Molecular basis of sulfolactate synthesis by sulfolactaldehyde dehydrogenase from Rhizobium leguminosarum
Molecular basis of sulfolactate synthesis by sulfolactaldehyde dehydrogenase from Rhizobium leguminosarum
Sulfolactate (SL) is a short-chain organosulfonate that is an important reservoir of sulfur in the biosphere. SL is produced by oxidation of sulfolactaldehyde (SLA), which in turn derives from sulfoglycolysis of the sulfosugar sulfoquinovose, or through oxidation of 2,3-dihydroxypropanesulfonate. Oxidation of SLA is catalyzed by SLA dehydrogenases belonging to the aldehyde dehydrogenase superfamily. We report that SLA dehydrogenase RlGabD from the sulfoglycolytic bacterium Rhizobium leguminsarum SRDI565 can use both NAD+ and NADP+ as cofactor to oxidize SLA, and indicatively operates through a rapid equilibrium ordered mechanism. We report the cryo-EM structure of RlGabD bound to NADH, revealing a tetrameric quaternary structure and supporting proposal of organosulfonate binding residues in the active site, and a catalytic mechanism. Sequence based homology searches identified SLA dehydrogenase homologs in a range of putative sulfoglycolytic gene clusters in bacteria predominantly from the phyla Actinobacteria, Firmicutes, and Proteobacteria. This work provides a structural and biochemical view of SLA dehydrogenases to complement our knowledge of SLA reductases, and provide detailed insights into a critical step in the organosulfur cycle.
11429-11440
Li, Jinling
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Sharma, Mahima
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Meek, Richard
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Alhifthi, Amani
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Armstrong, Zachary
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Soler, Niccolay Madiedo
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Lee, Mihwa
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Goddard-Borger, Ethan D.
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Blaza, James N.
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Davies, Gideon J.
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Williams, Spencer J.
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25 September 2023
Li, Jinling
25e5b88c-5f23-45b9-a238-70268030cb7a
Sharma, Mahima
50f9a3ac-ca58-4d3f-ba1b-8e9ea270af46
Meek, Richard
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Alhifthi, Amani
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Armstrong, Zachary
91223858-b123-4ce3-97d1-9d3e9a1a0faf
Soler, Niccolay Madiedo
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Lee, Mihwa
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Goddard-Borger, Ethan D.
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Blaza, James N.
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Davies, Gideon J.
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Williams, Spencer J.
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Li, Jinling, Sharma, Mahima, Meek, Richard, Alhifthi, Amani, Armstrong, Zachary, Soler, Niccolay Madiedo, Lee, Mihwa, Goddard-Borger, Ethan D., Blaza, James N., Davies, Gideon J. and Williams, Spencer J.
(2023)
Molecular basis of sulfolactate synthesis by sulfolactaldehyde dehydrogenase from Rhizobium leguminosarum.
Chemical Science, 14 (41), .
(doi:10.1039/d3sc01594g).
Abstract
Sulfolactate (SL) is a short-chain organosulfonate that is an important reservoir of sulfur in the biosphere. SL is produced by oxidation of sulfolactaldehyde (SLA), which in turn derives from sulfoglycolysis of the sulfosugar sulfoquinovose, or through oxidation of 2,3-dihydroxypropanesulfonate. Oxidation of SLA is catalyzed by SLA dehydrogenases belonging to the aldehyde dehydrogenase superfamily. We report that SLA dehydrogenase RlGabD from the sulfoglycolytic bacterium Rhizobium leguminsarum SRDI565 can use both NAD+ and NADP+ as cofactor to oxidize SLA, and indicatively operates through a rapid equilibrium ordered mechanism. We report the cryo-EM structure of RlGabD bound to NADH, revealing a tetrameric quaternary structure and supporting proposal of organosulfonate binding residues in the active site, and a catalytic mechanism. Sequence based homology searches identified SLA dehydrogenase homologs in a range of putative sulfoglycolytic gene clusters in bacteria predominantly from the phyla Actinobacteria, Firmicutes, and Proteobacteria. This work provides a structural and biochemical view of SLA dehydrogenases to complement our knowledge of SLA reductases, and provide detailed insights into a critical step in the organosulfur cycle.
Text
d3sc01594g
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Accepted/In Press date: 25 August 2023
e-pub ahead of print date: 25 September 2023
Published date: 25 September 2023
Additional Information:
Funding Information:
This work was supported by the Australian Research Council (DP210100233, DP210100235), the Biotechnology and Biological Sciences Research Council (BB/W003805/1), the UKRI Future Leader Fellowship Program (MR/T040742/1), and the Royal Society for the Ken Murray Research Professorship to G. J. D. and the associated PDRA funding (RP\EA\180016) for RWM. J. L. is supported by the China Scholarship Council. E. D. G.-B. acknowledges support from The Walter and Eliza Hall Institute of Medical Research, National Health and Medical Research Council of Australia (NHMRC) project grant GNT2000517, the Australian Cancer Research Fund, and the Brian M. Davis Charitable Foundation Centenary Fellowship. We thank the Wellcome Trust for funding the Glacios electron microscope (grant number 206161/Z/17/Z) and Dr Johan Turkenburg and Sam Hart for assistance with cryo-EM data collection. We acknowledge Dr Andrew Leech at the University of York Bioscience Technology Facility for assistance with SEC-MALLS analysis, and Arashdeep Kaur for assistance with bioinformatics.
Identifiers
Local EPrints ID: 484415
URI: http://eprints.soton.ac.uk/id/eprint/484415
ISSN: 2041-6520
PURE UUID: ee570034-e7a0-4896-a1e6-8cd903b547d8
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Date deposited: 16 Nov 2023 11:55
Last modified: 06 Jun 2024 02:16
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Contributors
Author:
Jinling Li
Author:
Mahima Sharma
Author:
Richard Meek
Author:
Amani Alhifthi
Author:
Zachary Armstrong
Author:
Niccolay Madiedo Soler
Author:
Mihwa Lee
Author:
Ethan D. Goddard-Borger
Author:
James N. Blaza
Author:
Gideon J. Davies
Author:
Spencer J. Williams
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