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Front. Microbiol. | doi: 10.3389/fmicb.2018.02792

Anaerobic degradation of the plant sugar sulfoquinovose concomitant with H2S production: Escherichia coli K-12 and Desulfovibrio sp. strain DF1 as co-culture model

Anna Burrichter1, Karin Denger1,  Paolo Franchini1, Thomas Huhn1, Nicolai Müller1, Dieter Spiteller1 and  David Schleheck1, 2*
  • 1Universität Konstanz, Germany
  • 2Fachbereich Biologie, Mathematisch Naturwissenschaftliche Sektion, Universität Konstanz, Germany

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.

Keywords: anaerobic bacterial metabolism, sulfidogenesis, Hydrogen sulfide production, organosulfonate respiration, Sulfoquinovosyldiacylglycerol, Plant sulfolipid, biogeochemical carbon and sulfur cycle, gut microbiome, human health and disease

Received: 24 Aug 2018; Accepted: 30 Oct 2018.

Edited by:

Christiane Dahl, Universität Bonn, Germany

Reviewed by:

Jonathan D. Todd, University of East Anglia, United Kingdom
Jochen A. Mueller, Helmholtz-Zentrum für Umweltforschung, Helmholtz-Gemeinschaft Deutscher Forschungszentren (HZ), Germany
Silke Leimkuehler, Universität Potsdam, Germany  

Copyright: © 2018 Burrichter, Denger, Franchini, Huhn, Müller, Spiteller and Schleheck. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. David Schleheck, Universität Konstanz, Konstanz, Germany, david.schleheck@uni-konstanz.de