Environmental and Intestinal Phylum Firmicutes Bacteria Metabolize the Plant Sugar Sulfoquinovose via a 6-Deoxy-6-sulfofructose Transaldolase Pathway

Frommeyer, Benjamin; Fiedler, Alexander W.; Oehler, Sebastian; Hanson, Buck; Loy, Alexander; Franchini, Paolo; Spiteller, Dieter; Schleheck, David

doi:10.1016/j.isci.2020.101510

Cited by 52 publications

(66 citation statements)

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“…The sugar 6-deoxy-6-sulfoglucose (sulfoquinovose, SQ), which is produced by plants, algae, and cyanobacteria, is an important component of carbon and sulfur cycles ( Frommeyer et al, 2020 ). The microbial community can completely degrade SQ into inorganic sulfate or hydrogen sulfide through three pathways, i.e., sulfo-Embden-Meyerhof-Parnas (sulfo-EMP) ( Denger et al, 2014 ), sulfo-Entner-Doudoroff (sulfo-ED) ( Felux et al, 2015 ), and 6-deoxy-6-sulfofructose-transaldolase (SFT) pathways ( Frommeyer et al, 2020 ).…”

Section: Methodsmentioning

confidence: 99%

DiTing: A Pipeline to Infer and Compare Biogeochemical Pathways From Metagenomic and Metatranscriptomic Data

et al. 2021

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Metagenomics and metatranscriptomics are powerful methods to uncover key micro-organisms and processes driving biogeochemical cycling in natural ecosystems. Databases dedicated to depicting biogeochemical pathways (for example, metabolism of dimethylsulfoniopropionate (DMSP), which is an abundant organosulfur compound) from metagenomic/metatranscriptomic data are rarely seen. Additionally, a recognized normalization model to estimate the relative abundance and environmental importance of pathways from metagenomic and metatranscriptomic data has not been organized to date. These limitations impact the ability to accurately relate key microbial-driven biogeochemical processes to differences in environmental conditions. Thus, an easy-to-use, specialized tool that infers and visually compares the potential for biogeochemical processes, including DMSP cycling, is urgently required. To solve these issues, we developed DiTing, a tool wrapper to infer and compare biogeochemical pathways among a set of given metagenomic or metatranscriptomic reads in one step, based on the Kyoto Encyclopedia of Genes and Genomes (KEGG) and a manually created DMSP cycling gene database. Accurate and specific formulae for over 100 pathways were developed to calculate their relative abundance. Output reports detail the relative abundance of biogeochemical pathways in both text and graphical format. DiTing was applied to simulated metagenomic data and resulted in consistent genetic features of simulated benchmark genomic data. Subsequently, when applied to natural metagenomic and metatranscriptomic data from hydrothermal vents and the Tara Ocean project, the functional profiles predicted by DiTing were correlated with environmental condition changes. DiTing can now be confidently applied to wider metagenomic and metatranscriptomic datasets, and it is available at https://github.com/xuechunxu/DiTing.

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Section: Methodsmentioning

confidence: 99%

DiTing: A Pipeline to Infer and Compare Biogeochemical Pathways From Metagenomic and Metatranscriptomic Data

et al. 2021

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“… 4 SQDG is believed to primarily enter the environment through decomposition of photosynthetic tissues and herbivory, whereupon it becomes available to environmental and intestinal bacteria. 6 − 10 The catabolism of SQ, a process termed sulfoglycolysis, 6 − 8 is therefore of great relevance to understanding the biogeochemical sulfur cycle.…”

