Anaerobic Faecalicatena spp. degrade sulfoquinovose via a bifurcated 6-deoxy-6-sulfofructose transketolase/transaldolase pathway to both C2- and C3-sulfonate intermediates
Plant-produced sulfoquinovose (SQ, 6-deoxy-6-sulfoglucose) is one of the most abundant sulfur-containing compounds in nature and its bacterial degradation plays an important role in the biogeochemical sulfur and carbon cycles and in all habitats where SQ is produced and degraded, particularly in gut...
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Frontiers Media S.A.
2024-12-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2024.1491101/full |
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| author | Sabrina Borusak Sabrina Borusak Sabrina Borusak Karin Denger Till Dorendorf Till Dorendorf Corentin Fournier Corentin Fournier Harry Lerner Harry Lerner Olga Mayans Olga Mayans Dieter Spiteller Dieter Spiteller David Schleheck David Schleheck David Schleheck |
| author_facet | Sabrina Borusak Sabrina Borusak Sabrina Borusak Karin Denger Till Dorendorf Till Dorendorf Corentin Fournier Corentin Fournier Harry Lerner Harry Lerner Olga Mayans Olga Mayans Dieter Spiteller Dieter Spiteller David Schleheck David Schleheck David Schleheck |
| author_sort | Sabrina Borusak |
| collection | DOAJ |
| description | Plant-produced sulfoquinovose (SQ, 6-deoxy-6-sulfoglucose) is one of the most abundant sulfur-containing compounds in nature and its bacterial degradation plays an important role in the biogeochemical sulfur and carbon cycles and in all habitats where SQ is produced and degraded, particularly in gut microbiomes. Here, we report the enrichment and characterization of a strictly anaerobic SQ-degrading bacterial consortium that produces the C2-sulfonate isethionate (ISE) as the major product but also the C3-sulfonate 2,3-dihydroxypropanesulfonate (DHPS), with concomitant production of acetate and hydrogen (H2). In the second step, the ISE was degraded completely to hydrogen sulfide (H2S) when an additional electron donor (external H2) was supplied to the consortium. Through growth experiments, analytical chemistry, genomics, proteomics, and transcriptomics, we found evidence for a combination of the 6-deoxy-6-sulfofructose (SF) transketolase (sulfo-TK) and SF transaldolase (sulfo-TAL) pathways in a SQ-degrading Faecalicatena-phylotype (family Lachnospiraceae) of the consortium, and for the ISE-desulfonating glycyl-radical enzyme pathway, as described for Bilophila wadsworthia, in an Anaerospora-phylotype (Sporomusaceae). Furthermore, using total proteomics, a new gene cluster for a bifurcated SQ pathway was also detected in Faecalicatena sp. DSM22707, which grew with SQ in pure culture, producing mainly ISE, but also 3-sulfolacate (SL) 3-sulfolacaldehyde (SLA), acetate, butyrate, succinate, and formate, but not H2. We then reproduced the growth of the consortium with SQ in a defined co-culture model consisting of Faecalicatena sp. DSM22707 and Bilophila wadsworthia 3.1.6. Our findings provide the first description of an additional sulfoglycolytic, bifurcated SQ pathway. Furthermore, we expand on the knowledge of sulfidogenic SQ degradation by strictly anaerobic co-cultures, comprising SQ-fermenting bacteria and cross-feeding of the sulfonate intermediate to H2S-producing organisms, a process in gut microbiomes that is relevant for human health and disease. |
| format | Article |
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| publishDate | 2024-12-01 |
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| spelling | doaj-art-d20fb788f82948f88a7a0885df3fdc7e2025-08-20T02:36:10ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2024-12-011510.3389/fmicb.2024.14911011491101Anaerobic Faecalicatena spp. degrade sulfoquinovose via a bifurcated 6-deoxy-6-sulfofructose transketolase/transaldolase pathway to both C2- and C3-sulfonate intermediatesSabrina Borusak0Sabrina Borusak1Sabrina Borusak2Karin Denger3Till Dorendorf4Till Dorendorf5Corentin Fournier6Corentin Fournier7Harry Lerner8Harry Lerner9Olga Mayans10Olga Mayans11Dieter Spiteller12Dieter Spiteller13David Schleheck14David Schleheck15David Schleheck16Department of Biology, University of Konstanz, Konstanz, GermanyThe Konstanz Research School Chemical Biology, University of Konstanz, Konstanz, GermanyDepartment of Biology, Limnological Institute, University of Konstanz, Konstanz, GermanyDepartment of Biology, University of Konstanz, Konstanz, GermanyDepartment of Biology, University of Konstanz, Konstanz, GermanyThe Konstanz Research School Chemical Biology, University of Konstanz, Konstanz, GermanyDepartment of Biology, University of Konstanz, Konstanz, GermanyDepartment of Biology, Limnological Institute, University of Konstanz, Konstanz, GermanyDepartment of Biology, University of Konstanz, Konstanz, GermanyDepartment of Biology, Limnological Institute, University of