Insights into methionine S-methylation in diverse organisms

Peng, Ming; Li, Chun-Yang; Chen, Xiu-Lan; Williams, Beth T.; Li, Kang; Gao, Yanan; Wang, Peng; Wang, Ning; Gao, Chao; Zhang, Shan; Schoelmerich, Marie Charlotte; Banfield, Jillian F.; Miller, J. Benjamin; Brun, Nick E. Le; Todd, Jonathan D.; Zhang, Yuzhong

doi:10.1038/s41467-022-30491-5

Cited by 14 publications

(9 citation statements)

References 60 publications

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“…To conclude, DMSP is an abundant organosulfur compound in the ocean, and plays important roles in marine stress responses, microbial food webs and the global sulfur and carbon cycling. Despite some bacteria producing DMSP themselves [4,[54][55][56], the uptake of DMSP is the prerequisite for most marine bacterial utilisation. Here, we identified an efficient ABC-type transporter DmpXWV, which is specific for DMSP and prevalent in numerous cosmopolitan marine bacteria.…”

Section: Discussionmentioning

confidence: 99%

Ubiquitous occurrence of a dimethylsulfoniopropionate ABC transporter in abundant marine bacteria

Mausz

Murphy

et al. 2023

The ISME Journal

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Dimethylsulfoniopropionate (DMSP) is a ubiquitous organosulfur compound in marine environments with important functions in both microorganisms and global biogeochemical carbon and sulfur cycling. The SAR11 clade and marine Roseobacter group (MRG) represent two major groups of heterotrophic bacteria in Earth’s surface oceans, which can accumulate DMSP to high millimolar intracellular concentrations. However, few studies have investigated how SAR11 and MRG bacteria import DMSP. Here, through comparative genomics analyses, genetic manipulations, and biochemical analyses, we identified an ABC (ATP-binding cassette)-type DMSP-specific transporter, DmpXWV, in Ruegeria pomeroyi DSS-3, a model strain of the MRG. Mutagenesis suggested that DmpXWV is a key transporter responsible for DMSP uptake in strain DSS-3. DmpX, the substrate binding protein of DmpXWV, had high specificity and binding affinity towards DMSP. Furthermore, the DmpX DMSP-binding mechanism was elucidated from structural analysis. DmpX proteins are prevalent in the numerous cosmopolitan marine bacteria outside the SAR11 clade and the MRG, and dmpX transcription was consistently high across Earth’s entire global ocean. Therefore, DmpXWV likely enables pelagic marine bacteria to efficiently import DMSP from seawater. This study offers a new understanding of DMSP transport into marine bacteria and provides novel insights into the environmental adaption of marine bacteria.

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Section: Discussionmentioning

confidence: 99%

Ubiquitous occurrence of a dimethylsulfoniopropionate ABC transporter in abundant marine bacteria

Mausz

Murphy

et al. 2023

The ISME Journal

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“…115,116 Besides the aforementioned methyl donors, S-methyl-Lmethionine (SMM) can also serve as the methyl donor to remethylate L-homocysteine to L-methionine (Figure 4B). 37,117 However, because the formation of SMM itself is dependent on either L-methionine or SAM, 118 this route does not seem attractive in developing SdNP MCFs. The halide methyltransferase (HMT) has also been used in the in vitro enzymatic cascades of SAM recycle.…”

Section: Acetyl-coa and Othersmentioning

confidence: 99%

Improving Microbial Cell Factory Performance by Engineering SAM Availability

Lv,

Chang,

Zhang

et al. 2024

J. Agric. Food Chem.

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Methylated natural products are widely spread in nature. S-Adenosyl-L-methionine (SAM) is the secondary abundant cofactor and the primary methyl donor, which confer natural products with structural and functional diversification. The increasing demand for SAM-dependent natural products (SdNPs) has motivated the development of microbial cell factories (MCFs) for sustainable and efficient SdNP production. Insufficient and unsustainable SAM availability hinders the improvement of SdNP MCF performance. From the perspective of developing MCF, this review summarized recent understanding of de novo SAM biosynthesis and its regulatory mechanism. SAM is just the methyl mediator but not the original methyl source. Effective and sustainable methyl source supply is critical for efficient SdNP production. We compared and discussed the innate and relatively less explored alternative methyl sources and identified the one involving cheap one-carbon compound as more promising. The SAM biosynthesis is synergistically regulated on multilevels and is tightly connected with ATP and NAD(P)H pools. We also covered the recent advancement of metabolic engineering in improving intracellular SAM availability and SdNP production. Dynamic regulation is a promising strategy to achieve accurate and dynamic fine-tuning of intracellular SAM pool size. Finally, we discussed the design and engineering constraints underlying construction of SAM-responsive genetic circuits and envisioned their future applications in developing SdNP MCFs.

