Genome sequences of Arthrobacter spp. that use a modified sulfoglycolytic Embden–Meyerhof–Parnas pathway

Abstract

Sulfoglycolysis pathways enable the breakdown of the sulfosugar sulfoquinovose and environmental recycling of its carbon and sulfur content. The prototypical sulfoglycolytic pathway is a variant of the classical Embden–Meyerhof–Parnas (EMP) pathway that results in formation of 2,3-dihydroxypropanesulfonate and was first described in gram-negative Escherichia coli. We used enrichment cultures to discover new sulfoglycolytic bacteria from Australian soil samples. Two gram-positive Arthrobacter spp. were isolated that produced sulfolactate as the metabolic end-product. Genome sequences identified a modified sulfoglycolytic EMP gene cluster, conserved across a range of other Actinobacteria, that retained the core sulfoglycolysis genes encoding metabolic enzymes but featured the replacement of the gene encoding sulfolactaldehyde (SLA) reductase with SLA dehydrogenase, and the absence of sulfoquinovosidase and sulfoquinovose mutarotase genes. Excretion of sulfolactate by these Arthrobacter spp. is consistent with an aerobic saprophytic lifestyle. This work broadens our knowledge of the sulfo-EMP pathway to include soil bacteria.

New mechanisms for bacterial degradation of sulfoquinovose

“…While the traditional approach to identification of new SQ degradation pathways has involved isolation and cultivation of SQ-degrading bacteria [ 1 , 15 , 19 , 20 , 29 ], recent research has relied heavily on bioinformatics analyses [ 20–22 ]. Several of the pathways (sulfo-TAL, sulfo-EMP2 and sulfo-TK) share enzymes in common (SqvB, SqvD), and the two non-orthologous sulfo-EMP(2) pathways contain isozymes that are frequently interchanged in different organisms [ 22 ].…”

“…Degradation of SQ through the sulfo-EMP pathway in Arthrobacter spp. and related Actinobacteria was recently reported, involving gene clusters encoding orthologs of YihS, YihV and YihT [ 29 ]. These bacteria lack close homologs of YihQ and YihR but are nevertheless able to utilize both free SQ and methyl α-sulfoquinovoside, suggesting the involvement of a non-specific sulfoquinovosidase.…”

“…( D ) Proposed catalytic scheme for SqiA. Both models were constructed using AlphaFold2 [ 29 ] in ColabFold [ 30 ]. The putative Mn 2+ site of SqvD and two putative Zn 2+ sites of SqiA were estimated by alignment with the crystal structures of E. coli FucI (PDB: 1FUI ) [ 28 ] and Helicobacter pylori class II fructose-1,6-biphosphate adolase (5UCK) [ 33 ], respectively.…”

Implications of hydrogen sulfide in colorectal cancer: Mechanistic insights and diagnostic and therapeutic strategies

“…In recent years, some advances have been made in the SQ metabolism (described as sulfoglycolysis) of microorganisms. A total of five pathways have been identified, including the sulfo-Embden-Meyerhof-Parnas (sulfo-EMP) pathway [ [ [29] , [30] , [31] , [32] , [33] ]], the sulfo-Entner-Doudoroff (sulfo-ED) pathway [ 34 , 35 ], the sulfo-sulfofructose transaldolase (sulfo-SFT; or named sulfo-transaldolase, sulfo-TAL) pathway [ 36 , 37 ], the sulfo-transketolase (sulfo-TK) pathway [ 33 ], and the sulfo-sulfoquinovose monooxygenase (sulfo-SMO; or named sulfo-alkanesulfonate monooxygenase, sulfo-ASMO) pathway [ 33 , 38 ]. Among them, the sulfo-SMO pathway allows for complete SQ metabolism and sulfite release, while the other pathways utilize only part of the carbons within the SQ skeleton ( Fig.…”

Widespread Family of NAD+-Dependent Sulfoquinovosidases at the Gateway to Sulfoquinovose Catabolism

“…soil bacteria that contain a sulfoglycolytic Embden−Meyerhof− Parnas (sulfo-EMP) pathway but lack a candidate GH31 SQase, yet grow robustly on the SQ glycoside methyl α-sulfoquinovoside (SQMe) as sole carbon source. 17 Here, we identify an alternative approach to sulfoquinovoside hydrolysis that is adopted by these organisms and discover a family of SQases belonging to a new glycoside hydrolase family (GH188). These new SQases operate through an oxidoreductive mechanism that results in net hydrolysis and involves a catalytic NAD + cofactor.…”