Konstanz, Konstanz, GermanyDepartment of Biology, University of Konstanz, Konstanz, GermanyThe Konstanz Research School Chemical Biology, University of Konstanz, Konstanz, GermanyDepartment of Biology, University of Konstanz, Konstanz, GermanyThe Konstanz Research School Chemical Biology, University of Konstanz, Konstanz, GermanyDepartment of Biology, University of Konstanz, Konstanz, GermanyThe Konstanz Research School Chemical Biology, University of Konstanz, Konstanz, GermanyDepartment of Biology, Limnological Institute, University of Konstanz, Konstanz, GermanyPlant-produced sulfoquinovose (SQ, 6-deoxy-6-sulfoglucose) is one of the most abundant sulfur-containing compounds in nature and its bacterial degradation plays an important role in the biogeochemical sulfur and carbon cycles and in all habitats where SQ is produced and degraded, particularly in gut microbiomes. Here, we report the enrichment and characterization of a strictly anaerobic SQ-degrading bacterial consortium that produces the C2-sulfonate isethionate (ISE) as the major product but also the C3-sulfonate 2,3-dihydroxypropanesulfonate (DHPS), with concomitant production of acetate and hydrogen (H2). In the second step, the ISE was degraded completely to hydrogen sulfide (H2S) when an additional electron donor (external H2) was supplied to the consortium. Through growth experiments, analytical chemistry, genomics, proteomics, and transcriptomics, we found evidence for a combination of the 6-deoxy-6-sulfofructose (SF) transketolase (sulfo-TK) and SF transaldolase (sulfo-TAL) pathways in a SQ-degrading Faecalicatena-phylotype (family Lachnospiraceae) of the consortium, and for the ISE-desulfonating glycyl-radical enzyme pathway, as described for Bilophila wadsworthia, in an Anaerospora-phylotype (Sporomusaceae). Furthermore, using total proteomics, a new gene cluster for a bifurcated SQ pathway was also detected in Faecalicatena sp. DSM22707, which grew with SQ in pure culture, producing mainly ISE, but also 3-sulfolacate (SL) 3-sulfolacaldehyde (SLA), acetate, butyrate, succinate, and formate, but not H2. We then reproduced the growth of the consortium with SQ in a defined co-culture model consisting of Faecalicatena sp. DSM22707 and Bilophila wadsworthia 3.1.6. Our findings provide the first description of an additional sulfoglycolytic, bifurcated SQ pathway. Furthermore, we expand on the knowledge of sulfidogenic SQ degradation by strictly anaerobic co-cultures, comprising SQ-fermenting bacteria and cross-feeding of the sulfonate intermediate to H2S-producing organisms, a process in gut microbiomes that is relevant for human health and disease.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1491101/fullanaerobic microbial metabolismcarbon and sulfur cycleisethionate3-sulfolactaldehyde6-deoxy-6-sulfofructose transaldolasetransketolase |
| spellingShingle | Sabrina Borusak Sabrina Borusak Sabrina Borusak Karin Denger Till Dorendorf Till Dorendorf Corentin Fournier Corentin Fournier Harry Lerner Harry Lerner Olga Mayans Olga Mayans Dieter Spiteller Dieter Spiteller David Schleheck David Schleheck David Schleheck Anaerobic Faecalicatena spp. degrade sulfoquinovose via a bifurcated 6-deoxy-6-sulfofructose transketolase/transaldolase pathway to both C2- and C3-sulfonate intermediates Frontiers in Microbiology anaerobic microbial metabolism carbon and sulfur cycle isethionate 3-sulfolactaldehyde 6-deoxy-6-sulfofructose transaldolase transketolase |
| title | Anaerobic Faecalicatena spp. degrade sulfoquinovose via a bifurcated 6-deoxy-6-sulfofructose transketolase/transaldolase pathway to both C2- and C3-sulfonate intermediates |
| title_full | Anaerobic Faecalicatena spp. degrade sulfoquinovose via a bifurcated 6-deoxy-6-sulfofructose transketolase/transaldolase pathway to both C2- and C3-sulfonate intermediates |
| title_fullStr | Anaerobic Faecalicatena spp. degrade sulfoquinovose via a bifurcated 6-deoxy-6-sulfofructose transketolase/transaldolase pathway to both C2- and C3-sulfonate intermediates |
| title_full_unstemmed | Anaerobic Faecalicatena spp. degrade sulfoquinovose via a bifurcated 6-deoxy-6-sulfofructose transketolase/transaldolase pathway to both C2- and C3-sulfonate intermediates |
| title_short | Anaerobic Faecalicatena spp. degrade sulfoquinovose via a bifurcated 6-deoxy-6-sulfofructose transketolase/transaldolase pathway to both C2- and C3-sulfonate intermediates |
| title_sort | anaerobic faecalicatena spp degrade sulfoquinovose via a bifurcated 6 deoxy 6 sulfofructose transketolase transaldolase pathway to both c2 and c3 sulfonate intermediates |
| topic | anaerobic microbial metabolism carbon and sulfur cycle isethionate 3-sulfolactaldehyde 6-deoxy-6-sulfofructose transaldolase transketolase |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2024.1491101/full |
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