The frequent occurrence and metabolic versatility of Marinifilaceae bacteria involved in organic matter mineralization as a key member in global deep sea

Transfer of animal and plant detritus of both terrestrial and marine origins to the deep sea occurs on the global scale. Microorganisms play an important role in mineralizing them therein, yet to identify in situ. To observe key bacteria involved, we conducted long-term in situ incubation and found the family Marinifilaceae occurred as one of the most predominant bacteria thriving on the new inputs of plant and animal biomasses in the deep sea of both marginal and oceanic areas. This taxa is diverse and ubiquitous in marine environments. A total of 11 MAGs belonging to MF were retrieved from metagenomic data and diverged into four subgroups based on the phylogenomic tree. We described the metabolic features and in situ metabolizing activities of different MF subgroups via the metagenomic and metatranscriptomic data. One representative subgroup MF-2 dominated plant detritus-enriched cultures and specialized in polysaccharide degradation and lignin oxidation. Intriguingly, they encode nitrogen fixation pathway to compensate for the shortage of nitrogen sources inside the plant detritus. In contrast, those dominating the animal tissue-supported microbiomes were more diverse and formed three subgroups, which distinguished themselves from MF-2 in carbon and nitrogen metabolisms. Despite these metabolic divergences of MF lineages, they harbored anaerobic processes for energy conservation via organic fermentation, anaerobic respiration via iron and manganese reduction, and/or dimethyl sulfoxide reduction. These results highlight the role of Marinifilaceae bacteria neglected before in organic matter mineralizing in marine environments coupling carbon and nitrogen cycling with metals and other elements.

全球尺度下，陆地与海洋来源的动植物碎屑会向深海输运。微生物在该环境中对这些碎屑的矿化过程发挥重要作用，但相关功能类群的原位识别仍有待深入解析。为明确参与该过程的关键细菌类群，本研究开展了长期原位培养实验，结果发现：在边缘海与远洋深海区域的动植物生物质新输入环境中，绳菌科（Marinifilaceae）是最为优势的增殖细菌类群之一。该类群在海洋环境中分布广泛且具有丰富的多样性。本研究从宏基因组数据中共获得11个隶属于绳菌科的宏基因组组装基因组（metagenome-assembled genome, MAG），基于系统发育基因组树可将其划分为4个亚群。本研究通过宏基因组与宏转录组数据，解析了不同绳菌科亚群的代谢特征与原位代谢活性。其中代表性亚群MF-2在富含植物碎屑的培养体系中占据主导地位，其功能专长为多糖降解与木质素氧化。值得注意的是，该亚群携带固氮通路，可弥补植物碎屑中氮源匮乏的缺陷。与之相对，在以动物组织为底物的微生物群落中占据主导的绳菌科类群则具有更高的多样性，可划分为3个亚群，且在碳、氮代谢模式上与MF-2亚群存在显著差异。尽管不同绳菌科演化支的代谢模式存在上述差异，但它们均具备通过有机发酵实现能量留存的厌氧过程，以及通过铁、锰还原或二甲基亚砜还原完成厌氧呼吸的代谢通路。本研究结果表明，绳菌科细菌在海洋环境有机质矿化过程中发挥了此前被忽视的重要作用，其代谢活动将碳、氮循环与金属及其他元素循环耦合在了一起。