Radical-mediated C-S bond cleavage in C2 sulfonate degradation by anaerobic bacteria

Xing, Meining; Wei, Yifeng; Zhou, Yan; Zhang, Jun; Lin, Lei; Hu, Yiling; Hua, Gaoqun; Urs, Ankanahalli N. Nanjaraj; Liu, Dazhi; Wang, Feifei; Guo, Cuixia; Yang, Ting; Li, Mengya; Liu, Yanhong; Ang, Ee Lui; Zhao, Huimin; Yuchi, Zhiguang; Zhang, Yan

doi:10.1038/s41467-019-09618-8

Cited by 49 publications

(70 citation statements)

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“…Notably, the SEC results indicate that wild‐type PhdB occurs as a functional homodimer in solution, as the molecular weight estimated by SEC was approximately 200 kDa and the calculated, sequence‐based value is 95.6 kDa (accounting for the N‐terminal GH scar; see Experimental Section). Other single‐subunit GREs that have been characterized also occur as homodimers …”

Section: Resultsmentioning

confidence: 99%

“…Phenylacetate decarboxylase (PhdB), which was recently discovered via activity‐guided metaproteomic studies of toluene‐producing microbial communities, has promise as a catalyst for first‐time biochemical synthesis of toluene from renewable resources. PhdB represents one of ten glycyl radical enzyme (GRE) reaction types that have been discovered to date, namely, pyruvate formate‐lyase (EC 2.3.1.54), anaerobic ribonucleotide reductase (EC 1.17.4.1), benzylsuccinate synthase (EC 4.1.99.11), p ‐hydroxyphenylacetate decarboxylase (EC 4.1.1.83), B 12 ‐independent glycerol (and propane‐1,2‐diol) dehydratase (EC 4.2.1.30), choline trimethylamine‐lyase (EC 4.3.99.4), and the very recently discovered (since 2017) trans ‐4‐hydroxy‐ l ‐proline dehydratase, phenylacetate decarboxylase, indoleacetate decarboxylase, and isethionate sulfite‐lyase …”

Section: Introductionmentioning

confidence: 99%

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Insight into the Mechanism of Phenylacetate Decarboxylase (PhdB), a Toluene‐Producing Glycyl Radical Enzyme

et al. 2019

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We recently reported the discovery of phenylacetate decarboxylase (PhdB), representing one of only ten glycyl‐radical‐enzyme reaction types known, and a promising biotechnological tool for first‐time biochemical synthesis of toluene from renewable resources. Here, we used experimental and computational data to evaluate the plausibility of three candidate PhdB mechanisms, involving either attack at the phenylacetate methylene carbon or carboxyl group [via H‐atom abstraction from COOH or single‐electron oxidation of COO− (Kolbe‐type decarboxylation)]. In vitro experimental data included assays with F‐labeled phenylacetate, kinetic studies, and tests with site‐directed PhdB mutants; computational data involved estimation of reaction energetics using density functional theory (DFT). The DFT results indicated that all three mechanisms are thermodynamically challenging (beyond the range of many known enzymes in terms of endergonicity or activation energy barrier), reflecting the formidable demands on PhdB for catalysis of this reaction. Evidence that PhdB was able to bind α,α‐difluorophenylacetate but was unable to catalyze its decarboxylation supported the enzyme's abstraction of a methylene H atom. Diminished activity of H327A and Y691F mutants was consistent with proposed proton donor roles for His327 and Tyr691. Collectively, these and other data most strongly support PhdB attack at the methylene carbon.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Insight into the Mechanism of Phenylacetate Decarboxylase (PhdB), a Toluene‐Producing Glycyl Radical Enzyme

et al. 2019

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“…Methionine catabolism to cysteine via the reverse transsulfuration pathway ( Fig. 2A) and the catabolism of organic sulfonates, notably taurine, are known to be catalyzed by gut microbiota (41,42,(68)(69)(70)(71)(72). This niche is also home to sulfate-reducing bacteria that are responsible for significant production of H 2 S (73,74), in addition to the reduction of tetrathionate and thiosulfate to H 2 S that also occurs in the gut (75).…”

Section: Physiological Conditions For the Production Regulation Andmentioning

confidence: 99%

“…Bacteria generally encode either 3MST or CBS/CSE, and it was recently demonstrated that L-cysteine desulfhydrases and cysteine desulfurases also contribute to H 2 S biogenesis in Escherichia coli (39,40). In addition, two groups recently reported the discovery of a glycyl radical enzyme from Bilophila wadsworthia that catalyzes C-S bond cleavage in the catabolism of tissueabundant taurine and the analogous alcohol isethionate (2hydroxyethanesulfonate) (41,42). This reaction produces sulfite (SO 2À 3 ), which is reduced to H 2 S by a dissimilatory sulfite reductase, thus defining a novel pathway for H 2 S production by gut microbiota.…”

