Sulfoquinovose degradation in bacteria

Sulfoquinovose (SQ, 6-deoxy-6-sulfoglucose) has been known for 50 years as the polar headgroup of the plant sulfolipid (Benson 1963, Benning 2007) in the photosynthetic membranes of all higher plants, mosses, ferns, algae, and most photosynthetic bacteria (Benning 1998). It is also found in some non-photosynthetic bacteria (Harwood and Nicholls 1979), and SQ is part of the surface layer of some Archaea (Meyer et al. 2011). The estimated annual production of SQ (Harwood and Nicholls 1979) is 10,000,000,000 tones (10 petagrams), thus it comprises a major portion of the organo-sulfur in nature, where SQ is degraded by bacteria (Martelli 1967, Roy et al. 2003). However, despite evidence for at least three different degradative pathways in bacteria (Martelli 1967, Roy et al. 2003, Denger et al. 2012), no enzymic reaction or gene in any pathway has been defined, although a sulfoglycolytic pathway has been proposed (Roy et al. 2003). Here we show that Escherichia coli K-12, the most widely studied prokaryotic model organism, performs sulfoglycolysis, in addition to standard glycolysis. SQ is catabolized through four newly discovered reactions that we established using purified, heterologously expressed enzymes: SQ isomerase, 6-deoxy-6-sulfofructose (SF) kinase, 6-deoxy-6sulfofructose-1-phosphate (SFP) aldolase, and 3-sulfolactaldehyde (SLA) reductase. The enzymes are encoded in a ten-gene cluster, which probably also encodes regulation, transport and degradation of the whole sulfolipid; the gene cluster is present in almost all (>91%) available E. coli genomes, and is widespread in Enterobacteriaceae. The pathway yields dihydroxyacetone phosphate (DHAP), which powers energy conservation and growth of E. coli, and the sulfonate product 2,3-dihydroxypropane-1-sulfonate (DHPS), which is excreted. DHPS is mineralized by other bacteria, thus closing the sulfur cycle within a bacterial community. INTRODUCTION, RESULTS, AND DISCUSSION Recent work showed that environmental isolates of Klebsiella spp. (Enterobacteriaceae) convert SQ quantitatively to DHPS (Roy et al. 2003, Denger et al. 2012), and we hypothesized that utilization of SQ might be a property of Enterobacteriaceae. We found that four genome-sequenced E. coli K-12 substrains (BW25113, DH1, MG1655 and W3100), after subculturing, grew with SQ within 1 to 3 days. We chose to work (largely) with the fastest-growing substrain, MG1655. The organism used SQ as a sole source of carbon and energy with a molar-growth yield of 3 g of protein per mol of SQ carbon, whereas glucose gave about 6 g of protein per mol of carbon; the latter value represented mass balance of