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Metabolism of chiral sulfonate compound 2,3-dihydroxypropane-1-sulfonate (DHPS) by Roseobacter bacteria in marine environment
Environment International ( IF 10.3 ) Pub Date : 2021-08-20 , DOI: 10.1016/j.envint.2021.106829
Xiaofeng Chen 1 , Le Liu 1 , Xiang Gao 2 , Xi Dai 1 , Yu Han 1 , Quanrui Chen 1 , Kai Tang 1
Affiliation  

The sulfonate compound 2,3-dihydroxypropane-1-sulfonate (DHPS) is one of the most abundant organic sulfur compounds in the biosphere. DHPS derived from dietary intake could be transformed into sulfide by intestinal microbiota and thus impacts human health. However, little is known about its sulfur transformation and subsequent impacts in marine environment. In this study, laboratory-culturing was combined with targeted metabolomic, chemical fluorescence probing, and comparative proteomic methods to examine the bioavailability of chiral DHPS (R and S isomers) for bacteria belonging to the marine Roseobacter clade. The metabolic potential of DHPS in bacteria was further assessed based on genomic analysis. Roseobacter members Ruegeria pomeroyi DSS-3, Dinoroseobacter shibae DFL 12, and Roseobacter denitrificans OCh 114 could utilize chiral DHPS for growth, producing sulfite. They all contained a similar gene cluster for DHPS metabolism but differed in the genes encoding enzymes for desulfonation. There was no significant difference in the growth rate and DHPS consumption rate for R. pomeroyi DSS-3 between R- and S-DHPS cultures, with few proteins expressed differentially were found. Proteomic data suggested that a series of hydrogenases oxidized DHPS, after which desulfonation could proceed via three distinct enzymatic pathways. Strain R. pomeroyi DSS-3 completed the desulfonation via L-cysteate sulfo-lyase, while D. shibae DFL 12 and R. denitrificans OCh 114 primarily utilized sulfolactate sulfo-lyase, and sulfopyruvate decarboxylase followed by sulfoacetaldehyde acetyltransferase, respectively, to complete desulfonation releasing the sulfonate-moiety. The sulfite could be further oxidized or incorporated into sulfate assimilation, indicated by the proteomic data. Furthermore, DHPS metabolic pathways were found primarily in marine bacterial groups, including the majority of sequenced Roseobacter genomes. Our results suggest that chiral DHPS, as a vital reduced sulfur reservoir, could be metabolized by marine bacteria, providing a resource for bacterial growth, rather than acting as a source of toxic sulfide within the marine ecosystem.



中文翻译:

海洋环境中玫瑰杆菌对手性磺酸盐化合物 2,3-二羟基丙烷-1-磺酸盐 (DHPS) 的代谢

磺酸盐化合物 2,3-二羟基丙烷-1-磺酸盐 (DHPS) 是生物圈中最丰富的有机硫化合物之一。膳食摄入的 DHPS 可以通过肠道微生物群转化为硫化物,从而影响人类健康。然而,人们对其硫的转化及其对海洋环境的后续影响知之甚少。在这项研究中,实验室培养与靶向代谢组学、化学荧光探测和比较蛋白质组学方法相结合,以检查属于海洋玫瑰杆菌进化枝的细菌的手性 DHPS(R 和 S 异构体)的生物利用度。基于基因组分析进一步评估了 DHPS 在细菌中的代谢潜力。Roseobacter成员Ruegeria pomeroyi DSS-3,Dinoroseobacter shibae DFL 12 和Roseobacter denitrificans OCh 114 可以利用手性 DHPS 进行生长,产生亚硫酸盐。它们都包含相似的 DHPS 代谢基因簇,但编码脱磺化酶的基因不同。R. pomeroyi DSS-3 在 R-DHPS 和 S-DHPS 培养物中的生长速率和 DHPS 消耗速率没有显着差异,几乎没有发现差异表达的蛋白质。蛋白质组学数据表明,一系列氢化酶氧化了 DHPS,然后可以通过三种不同的酶促途径进行脱磺化。菌株R. pomeroyi DSS-3 通过 L-半胱氨酸磺基裂解酶完成脱磺化,而D. shibae DFL 12 和R. denitrificansOCh 114 主要利用磺基乳酸磺基裂解酶和磺基丙酮酸脱羧酶,然后分别利用磺基乙醛乙酰转移酶来完成脱磺化,释放磺酸盐部分。蛋白质组学数据表明,亚硫酸盐可以进一步氧化或结合到硫酸盐同化中。此外,DHPS 代谢途径主要存在于海洋细菌群中,包括大多数已测序的玫瑰杆菌基因组。我们的研究结果表明,手性 DHPS 作为重要的还原硫储库,可以被海洋细菌代谢,为细菌生长提供资源,而不是在海洋生态系统中充当有毒硫化物的来源。

更新日期:2021-08-20
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