Section: Introductionmentioning

confidence: 99%

Molecular Basis of Sulfosugar Selectivity in Sulfoglycolysis

et al. 2021

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The sulfosugar sulfoquinovose (SQ) is produced by essentially all photosynthetic organisms on Earth and is metabolized by bacteria through the process of sulfoglycolysis. The sulfoglycolytic Embden–Meyerhof–Parnas pathway metabolizes SQ to produce dihydroxyacetone phosphate and sulfolactaldehyde and is analogous to the classical Embden–Meyerhof–Parnas glycolysis pathway for the metabolism of glucose-6-phosphate, though the former only provides one C3 fragment to central metabolism, with excretion of the other C3 fragment as dihydroxypropanesulfonate. Here, we report a comprehensive structural and biochemical analysis of the three core steps of sulfoglycolysis catalyzed by SQ isomerase, sulfofructose (SF) kinase, and sulfofructose-1-phosphate (SFP) aldolase. Our data show that despite the superficial similarity of this pathway to glycolysis, the sulfoglycolytic enzymes are specific for SQ metabolites and are not catalytically active on related metabolites from glycolytic pathways. This observation is rationalized by three-dimensional structures of each enzyme, which reveal the presence of conserved sulfonate binding pockets. We show that SQ isomerase acts preferentially on the β-anomer of SQ and reversibly produces both SF and sulforhamnose (SR), a previously unknown sugar that acts as a derepressor for the transcriptional repressor CsqR that regulates SQ-utilization. We also demonstrate that SF kinase is a key regulatory enzyme for the pathway that experiences complex modulation by the metabolites SQ, SLA, AMP, ADP, ATP, F6P, FBP, PEP, DHAP, and citrate, and we show that SFP aldolase reversibly synthesizes SFP. This body of work provides fresh insights into the mechanism, specificity, and regulation of sulfoglycolysis and has important implications for understanding how this biochemistry interfaces with central metabolism in prokaryotes to process this major repository of biogeochemical sulfur.

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“…In the second tier SL-and DHPS-utilizing bacteria release inorganic sulfur as sulfite. Three Tier 1 pathways have been described, the sulfoglycolytic Embden-Meyerhof-Parnas (sulfo-EMP) 3 , Entner-Doudoroff (sulfo-ED) 4,5 and sulfofructose transaldolase (sulfo-SFT) pathways 6,7 . Tier 2 metabolism has been described for various specialized bacteria that utilize SL or DHPS and perform 'biomineralization', releasing sulfur as sulfite, which under aerobic conditions can readily oxidize to sulfate 1 .…”

Section: Introductionmentioning

confidence: 99%

A microbial sulfoquinovose monooxygenase pathway that enables sulfosugar assimilation

Williams

Sharma

Lingford

et al. 2021

Preprint

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Breakdown of the sulfosugar sulfoquinovose (SQ, 6-deoxy-6-sulfoglucose), produced by photosynthetic organisms, is an important component of the biogeochemical carbon and sulfur cycles. Here, we reveal a new pathway for SQ degradation involving oxidative desulfurization to release sulfite and complete breakdown of the carbon skeleton of this sugar to support the growth of the plant pathogen Agrobacterium tumefaciens. SQ or its glycoside sulfoquinovosyl glycerol are imported by an ABC transporter system with associated SQ binding protein. A sulfoquinovosidase cleaves the SQ glycoside and a flavin mononucleotide-dependent sulfoquinovose monooxygenase acts in concert with an NADH-dependent flavin reductase to release sulfite and form 6-oxo-glucose. A short-chain dehydrogenase/reductase oxidoreductase reduces 6-oxo-glucose to glucose, allowing it to enter primary metabolism. Structural and biochemical studies provide detailed insights into the binding and recognition of key species along the reaction coordinate. This sulfoquinovose monooxygenase pathway is distributed across alphaproteobacteria and especially within the rhizobiales. This metabolic strategy...

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Environmental and Intestinal Phylum Firmicutes Bacteria Metabolize the Plant Sugar Sulfoquinovose via a 6-Deoxy-6-sulfofructose Transaldolase Pathway

Cited by 52 publications

References 50 publications

DiTing: A Pipeline to Infer and Compare Biogeochemical Pathways From Metagenomic and Metatranscriptomic Data

DiTing: A Pipeline to Infer and Compare Biogeochemical Pathways From Metagenomic and Metatranscriptomic Data

Molecular Basis of Sulfosugar Selectivity in Sulfoglycolysis

A microbial sulfoquinovose monooxygenase pathway that enables sulfosugar assimilation

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