Microbial chemoautotroph-heterotroph interactions may play a pivotal role in the cycling of carbon in the deep ocean, reminiscent of phytoplankton-heterotroph associations in surface waters. Nitrifiers are the most abundant chemoautotrophs in the global ocean, yet very little is known about nitrifier metabolite production, release, and transfer to heterotrophic microbial communities. To elucidate which organic compounds are released by nitrifiers and potentially available to heterotrophs, we characterized the exo- and endometabolomes of the ammonia-oxidizing archaeon Nitrosopumilus adriaticus CCS1 and the nitrite-oxidizing bacterium Nitrospina gracilis Nb-211. Nitrifier endometabolome composition was not a good predictor of exometabolite availability, indicating that metabolites were predominately released by mechanisms other than cell death/lysis. Although both nitrifiers released labile organic compounds, N. adriaticus preferentially released amino acids, particularly glycine, suggesting that its cell membranes might be more permeable to small, hydrophobic amino acids. We further initiated co-culture systems between each nitrifier and a heterotrophic alphaproteobacterium, and compared exometabolite and transcript patterns of nitrifiers grown axenically to those in co-culture. In particular, B vitamins exhibited dynamic production and consumption patterns in nitrifier-heterotroph co-cultures. We observed an increased production of vitamin B2 and the vitamin B12 lower ligand dimethylbenzimidazole by N. adriaticus and N. gracilis, respectively. In contrast, the heterotroph likely produced vitamin B5 in co-culture with both nitrifiers and consumed the vitamin B7 precursor dethiobiotin when grown with N. gracilis. Our results indicate that B vitamins and their precursors could play a particularly important role in governing specific metabolic interactions between nitrifiers and heterotrophic microbes in the ocean.

中文翻译：

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硝化菌释放的代谢物促进海洋中的代谢相互作用


微生物化能自养-异养生物相互作用可能在深海碳循环中发挥关键作用，这让人想起地表水中的浮游植物-异养生物关联。硝化菌是全球海洋中最丰富的化能自养生物，但人们对硝化菌代谢物的产生、释放和向异养微生物群落的转移知之甚少。为了阐明硝化菌释放哪些有机化合物并可能被异养生物利用，我们对氨氧化古菌 Nitrosopumilus adriaticus CCS1 和亚硝酸盐氧化细菌 Nitrospina gracilis Nb-211 的外代谢组和内代谢组进行了表征。硝化菌内代谢组组成不能很好地预测外代谢物的可用性，这表明代谢物主要通过细胞死亡/裂解以外的机制释放。尽管两种硝化细菌都释放不稳定的有机化合物，但亚得里亚海藻优先释放氨基酸，特别是甘氨酸，这表明其细胞膜可能更容易渗透小的疏水性氨基酸。我们进一步启动了每个硝化菌和异养α变形菌之间的共培养系统，并将无菌生长的硝化菌的外代谢和转录模式与共培养的硝化菌进行了比较。特别是，B 族维生素在硝化菌-异养共培养物中表现出动态的生产和消耗模式。我们观察到亚得里亚海藻和巴西猪笼草分别增加了维生素 B2 和维生素 B12 下配体二甲基苯并咪唑的产量。相比之下，异养生物很可能在与两种硝化细菌共培养时产生维生素 B5，并在与巴西猪笼草一起生长时消耗维生素 B7 前体脱硫生物素。 我们的研究结果表明，B 族维生素及其前体在控制海洋中硝化细菌和异养微生物之间的特定代谢相互作用方面可以发挥特别重要的作用。