周期均保持较高丰度。研究发现，这类基因组精简的弗莫萨菌属（Formosa）细菌，携带一套扩增的褐藻淀粉水解酶、感应蛋白与转运蛋白编码基因，这些蛋白在藻华期间属于丰度最高的蛋白类群之一。相关功能基因被组装为三个多糖利用基因座（polysaccharide utilization loci）。蛋白质组学与生化分析结果显示，膜锚定酶与融合跨膜转运蛋白的褐藻淀粉酶可形成一套分解流水线，在高度弥散的水生环境中高效协同底物降解与摄取过程。此外，本研究证实藻华相关细菌可将褐藻淀粉利用与氨基酸等细胞结构单元的摄取过程相偶联。本研究表明，除基因组精简、酶融合、转运蛋白与水解酶扩增外，碳氮摄取的紧密偶联同样是弗莫萨菌属物种成为高效褐藻淀粉利用者的关键机制。