State Key Laboratory of Microbial Technology, Marine Biotechnology Research Center, Shandong University, Qingdao, China.
MOE Key Laboratory of Evolution and Marine Biodiversity, Frontiers Science Center for Deep Ocean Multispheres and Earth System & College of Marine Life Sciences, Ocean University of China, Qingdao, China.
Appl Environ Microbiol. 2024 Feb 21;90(2):e0202523. doi: 10.1128/aem.02025-23. Epub 2024 Jan 23.
Marine bacteria play important roles in the degradation and cycling of algal polysaccharides. However, the dynamics of epiphytic bacterial communities and their roles in algal polysaccharide degradation during kelp decay are still unclear. Here, we performed metagenomic analyses to investigate the identities and predicted metabolic abilities of epiphytic bacterial communities during the early and late decay stages of the kelp . During kelp decay, the dominant epiphytic bacterial communities shifted from Gammaproteobacteria to Verrucomicrobia and Bacteroidetes. In the early decay stage of , epiphytic bacteria primarily targeted kelp-derived labile alginate for degradation, among which the gammaproteobacterial (particularly ) and (particularly ), abundant in alginate lyases belonging to the polysaccharide lyase (PL) families PL6, PL7, and PL17, were key alginate degraders. More complex fucoidan was preferred to be degraded in the late decay stage of by epiphytic bacteria, predominantly from Verrucomicrobia (particularly ), of Planctomycetes (particularly ), of Kiritimatiellota, and of Bacteroidetes, which depended on using glycoside hydrolases (GHs) from the GH29, GH95, and GH141 families and sulfatases from the S1_15, S1_16, S1_17, and S1_25 families to depolymerize fucoidan. The pathways for algal polysaccharide degradation in dominant epiphytic bacterial groups were reconstructed based on analyses of metagenome-assembled genomes. This study sheds light on the roles of different epiphytic bacteria in the degradation of brown algal polysaccharides.IMPORTANCEKelps are important primary producers in coastal marine ecosystems. Polysaccharides, as major components of brown algal biomass, constitute a large fraction of organic carbon in the ocean. However, knowledge of the identities and pathways of epiphytic bacteria involved in the degradation process of brown algal polysaccharides during kelp decay is still elusive. Here, based on metagenomic analyses, the succession of epiphytic bacterial communities and their metabolic potential were investigated during the early and late decay stages of . Our study revealed a transition in algal polysaccharide-degrading bacteria during kelp decay, shifting from alginate-degrading Gammaproteobacteria to fucoidan-degrading Verrucomicrobia, Planctomycetes, Kiritimatiellota, and Bacteroidetes. A model for the dynamic degradation of algal cell wall polysaccharides, a complex organic carbon, by epiphytic microbiota during kelp decay was proposed. This study deepens our understanding of the role of epiphytic bacteria in marine algal carbon cycling as well as pathogen control in algal culture.
海洋细菌在藻类多糖的降解和循环中发挥着重要作用。然而，在海带腐烂过程中，附生细菌群落的动态及其在藻类多糖降解中的作用仍不清楚。在这里，我们进行了宏基因组分析，以研究海带早期和晚期腐烂过程中附生细菌群落的身份和预测代谢能力。在海带腐烂过程中，优势附生细菌群落从γ变形菌门转移到疣微菌门和拟杆菌门。在海带腐烂的早期阶段，附生细菌主要针对海带衍生的易降解褐藻胶进行降解，其中γ变形菌门（特别是）和（特别是），富含属于多糖裂解酶（PL）家族 PL6、PL7 和 PL17 的褐藻胶裂解酶，是关键的褐藻胶降解菌。在海带腐烂的晚期阶段，更多复杂的岩藻聚糖被附生细菌优先降解，主要来自疣微菌门（特别是）、浮霉菌门（特别是）、奇古菌门、拟杆菌门，它们依赖于使用糖苷水解酶（GH）家族 GH29、GH95 和 GH141 以及硫酸酯酶家族 S1_15、S1_16、S1_17 和 S1_25 来解聚岩藻聚糖。根据宏基因组组装基因组的分析，重建了优势附生细菌群在海藻多糖降解中的途径。这项研究揭示了不同附生细菌在褐藻多糖降解中的作用。
海带是沿海海洋生态系统中的重要初级生产者。多糖作为褐藻生物质的主要成分，构成了海洋中有机碳的很大一部分。然而，关于海带腐烂过程中参与褐藻多糖降解的附生细菌的身份和途径的知识仍然难以捉摸。在这里，基于宏基因组分析，研究了海带早期和晚期腐烂过程中附生细菌群落的演替及其代谢潜力。我们的研究揭示了海带腐烂过程中，从降解褐藻胶的γ变形菌门到降解岩藻聚糖的疣微菌门、浮霉菌门、奇古菌门和拟杆菌门，藻类多糖降解菌的转变。提出了一个关于海带腐烂过程中附生微生物对藻类细胞壁多糖（一种复杂的有机碳）动态降解的模型。这项研究加深了我们对附生细菌在海洋藻类碳循环以及藻类培养中病原体控制中的作用的理解。
