Dimethylsulfoniopropionate Sulfur and Methyl Carbon Assimilation in <italic toggle="yes">Ruegeria</italic> Species

ABSTRACT Dimethylsulfoniopropionate (DMSP) is abundant in marine environments and an important source of reduced carbon and sulfur for marine bacteria. While both Ruegeria pomeroyi and Ruegeria lacuscaerulensis possessed genes encoding the DMSP demethylation and cleavage pathways, their responses to...

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Autores principales:	Joseph S. Wirth, Tao Wang, Qiuyuan Huang, Robert H. White, William B. Whitman
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Ruegeria cysteine biosynthesis dimethylsulfoniopropionate isotope labeling methanethiol methionine Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/f8e5f34321164ab6a1074cbbeb44ffc5
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spelling	oai:doaj.org-article:f8e5f34321164ab6a1074cbbeb44ffc52021-11-15T15:57:02ZDimethylsulfoniopropionate Sulfur and Methyl Carbon Assimilation in <italic toggle="yes">Ruegeria</italic> Species10.1128/mBio.00329-202150-7511https://doaj.org/article/f8e5f34321164ab6a1074cbbeb44ffc52020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00329-20https://doaj.org/toc/2150-7511ABSTRACT Dimethylsulfoniopropionate (DMSP) is abundant in marine environments and an important source of reduced carbon and sulfur for marine bacteria. While both Ruegeria pomeroyi and Ruegeria lacuscaerulensis possessed genes encoding the DMSP demethylation and cleavage pathways, their responses to DMSP differed. A glucose-fed, chemostat culture of R. pomeroyi consumed 99% of the DMSP even when fed a high concentration of 5 mM. At the same time, cultures released 19% and 7.1% of the DMSP as dimethylsulfide (DMS) and methanethiol, respectively. Under the same conditions, R. lacuscaerulensis consumed only 28% of the DMSP and formed one-third of the amount of gases. To examine the pathways of sulfur and methyl C assimilation, glucose-fed chemostats of both species were fed 100 μM mixtures of unlabeled and doubly labeled [dimethyl-13C, 34S]DMSP. Both species derived nearly all of their sulfur from DMSP despite high sulfate availability. In addition, only 33% and 50% of the methionine was biosynthesized from the direct capture of methanethiol in R. pomeroyi and R. lacuscaerulensis, respectively. The remaining methionine was biosynthesized by the random assembly of free sulfide and methyl-tetrahydrofolate derived from DMSP. Thus, although the two species possessed similar genes encoding DMSP metabolism, their growth responses were very different. IMPORTANCE Dimethylsulfoniopropionate (DMSP) is abundant in marine environments and an important source of reduced carbon and sulfur for marine bacteria. DMSP is the precursor for the majority of atmospheric dimethylsulfide (DMS), a climatically active gas that connects the marine and terrestrial sulfur cycles. Although research into the assimilation of DMSP has been conducted for over 20 years, the fate of DMSP in microbial biomass is not well understood. In particular, the biosynthesis of methionine from DMSP has been a focal point, and it has been widely believed that most methionine was synthesized via the direct capture of methanethiol. Using an isotopic labeling strategy, we have demonstrated that the direct capture of methanethiol is not the primary pathway used for methionine biosynthesis in two Ruegeria species, a genus comprised primarily of globally abundant marine bacteria. Furthermore, although the catabolism of DMSP by these species varied greatly, the anabolic pathways were highly conserved.Joseph S. WirthTao WangQiuyuan HuangRobert H. WhiteWilliam B. WhitmanAmerican Society for MicrobiologyarticleRuegeriacysteine biosynthesisdimethylsulfoniopropionateisotope labelingmethanethiolmethionineMicrobiologyQR1-502ENmBio, Vol 11, Iss 2 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Ruegeria cysteine biosynthesis dimethylsulfoniopropionate isotope labeling methanethiol methionine Microbiology QR1-502
