Oxidative desulfurization pathway for complete catabolism of sulfoquinovose by bacteria

Abstract

Catabolism of sulfoquinovose (SQ; 6-deoxy-6-sulfoglucose), the ubiquitous sulfosugar produced by photosynthetic organisms, is an important component of the biogeochemical carbon and sulfur cycles. Here, we describe a pathway for SQ degradation that involves oxidative desulfurization to release sulfite and enable utilization of the entire carbon skeleton of the sugar to support the growth of the plant pathogen Agrobacterium tumefaciens. SQ or its glycoside sulfoquinovosyl glycerol are imported into the cell by an ATP-binding cassette transporter system with an associated SQ binding protein. A sulfoquinovosidase hydrolyzes the SQ glycoside and the liberated SQ is acted on by a flavin mononucleotide-dependent sulfoquinovose monooxygenase, in concert with an NADH-dependent flavin reductase, to release sulfite and 6-oxo-glucose. An NAD(P)H-dependent oxidoreductase reduces the 6-oxo-glucose to glucose, enabling entry into primary metabolic pathways. Structural and biochemical studies provide detailed insights into the recognition of key metabolites by proteins in this pathway. Bioinformatic analyses reveal that the sulfoquinovose monooxygenase pathway is distributed across Alpha- and Betaproteobacteria and is especially prevalent within the Rhizobiales order. This strategy for SQ catabolism is distinct from previously described pathways because it enables the complete utilization of all carbons within SQ by a single organism with concomitant production of inorganic sulfite.

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

“…Both AK01 and AK04 contain genes annotated as ABC transporter cassettes and solute binding proteins. ABC transporter systems have been identified in Agrobacterium tumefaciens C58 (which uses the sulfo-SMO pathway) (Sharma et al 2022 ) and R. leguminosarum SRDI858 (which utilizes a sulfo-ED pathway) (Li et al 2020 ). The A. tumefaciens solute binding protein binds SQGro with high affinity (Sharma et al 2022 ).…”

“…ABC transporter systems have been identified in Agrobacterium tumefaciens C58 (which uses the sulfo-SMO pathway) (Sharma et al 2022 ) and R. leguminosarum SRDI858 (which utilizes a sulfo-ED pathway) (Li et al 2020 ). The A. tumefaciens solute binding protein binds SQGro with high affinity (Sharma et al 2022 ). We, therefore, propose that these Arthrobacter isolates utilize the solute binding protein and an ABC transporter system to import SQ or its glycosides.…”

“…The sulfoglycolytic sulfofructose transketolase (sulfo-TK) pathway uses four of the six carbons in primary metabolism while the last two are excreted as isethionate (Liu et al 2021 ). The sulfoglycolytic sulfoquinovose monooxygenase (sulfo-SMO) pathway results in cleavage of the C–S bond of sulfoquinovose and leads to production of glucose, and thus enables the complete breakdown of the SQ molecule (Liu et al 2021 ; Sharma et al 2022 ). The genes encoding these sulfoglycolytic pathways are found within clusters that typically contain genes encoding proteins for the import of SQ or its glycosides, the export of the end-products, SL or DHPS, and a specialized glycoside hydrolase termed a sulfoquinovosidase (SQase) (Speciale et al 2016 ; Abayakoon et al 2018a ; Liu et al 2021 ) that can cleave SQ glycosides to release SQ that can undergo sulfoglycolysis.…”

Formation of sulfoquinovosyl diacylglycerol by acylation of sulfoquinovosyl glycerol

“…SQDGs are very abundant lipids and promiscuous acyl hydrolases convert them sequentially to the metabolites lyso-SQDG and SQGro (Goddard-Borger and Williams, 2017). Recently, different pathways for degradation of sulfoquinovose and SQGro have been described (Sharma et al ., 2022) that allow to use these compounds as carbon and sulfur source. According to our results, environmental SQGro can also be used as a building block for the synthesis of the membrane lipid SQDG, in an analogous way as human GPC is used as building block for synthesis of PC (Joyce et al ., 2019).…”

“…SQDGs are very abundant lipids and promiscuous acyl hydrolases convert them sequentially to the metabolites lyso-SQDG and SQGro (Goddard-Borger and Williams, 2017). Recently, different pathways for degradation of sulfoquinovose and SQGro have been described (Sharma et al, 2022) that allow to use these compounds as carbon and sulfur source.…”