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“…The optimal temperature of DsyGD was determined by incubating the reaction mixture at 10, 15, 20, 25, 30, 40, 50 and 60℃ with MTHB and monitoring MSM activity. The optimal pH of DsyGD was determined by incubating the reaction mixture with MTHB in Britton-Robinson buffer at 25℃ at pH 4, 5, 6, 7, 8, 9, and 10, as performed in [71] and assaying MSM activity. The kinetic parameters of DsyGD for MSM and DDC activity were determined by nonlinear analysis based on the initial rates determined with 5-1000 μM MTHB, 0-250 μM SAM or 500-3000 μM DMSHB at the optimal temperature and pH, as described in [8] .…”

Section: In Vitro Msm Ddc and Mtob Reductase Enzyme Assaysmentioning

confidence: 99%

Novel dimethylsulfoniopropionate biosynthesis enzymes in diverse marine bacteria, cyanobacteria and abundant algae

Wang

Zhou

Curson

et al. 2023

Preprint

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Dimethylsulfoniopropionate (DMSP) is an abundant marine organosulfur compound[1] with roles in stress protection[2, 3], chemotaxis[4], nutrient and sulfur cycling[5] and, potentially, climate regulation[6, 7]. Marine algae and bacteria are considered significant DMSP producers, but many diverse representatives lack known DMSP synthesis genes/enzymes[8, 9]. Here, new DMSP biosynthesis enzymes were identified that considerably increase the number and diversity of potential DMSP-producing organisms, inferring new and significant global DMSP producers. A novel bifunctional DMSP biosynthesis enzyme, DsyGD, identified in the rhizobacterium Gynuella sunshinyii, produces DMSP at levels higher than any other bacterium from methylthiohydroxybutyrate (MTHB) via an N-terminal MTHB S-methyltransferase domain (termed DsyG) and a C-terminal dimethylsulfoniohydroxybutyrate (DMSHB) decarboxylase domain (termed DsyD, which is the first reported enzyme with this activity). DsyGD is also found in some filamentous cyanobacteria, not previously known to produce DMSP. Regulation of DMSP production and dsyGD transcription was consistent with their role in osmoprotection. Indeed, cloned dsyGD conferred osmotolerance to bacteria deficient in osmolyte production, something not previously demonstrated for any known DMSP synthesis gene, and which could be exploited for biotechnology e.g., engineering salt tolerance. DsyGD characterisation led to identification of phylogenetically distinct DsyG-like proteins, termed DSYE, with MTHB S-methyltransferase activity, in diverse and environmentally abundant Chlorophyta, Chlorachniophyta, Ochraphyta, Haptophyta and Bacillariophyta algae. These algae comprise a mix of low, high and previously unknown DMSP producers[10]. Algae containing DSYE, particularly bloom-forming Pelagophyceae species, which we showed to accumulate medium-high intracellular DMSP levels, were globally more abundant DMSP producers than Haptophyta, Dinophyta and Bacillariophyta with DSYB and/or TpMMT. This highlights the potential importance of Pelagophyceae and other DSYE containing algae in global DMSP production and sulfur cycling.

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Insights into methionine S-methylation in diverse organisms

Cited by 14 publications

References 60 publications

Ubiquitous occurrence of a dimethylsulfoniopropionate ABC transporter in abundant marine bacteria

Ubiquitous occurrence of a dimethylsulfoniopropionate ABC transporter in abundant marine bacteria

Improving Microbial Cell Factory Performance by Engineering SAM Availability

Novel dimethylsulfoniopropionate biosynthesis enzymes in diverse marine bacteria, cyanobacteria and abundant algae

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