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confidence: 99%

H2S and reactive sulfur signaling at the host-bacterial pathogen interface

Walsh

Giedroc

2020

Journal of Biological Chemistry

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Bacterial pathogens that cause invasive disease in the vertebrate host must adapt to host efforts to cripple their viability. Major host insults are reactive oxygen and reactive nitrogen species as well as cellular stress induced by antibiotics. Hydrogen sulfide (H2S) is emerging as an important player in cytoprotection against these stressors, which may well be attributed to downstream more oxidized sulfur species termed reactive sulfur species (RSS). In this review, we summarize recent work that suggests that H2S/RSS impacts bacterial survival in infected cells and animals. We discuss the mechanisms of biogenesis and clearance of RSS in the context of a bacterial H2S/RSS homeostasis model, and the bacterial transcriptional regulatory proteins that act as “sensors” of cellular RSS that maintain H2S/RSS homeostasis. In addition, we cover fluorescence imaging- and mass spectrometry-based approaches used to detect and quantify RSS in bacterial cells. Lastly, we discuss proteome persulfidation (S-sulfuration) as potential mediators of H2S/RSS signaling in bacteria in the context of the writer-reader-eraser paradigm, and progress toward ascribing regulatory significance to this widespread post-translational modification.

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“…The proposed reaction for IseD, NAD ϩ -dependent isethionate oxidation, is thermodynamically reversible and has been detected in vitro for several sulfoacetaldehyde reductases that function in various taurine degradation pathways. These include Klebsiella pneumoniae IsfD, belonging to the short-chain ADH family, and Bilophila wadsworthia SarD (9,13) and Bifidobacterium kashiwanohense TauF (14), belonging to the M-ADH family. IseD is distantly related to the two M-ADH enzymes (34.2% and 33.8% identity with SarD and TauF, respectively).…”

Section: Resultsmentioning

confidence: 99%

A Pathway for Isethionate Dissimilation in Bacillus krulwichiae

Yang

Wei

et al. 2019

Appl Environ Microbiol

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Hydroxyethyl sulfonate (isethionate) is widely distributed in the environment as an industrial pollutant and as a product of microbial metabolism. It is used as a substrate for growth by metabolically diverse environmental bacteria. Aerobic pathways for isethionate dissimilation in Gram-negative bacteria involve the cytochrome c-dependent oxidation of isethionate to sulfoacetaldehyde by a membranebound flavoenzyme (IseJ), followed by C-S cleavage by the thiamine pyrophosphate (TPP)-dependent enzyme sulfoacetaldehyde acetyltransferase (Xsc). Here, we report a bioinformatics analysis of Xsc-containing gene clusters in Gram-positive bacteria, which revealed the presence of an alternative isethionate dissimilation pathway involving the NAD ϩ -dependent oxidation of isethionate by a cytosolic metal-dependent alcohol dehydrogenase (IseD). We describe the biochemical characterization of recombinant IseD from the haloalkaliphilic environmental bacterium Bacillus krulwichiae AM31D T and demonstrate the growth of this bacterium using isethionate as its sole carbon source, with the excretion of sulfite as a waste product. The IseD-dependent pathway provides the only mechanism for isethionate dissimilation in Gram-positive species to date and suggests a role of the metabolically versatile Bacilli in the mineralization of this ubiquitous organosulfur compound. IMPORTANCE Isethionate of biotic and industrial sources is prevalent. Dissimilation of isethionate under aerobic conditions is thus far only known in Gram-negative bacteria. Here, we report the discovery of a new pathway in Gram-positive Bacillus krulwichiae. Isethionate is oxidized by a cytosolic metal-dependent alcohol dehydrogenase (which we named IseD), with NAD ϩ as the electron acceptor, generating sulfoacetaldehyde for subsequent cleavage by Xsc. This work highlights the diversity of organisms and pathways involved in the degradation of this ubiquitous organosulfonate. The new pathway that we discovered may play an important role in organosulfur mineralization and in the sulfur cycle in certain environments.

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Radical-mediated C-S bond cleavage in C2 sulfonate degradation by anaerobic bacteria

Cited by 49 publications

References 54 publications

Insight into the Mechanism of Phenylacetate Decarboxylase (PhdB), a Toluene‐Producing Glycyl Radical Enzyme

Insight into the Mechanism of Phenylacetate Decarboxylase (PhdB), a Toluene‐Producing Glycyl Radical Enzyme

H2S and reactive sulfur signaling at the host-bacterial pathogen interface

A Pathway for Isethionate Dissimilation in Bacillus krulwichiae

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