Journal Article

Sulphoglycolysis in Escherichia coli K-12 closes a gap in the biogeochemical sulphur cycle

Spiteller, Dieter, Denger, Karin, Schneider, Alexander, Huhn, Thomas, Cook, Alasdair M., Mayer, Christoph, Schleheck, David, Weiss, Michael, Felux, Ann-Katrin

2014

Overview

Escherichia coli K-12 performs sulphoglycolysis; heterologous expression of enzymes encoded in a ten-gene cluster present in almost all (>91%) available E. coli genomes is used to show that sulphoquinovose is catabolised through four reactions to produce dihydroxyacetone phosphate, which powers energy conservation and growth, and a sulphonate product, which is excreted. Sulphoglycolysis as well as glycolysis in E. coli The monosaccharide sugar sulphoquinovose is a major component of the biological sulphur cycle, distributed widely in photosynthetic membranes and also in some non-photosynthetic bacteria and archaea. There is evidence for three different degradative pathways for sulphoquinovose in bacteria, but until now none had been fully characterized. This study shows that Escherichia coli K-12, the most widely-studied prokaryotic model organism, can perform sulphoglycolysis as well as standard glycolysis. A ten-gene cluster encodes all the enzymes needed to degrade sulphoquinovose to dihydroxyacetone phosphate. The same gene cluster is present in almost all available E. coli genomes and is widespread among the Enterobacteriaceae. The authors suggest that this newly defined pathway may represent a substantial part of the biogeochemical sulphur cycle, and may have a significant role in bacteria in the alimentary tract of all omnivores and herbivores, and in plant pathogens. Sulphoquinovose (SQ, 6-deoxy-6-sulphoglucose) has been known for 50 years as the polar headgroup of the plant sulpholipid 1 , 2 in the photosynthetic membranes of all higher plants, mosses, ferns, algae and most photosynthetic bacteria 3 . It is also found in some non-photosynthetic bacteria 4 , and SQ is part of the surface layer of some Archaea 5 . The estimated annual production of SQ 4 is 10,000,000,000 tonnes (10 petagrams), thus it comprises a major portion of the organo-sulphur in nature, where SQ is degraded by bacteria 6 , 7 . However, despite evidence for at least three different degradative pathways in bacteria 6 , 7 , 8 , no enzymic reaction or gene in any pathway has been defined, although a sulphoglycolytic pathway has been proposed 7 . Here we show that Escherichia coli K-12, the most widely studied prokaryotic model organism, performs sulphoglycolysis, in addition to standard glycolysis. SQ is catabolised through four newly discovered reactions that we established using purified, heterologously expressed enzymes: SQ isomerase, 6-deoxy-6-sulphofructose (SF) kinase, 6-deoxy-6-sulphofructose-1-phosphate (SFP) aldolase, and 3-sulpholactaldehyde (SLA) reductase. The enzymes are encoded in a ten-gene cluster, which probably also encodes regulation, transport and degradation of the whole sulpholipid; 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 sulphonate product 2,3-dihydroxypropane-1-sulphonate (DHPS), which is excreted. DHPS is mineralized by other bacteria, thus closing the sulphur cycle within a bacterial community.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 38 / 631/326/47 / 82 / 82/29 / 82/58 / 82/80 / 82/83 / Aldehyde-Lyases - genetics / Aldehyde-Lyases - metabolism / Algae / Alkanesulfonates - metabolism / Bacteria / Biological Transport / Carbon / Dehydrogenases / Dihydroxyacetone Phosphate - metabolism / E coli / Energy conservation / Enterobacteriaceae - enzymology / Enterobacteriaceae - genetics / Enzymes / Escherichia coli K12 - enzymology / Escherichia coli K12 - genetics / Escherichia coli K12 - growth & development / Escherichia coli K12 - metabolism / Escherichia coli Proteins - genetics / Escherichia coli Proteins - metabolism / Ferns / Genes / Genes, Bacterial - genetics / Genomes / Glucose / Glycolysis - genetics / Humanities and Social Sciences / Isomerases - genetics / Isomerases - metabolism / Kinases / letter / Methylglucosides - metabolism / multidisciplinary / Multigene Family - genetics / Oxidoreductases - genetics / Oxidoreductases - metabolism / Phosphotransferases - genetics / Phosphotransferases - metabolism / Proteins / Science / Sulfur - metabolism