Microbial photoautotroph-heterotroph interactions underlie marine food webs and shape ecosystem diversity and structure in upper ocean environments. Here, bacterial community composition, lifestyle preference, and genomic- and proteomic-level metabolic characteristics were investigated for an open ocean Synechococcus ecotype and its associated heterotrophs over 91 days of cocultivation. The associated heterotrophic bacterial assembly mostly constituted five classes, including Flavobacteria, Bacteroidetes, Phycisphaerae, Gammaproteobacteria, and Alphaproteobacteria The seven most abundant taxa/genera comprised >90% of the total heterotrophic bacterial community, and five of these displayed distinct lifestyle preferences (free-living or attached) and responses to Synechococcus growth phases. Six high-quality genomes, including Synechococcus and the five dominant heterotrophic bacteria, were reconstructed. The only primary producer of the coculture system, Synechococcus, displayed metabolic processes primarily involved in inorganic nutrient uptake, photosynthesis, and organic matter biosynthesis and release. Two of the flavobacterial populations, Muricauda and Winogradskyella, and an SM1A02 population, displayed preferences for initial degradation of complex compounds and biopolymers, as evinced by high abundances of TonB-dependent transporters (TBDTs), glycoside hydrolase, and peptidase proteins. Polysaccharide utilization loci present in the flavobacterial genomes influence their lifestyle preferences and close associations with phytoplankton. In contrast, the alphaproteobacterium Oricola sp. population mainly utilized low-molecular-weight dissolved organic carbon (DOC) through ATP-binding cassette (ABC), tripartite ATP-independent periplasmic (TRAP), and tripartite tricarboxylate transporter (TTT) transport systems. The heterotrophic bacterial populations exhibited complementary mechanisms for degrading Synechococcus-derived organic matter and driving nutrient cycling. In addition to nutrient exchange, removal of reactive oxygen species and vitamin trafficking might also contribute to the maintenance of the Synechococcus-heterotroph coculture system and the interactions shaping the system.IMPORTANCE The high complexity of in situ ecosystems renders it difficult to study marine microbial photoautotroph-heterotroph interactions. Two-member coculture systems of picocyanobacteria and single heterotrophic bacterial strains have been thoroughly investigated. However, in situ interactions comprise far more diverse heterotrophic bacterial associations with single photoautotrophic organisms. In the present study, combined metagenomic and metaproteomic data supplied the metabolic potentials and activities of uncultured dominant bacterial populations in the coculture system. The results of this study shed light on the nature of interactions between photoautotrophs and heterotrophs, improving our understanding of the complexity of in situ environments.

中文翻译：

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元基因组学和蛋白质组学的洞察球菌文化中的光合自养和异养相互作用。

微生物光自养与异养之间的相互作用是海洋食物网的基础，并影响着上层海洋环境中的生态系统多样性和结构。在这里，共培养91天后，研究了开放海洋Synechococcus生态型及其相关异养生物的细菌群落组成，生活方式偏爱以及基因组和蛋白质组水平的代谢特征。相关的异养细菌装配体主要分为五类，包括黄杆菌属，拟杆菌属，Phycisphaerae，γ变形杆菌和Alphaproteobacteria。七种最丰富的分类单元/属占异养细菌总数的90％以上，其中五种显示出不同的生活方式偏好（生活或依恋）以及对Synechococcus生长阶段的反应。六个高质量的基因组，包括合成球菌和五个优势异养细菌。共培养系统的唯一主要生产者Synechococcus，显示出代谢过程，主要涉及无机养分的吸收，光合作用以及有机物的生物合成和释放。两个黄细菌种群，Muricauda和Winogradskyella，以及一个SM1A02种群，表现出对复杂化合物和生物聚合物进行初始降解的偏好，这由高水平的TonB依赖转运蛋白（TBDT），糖苷水解酶和肽酶蛋白证明。黄细菌基因组中存在的多糖利用位点会影响其生活方式偏好，并与浮游植物密切相关。相反，αproteobacterOricola sp。人口主要通过ATP结合盒（ABC），不依赖ATP的三方质（TRAP）和三羧酸三羧酸盐转运蛋白（TTT）转运系统利用低分子量溶解有机碳（DOC）。异养细菌群体表现出互补的机制，可以降解源自球菌的有机物并促进营养循环。除了交换养分外，活性氧的去除和维生素的运输也可能有助于维持Syechococcus-异养共养系统和系统相互作用。重要原位生态系统的高度复杂性使其难以研究海洋微生物的自养生物。 -异养相互作用。蓝藻细菌和单一异养细菌菌株的两人共培养系统已被彻底研究。然而，原位相互作用包括与单一光合自养生物的多种多样的异养细菌缔合。在本研究中，宏基因组学和元蛋白质组学数据相结合提供了共培养系统中未培养的优势细菌种群的代谢潜力和活性。这项研究的结果阐明了光自养生物和异养生物之间相互作用的性质，从而增进了我们对原位环境复杂性的理解。宏基因组学和元蛋白质组学数据相结合，提供了共培养系统中未培养的优势细菌种群的代谢潜力和活性。这项研究的结果阐明了光自养生物和异养生物之间相互作用的性质，从而增进了我们对原位环境复杂性的理解。宏基因组学和元蛋白质组学数据相结合，提供了共培养系统中未培养的优势细菌种群的代谢潜力和活性。这项研究的结果阐明了光自养生物和异养生物之间相互作用的性质，从而增进了我们对原位环境复杂性的理解。