State Key Laboratory of Marine Environmental Science, Fujian Key Laboratory of Marine Carbon Sequestration, College of Ocean and Earth Sciences, Xiamen University, Xiang'an South Road, Xiamen 361102, China.
State Key Laboratory of Cellular Stress Biology, Fujian Provincial Key Laboratory of Innovative Drug Target Research, School of Pharmaceutical Sciences, Xiamen University, Xiamen 361102, China.
ISME J. 2024 Jan 8;18(1). doi: 10.1093/ismejo/wrae084.
Chirality, a fundamental property of matter, is often overlooked in the studies of marine organic matter cycles. Dihydroxypropanesulfonate (DHPS), a globally abundant organosulfur compound, serves as an ecologically important currency for nutrient and energy transfer from phytoplankton to bacteria in the ocean. However, the chirality of DHPS in nature and its transformation remain unclear. Here, we developed a novel approach using chiral phosphorus-reagent labeling to separate DHPS enantiomers. Our findings demonstrated that at least one enantiomer of DHPS is present in marine diatoms and coccolithophores, and that both enantiomers are widespread in marine environments. A novel chiral-selective DHPS catabolic pathway was identified in marine Roseobacteraceae strains, where HpsO and HpsP dehydrogenases at the gateway to DHPS catabolism act specifically on R-DHPS and S-DHPS, respectively. R-DHPS is also a substrate for the dehydrogenase HpsN. All three dehydrogenases generate stable hydrogen bonds between the chirality-center hydroxyls of DHPS and highly conserved residues, and HpsP also form coordinate-covalent bonds between the chirality-center hydroxyls and Zn2+, which determines the mechanistic basis of strict stereoselectivity. We further illustrated the role of enzymatic promiscuity in the evolution of DHPS metabolism in Roseobacteraceae and SAR11. This study provides the first evidence of chirality's involvement in phytoplankton-bacteria metabolic currencies, opening a new avenue for understanding the ocean organosulfur cycle.
手性是物质的基本属性之一，但在海洋有机物质循环的研究中往往被忽视。二羟丙磺酸(DHPS)是一种在全球范围内广泛存在的有机硫化合物，是海洋中从浮游植物到细菌的营养和能量转移的重要生态货币。然而，DHPS 的手性及其转化在自然界中仍不清楚。在这里，我们开发了一种使用手性磷试剂标记来分离 DHPS 对映体的新方法。我们的研究结果表明，DHPS 的至少一种对映体存在于海洋硅藻和颗石藻中，并且两种对映体在海洋环境中广泛存在。在海洋玫瑰杆菌科菌株中发现了一种新的手性选择性 DHPS 代谢途径，其中 DHPS 代谢途径的 HpsO 和 HpsP 脱氢酶分别特异性作用于 R-DHPS 和 S-DHPS。R-DHPS 也是脱氢酶 HpsN 的底物。这三种脱氢酶在 DHPS 的手性中心羟基和高度保守残基之间形成稳定的氢键，而 HpsP 在手性中心羟基和 Zn2+ 之间也形成配位共价键，这决定了严格立体选择性的机制基础。我们进一步说明了酶的混杂性在玫瑰杆菌科和 SAR11 中 DHPS 代谢进化中的作用。本研究首次提供了手性参与浮游植物-细菌代谢货币的证据，为理解海洋有机硫循环开辟了新的途径。