spellingShingle	Ruegeria cysteine biosynthesis dimethylsulfoniopropionate isotope labeling methanethiol methionine Microbiology QR1-502 Joseph S. Wirth Tao Wang Qiuyuan Huang Robert H. White William B. Whitman Dimethylsulfoniopropionate Sulfur and Methyl Carbon Assimilation in <italic toggle="yes">Ruegeria</italic> Species
description	ABSTRACT Dimethylsulfoniopropionate (DMSP) is abundant in marine environments and an important source of reduced carbon and sulfur for marine bacteria. While both Ruegeria pomeroyi and Ruegeria lacuscaerulensis possessed genes encoding the DMSP demethylation and cleavage pathways, their responses to DMSP differed. A glucose-fed, chemostat culture of R. pomeroyi consumed 99% of the DMSP even when fed a high concentration of 5 mM. At the same time, cultures released 19% and 7.1% of the DMSP as dimethylsulfide (DMS) and methanethiol, respectively. Under the same conditions, R. lacuscaerulensis consumed only 28% of the DMSP and formed one-third of the amount of gases. To examine the pathways of sulfur and methyl C assimilation, glucose-fed chemostats of both species were fed 100 μM mixtures of unlabeled and doubly labeled [dimethyl-13C, 34S]DMSP. Both species derived nearly all of their sulfur from DMSP despite high sulfate availability. In addition, only 33% and 50% of the methionine was biosynthesized from the direct capture of methanethiol in R. pomeroyi and R. lacuscaerulensis, respectively. The remaining methionine was biosynthesized by the random assembly of free sulfide and methyl-tetrahydrofolate derived from DMSP. Thus, although the two species possessed similar genes encoding DMSP metabolism, their growth responses were very different. IMPORTANCE Dimethylsulfoniopropionate (DMSP) is abundant in marine environments and an important source of reduced carbon and sulfur for marine bacteria. DMSP is the precursor for the majority of atmospheric dimethylsulfide (DMS), a climatically active gas that connects the marine and terrestrial sulfur cycles. Although research into the assimilation of DMSP has been conducted for over 20 years, the fate of DMSP in microbial biomass is not well understood. In particular, the biosynthesis of methionine from DMSP has been a focal point, and it has been widely believed that most methionine was synthesized via the direct capture of methanethiol. Using an isotopic labeling strategy, we have demonstrated that the direct capture of methanethiol is not the primary pathway used for methionine biosynthesis in two Ruegeria species, a genus comprised primarily of globally abundant marine bacteria. Furthermore, although the catabolism of DMSP by these species varied greatly, the anabolic pathways were highly conserved.
format	article
author	Joseph S. Wirth Tao Wang Qiuyuan Huang Robert H. White William B. Whitman
author_facet	Joseph S. Wirth Tao Wang Qiuyuan Huang Robert H. White William B. Whitman
author_sort	Joseph S. Wirth
title	Dimethylsulfoniopropionate Sulfur and Methyl Carbon Assimilation in <italic toggle="yes">Ruegeria</italic> Species
title_short	Dimethylsulfoniopropionate Sulfur and Methyl Carbon Assimilation in <italic toggle="yes">Ruegeria</italic> Species
title_full	Dimethylsulfoniopropionate Sulfur and Methyl Carbon Assimilation in <italic toggle="yes">Ruegeria</italic> Species
title_fullStr	Dimethylsulfoniopropionate Sulfur and Methyl Carbon Assimilation in <italic toggle="yes">Ruegeria</italic> Species
title_full_unstemmed	Dimethylsulfoniopropionate Sulfur and Methyl Carbon Assimilation in <italic toggle="yes">Ruegeria</italic> Species
title_sort	dimethylsulfoniopropionate sulfur and methyl carbon assimilation in <italic toggle="yes">ruegeria</italic> species
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/f8e5f34321164ab6a1074cbbeb44ffc5
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Dimethylsulfoniopropionate Sulfur and Methyl Carbon Assimilation in <italic toggle="yes">Ruegeria</italic> Species

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