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PreprintCited by 0Microbial metabolism and enzyme functionEnzyme Production and CharacterizationCarbohydrate Chemistry and Synthesis

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Tandem sulfofucolytic-sulfolactate sulfolyase pathway for catabolism of the rare sulfosugar sulfofucose

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Stewart, Adam W. E., Li, Jinling, Lee, Mihwa, Lewis, Jessica M., Herisse, Marion, Hofferek, Vinzenz, McConville, Malcolm J., Pidot, Sacha J., Scott, Nichollas E., Williams, Spencer J.·2023·mBio
DOI 10.1101/2023.08.01.551581PMC PMC12421959

Preprint — published as 10.1128/mbio.01840-25

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Abstract

The rare sulfosugar sulfofucose (6-deoxy-6-sulfo-D-galactose) is catabolized by Paracoccus wurundjeri sp. nov. strain Merri via a novel tandem pathway that couples sulfofucolytic and sulfolactate sulfolyase reactions. We isolated P. wurundjeri from soil and demonstrated its ability to utilize SFuc as the sole carbon source, leading to complete degradation of sulfofucose and release of sulfite. Proteomics and metabolomics analysis revealed a sulfofucolytic variant of the Entner–Doudoroff (ED) pathway, wherein sulfofucose is converted to sulfolactaldehyde through oxidation, lactone hydrolysis, dehydration and retro-aldol steps. The sulfolactaldehyde is subsequently degraded to pyruvate and sulfite via a downstream biomineralization pathway involving sulfolactate as an intermediate. In vitro reconstitution of the key enzymatic steps validated the pathway, identifying four enzymes: SfcH (dehydrogenase), SfcD (lactonase), SfcF (dehydratase), and SfcE (aldolase), that collectively convert sulfofucose to sulfolactaldehyde and pyruvate. Our findings provide insight into microbial utilization of rare sulfosugars and expand the known metabolic versatility of the genus Paracoccus . Importance: Sulfosugars, such as sulfoquinovose, are integral to the global sulfur cycle, but the metabolism of rarer sulfosugars, like sulfofucose, remains poorly understood. This study identifies a unique bacterial catabolic pathway for sulfofucose degradation, comprising a sulfofucolytic ED pathway followed by biomineralization to sulfite. The identification of this tandem pathway highlights the metabolic flexibility of bacteria to adapt carbohydrate catabolic pathways for processing structurally similar sulfosugars. This work sheds light on the ecological role of sulfofucose metabolism and broadens our understanding of bacterial sulfur metabolism, offering potential implications for biogeochemical sulfur cycling and biotechnological applications.

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Metadata

Authors
Stewart, A. W. E., Li, J., Lee, M., Lewis, J. M., Herisse, M., Hofferek, V., McConville, M. J., Pidot, S. J., Scott, N. E., & Williams, S. J.
Affiliations
The University of Melbourne (AU)
Corresponding author
Williams, Spencer J.
ORCID
Venue
mBio
Publisher
openRxiv
Published
2023-08-02
Volume
16
Issue
9
Pages
e0184025-e0184025
ISSN
2150-7511 (ISSN-L)
DOI
10.1101/2023.08.01.551581
PMC
PMC12421959
OpenAlex
W4413286229
Cited by
0
References
1
FWCI
0.00
Type
journal article
Language
en
Open access
Licence
Locations
  • mBio (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Minerva Access (University of Melbourne) (submittedVersion, cc-by)
Funders
  • Australian Nuclear Science and Technology Organisation
  • Australian Cancer Research Foundation
  • Australian Synchrotron
  • China Scholarship Council
  • Department of Education and Training (DP210100362, FT200100270, DP250100819, DP210100233, DP240100126, DP210100233, DP210100235, DP240100126, DP250100819, FT200100270, DP210100362, DP230102668, DP210100235)
  • Goddard Space Flight Center
  • Medical Research Council
  • Australian Research Council (DP210100233, DP210100362, FT200100270, DP230102668)
  • National Health and Medical Research Council (2021638)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial metabolism and enzyme function
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Enzyme Production and Characterization
  • Physical Sciences › Chemistry › Organic Chemistry › Carbohydrate Chemistry and Synthesis
Keywords
Entner-Doudoroff pathway, biomineralization, sulfur cycling, carbohydrate catabolism, enzyme reconstitution, lactonase, aldolase, dehydratase, dehydrogenase
MeSH terms
Bacterial Proteins, Soil Microbiology, Sulfites, Proteomics, Metabolic Networks and Pathways, Metabolomics

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