Frontiers Science Center for Deep Ocean Multispheres and Earth System, and College of Marine Life Sciences , Ocean University of China, Qingdao, China.
School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, UK.
Microbiome. 2022 Jul 27;10(1):110. doi: 10.1186/s40168-022-01304-0.
Ubiquitous and diverse marine microorganisms utilise the abundant organosulfur molecule dimethylsulfoniopropionate (DMSP), the main precursor of the climate-active gas dimethylsulfide (DMS), as a source of carbon, sulfur and/or signalling molecules. However, it is currently difficult to discern which microbes actively catabolise DMSP in the environment, why they do so and the pathways used.
Here, a novel DNA-stable isotope probing (SIP) approach, where only the propionate and not the DMS moiety of DMSP was C-labelled, was strategically applied to identify key microorganisms actively using DMSP and also likely DMS as a carbon source, and their catabolic enzymes, in North Sea water. Metagenomic analysis of natural seawater suggested that Rhodobacterales (Roseobacter group) and SAR11 bacteria were the major microorganisms degrading DMSP via demethylation and, to a lesser extent, DddP-driven DMSP lysis pathways. However, neither Rhodobacterales and SAR11 bacteria nor their DMSP catabolic genes were prominently labelled in DNA-SIP experiments, suggesting they use DMSP as a sulfur source and/or in signalling pathways, and not primarily for carbon requirements. Instead, DNA-SIP identified gammaproteobacterial Oceanospirillales, e.g. Amphritea, and their DMSP lyase DddD as the dominant microorganisms/enzymes using DMSP as a carbon source. Supporting this, most gammaproteobacterial (with DddD) but few alphaproteobacterial seawater isolates grew on DMSP as sole carbon source and produced DMS. Furthermore, our DNA-SIP strategy also identified Methylophaga and other Piscirickettsiaceae as key bacteria likely using the DMS, generated from DMSP lysis, as a carbon source.
This is the first study to use DNA-SIP with C-labelled DMSP and, in a novel way, it identifies the dominant microbes utilising DMSP and DMS as carbon sources. It highlights that whilst metagenomic analyses of marine environments can predict microorganisms/genes that degrade DMSP and DMS based on their abundance, it cannot disentangle those using these important organosulfur compounds for their carbon requirements. Note, the most abundant DMSP degraders, e.g. Rhodobacterales with DmdA, are not always the key microorganisms using DMSP for carbon and releasing DMS, which in this coastal system were Oceanospirillales containing DddD. Video abstract.
丰富多样的海洋微生物利用丰富的有机硫分子二甲基巯基丙酸酯（DMSP），作为碳、硫和/或信号分子的主要前体，将其作为碳、硫和/或信号分子的来源。然而，目前很难确定哪些微生物在环境中积极地代谢 DMSP，它们为什么这样做以及使用哪些途径。
在这里，一种新的 DNA 稳定同位素探测（SIP）方法，其中只有 DMSP 的丙酸酯部分而不是 DMS 部分被 C 标记，被策略性地应用于识别在北海水中积极使用 DMSP 以及可能的 DMS 作为碳源的关键微生物，以及它们的代谢酶。对天然海水的宏基因组分析表明，红杆菌目（玫瑰杆菌群）和 SAR11 细菌是通过去甲基化和在较小程度上通过 DddP 驱动的 DMSP 裂解途径降解 DMSP 的主要微生物。然而，无论是红杆菌目和 SAR11 细菌及其 DMSP 代谢基因都没有在 DNA-SIP 实验中被显著标记，这表明它们将 DMSP 用作硫源和/或信号途径，而不是主要用于碳需求。相反，DNA-SIP 鉴定出γ变形菌目海洋螺旋体，例如 Amphritea，及其 DMSP 裂解酶 DddD 是主要的微生物/酶，将 DMSP 用作碳源。支持这一点的是，大多数γ变形菌（带有 DddD）而不是少数α变形菌海水分离株仅以 DMSP 作为唯一碳源生长并产生 DMS。此外，我们的 DNA-SIP 策略还鉴定出甲基噬菌菌和其他 Piscirickettsiaceae 可能作为关键细菌，利用从 DMSP 裂解中产生的 DMS 作为碳源。
这是首次使用 C 标记的 DMSP 进行 DNA-SIP 的研究，它以一种新的方式确定了利用 DMSP 和 DMS 作为碳源的主要微生物。它强调了尽管对海洋环境的宏基因组分析可以根据其丰度预测降解 DMSP 和 DMS 的微生物/基因，但它不能区分那些将这些重要的有机硫化合物用于其碳需求的微生物/基因。请注意，最丰富的 DMSP 降解物，例如具有 DmdA 的红杆菌目，并不总是关键的微生物，它们将 DMSP 用于碳并释放 DMS，在这个沿海系统中，DddD 是海洋螺旋体。视频摘要。
