Abstract
Sulfoquinovose (SQ, 6-deoxy-6-sulfoglucose) is produced by plants and other phototrophs and its biodegradation is a relevant component of the biogeochemical carbon and sulfur cycles. SQ is known to be degraded by aerobic bacterial consortia in two tiers via C3-organosulfonates as transient intermediates to CO2, water and sulfate. In this study, we present a first laboratory model for anaerobic degradation of SQ by bacterial consortia in two tiers to acetate and hydrogen sulfide (H2S). For the first tier, SQ-degrading Escherichia coli K-12 was used. It catalyzes the fermentation of SQ to 2,3-dihydroxypropane-1-sulfonate (DHPS), succinate, acetate and formate, thus, a novel type of mixed-acid fermentation. It employs the characterized SQ Embden-Meyerhof-Parnas pathway, as confirmed by mutational and proteomic analyses. For the second tier, a DHPS-degrading Desulfovibrio sp. isolate from anaerobic sewage sludge was used, strain DF1. It catalyzes another novel fermentation, of the DHPS to acetate and H2S. Its DHPS desulfonation pathway was identified by differential proteomics and demonstrated by heterologously produced enzymes: DHPS is oxidized via 3-sulfolactaldehyde to 3-sulfolactate (SL) by two NAD+-dependent dehydrogenases (DhpA, SlaB); the SL is cleaved by an SL sulfite-lyase known from aerobic bacteria (SuyAB) to pyruvate and sulfite. The pyruvate is oxidized to acetate, while the sulfite is used as electron acceptor in respiration and reduced to H2S. In conclusion, anaerobic sulfidogenic SQ degradation was demonstrated as a novel link in the biogeochemical sulfur cycle. SQ is also a constituent of the green-vegetable diet of herbivores and omnivores and H2S production in the intestinal microbiome has many recognized and potential contributions to human health and disease. Hence, it is important to examine bacterial SQ degradation also in the human intestinal microbiome, in relation to H2S production, dietary conditions and human health.
Highlights
Sulfoquinovose (6-deoxy-6-sulfoglucose; SQ) is the polar headgroup of plant sulfolipids in the photosynthetic membranes of, essentially, all higher plants, ferns, mosses, algae as well as most phototrophic bacteria (Benson et al, 1959; Benson, 1963); SQ is a component of the cell wall of archaea (Palmieri et al, 2013)
We cultivated E. coli K-12 MG1655 routinely under fermentative conditions with SQ in a carbonate-buffered mineral salts medium in the presence of Ti(III)NTA as reducing agent instead of Na2S, in order to allow for a co-cultivation of Desulfovibrio sp. and for a quantification of H2S production during DHPS degradation
We confirmed the involvement of the SQ Embden-Meyerhof-Parnas (SQ-EMP) pathway in E. coli K-12 during fermentative growth with SQ
Summary
Sulfoquinovose (6-deoxy-6-sulfoglucose; SQ) is the polar headgroup of plant sulfolipids (sulfoquinovosyl diacylglycerols; SQDGs) in the photosynthetic (thylakoid) membranes of, essentially, all higher plants, ferns, mosses, algae as well as most phototrophic bacteria (Benson et al, 1959; Benson, 1963); SQ is a component of the cell wall of archaea (Palmieri et al, 2013). All genes in E. coli required for this pathway are encoded in one gene cluster, which is a core feature of commensal and pathogenic E. coli species (Denger et al, 2014), together with an α-glucosidase gene (yihQ) for a hydrolysis of the SQ-glycoside (Speciale et al, 2016), an aldose epimerase gene (yihR) for an interconversion of the SQ epimers (Abayakoon et al, 2017) and an SQ-responsive DoeR-family repressor gene (yihW/csqR) (Shimada et al, 2018) This SQ Embden-Meyerhof-Parnas (SQ-EMP) pathway has been identified for aerobic growth of E. coli K-12 (Denger et al, 2014), but the potential of E. coli to utilize SQ for anaerobic, fermentative growth has not yet been explored. SLA is produced and not further degraded (not desulfonated), but the SLA is oxidized by an NAD+-dependent dehydrogenase to 3-sulfolactate (SL), rather than reduced to DHPS as with E. coli K-12, prior to excretion of the SL
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