A subfamily classification to choreograph the diverse activities within glycoside hydrolase family 31

Arumapperuma, Thimali; Li, Jinling; Hornung, Bastian; Soler, Niccolay Madiedo; Goddard‐Borger, Ethan D.; Terrapon, Nicolas; Williams, Spencer J.

doi:10.1016/j.jbc.2023.103038

Cited by 8 publications

(11 citation statements)

References 62 publications

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“…This indicates that PsGal31A may have independently acquired the tryptophan residue at a different position, suggesting that GH31 a-galactosidases have diversified during evolution. This is consistent with GH31_14 being phylogenetically distant from GH31_19, while GH31_19 and GH31_20 are sister subfamilies with a closely related common ancestor [24]. The structural differences in the subsite +1 that determine their substrate specificity are associated with the evolutionary divergence between GH31_19 and GH31_20.…”

Section: Discussionsupporting

confidence: 77%

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Structure–function analysis of bacterial GH31 α‐galactosidases specific for α‐(1→4)‐galactobiose

2023

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Glycoside hydrolase family 31 (GH31) contains α‐glycoside hydrolases with different substrate specificities involved in various physiological functions. This family has recently been classified into 20 subfamilies using sequence similarity networks. An α‐galactosidase from the gut bacterium Bacteroides salyersiae (BsGH31_19, which belongs to GH31 subfamily 19) was reported to have hydrolytic activity against the synthetic substrate p‐ nitrophenyl α‐galactopyranoside, but its natural substrate remained unknown. BsGH31_19 shares low sequence identity (around 20%) with other reported GH31 α‐galactosidases, PsGal31A from Pseudopedobacter saltans and human myogenesis‐regulating glycosidase (MYORG), and was expected to have distinct specificity. Here, we characterized BsGH31_19 and its ortholog from a soil Bacteroidota bacterium, Flavihumibacter petaseus (FpGH31_19), and demonstrated that they showed high substrate specificity against α‐(1→4)‐linkages in α‐(1→4)‐galactobiose and globotriose [α‐Gal‐(1→4)‐β‐Gal‐(1→4)‐Glc], unlike PsGal31A and MYORG. The crystallographic analyses of BsGH31_19 and FpGH31_19 showed that their overall structures resemble those of MYORG and form a dimer with an interface different from that of PsGal31A and MYORG dimers. The structures of FpGH31_19 complexed with d‐galactose and α‐(1→4)‐galactobiose revealed that amino acid residues that recognize a galactose residue at subsite +1 are not conserved between FpGH31_19 and BsGH31_19. The tryptophan (Trp153) that recognizes galactose at subsite −1 is homologous to the tryptophan residues in MYORG and α‐galactosidases belonging to GH27, GH36, and GH97, but not in the bacterial GH31 member PsGal31A. Our results provide structural insights into molecular diversity and evolutionary relationships in the GH31 α‐galactosidase subfamilies and the other α‐galactosidase families.

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Section: Discussionsupporting

confidence: 77%

“…They include not only a-glucosidases [16,17] but also a-xylosidases [18], a-galactosidases [19], sulfoquinovosidases [20], and a-N-acetylgalactosaminidases [21][22][23]. Due to the extensive diversity and large number of GH31 members, this family has recently been classified into 20 subfamilies using sequence similarity networks [24].…”

Section: Introductionmentioning

confidence: 99%

Structure–function analysis of bacterial GH31 α‐galactosidases specific for α‐(1→4)‐galactobiose

2023

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“…13,14 It forms a subfamily of the carbohydrate active enzyme (CAZy) family of glycoside hydrolase 31 (GH31). 16 Bioinformatic studies have shown that gene clusters encoding sulfoglycolytic and sulfolytic SQ degradation pathways often include genes encoding family GH31 SQases. 15 However, some organisms harboring SQ degradation pathways lack GH31 SQases, 6,17 raising questions as to how such organisms can utilize SQ glycosides.…”

Section: ■ Introductionmentioning

confidence: 99%

“…To date, only one class of SQase has been identified. , It forms a subfamily of the carbohydrate active enzyme (CAZy) family of glycoside hydrolase 31 (GH31) . Bioinformatic studies have shown that gene clusters encoding sulfoglycolytic and sulfolytic SQ degradation pathways often include genes encoding family GH31 SQases .…”

Section: Introductionmentioning

confidence: 99%

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

Kaur,

Pickles,

Sharma

et al. 2023

J. Am. Chem. Soc.

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“…GH family 31 (GH31) is a large glycoside hydrolase family with >20,000 members that possess diverse activities on α-glycosidic bonds including α-glucosidase, α-glucan lyase, α-xylanase and sulfoquinovosidases (SQases). 3 SQases catalyze hydrolysis of glycosides of sulfoquinovose (SQ; 6deoxy-6-sulfo-glucose), 4,5 such as in the ubiquitous plant sulfolipid α-sulfoquinovosyl diacylglyceride (SQDG). SQDG is produced by essentially all photosynthetic organisms, and is one of the most abundant organosulfur compounds in nature.…”

Section: Introductionmentioning

confidence: 99%

A broad-spectrum α-glucosidase of glycoside hydrolase family 13 fromMarinovumsp., a member of theRoseobacterclade

Mui

Silva

et al. 2023

Preprint

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Glycoside hydrolases (GHs) are a diverse group of enzymes that catalyze the hydrolysis of glycosidic bonds. The Carbohydrate-Active enZymes (CAZy) database organizes GHs into families based on sequence data and function, with fewer than 1% of the predicted proteins characterized biochemically. Consideration of genomic context can provide a useful guide to infer possible enzyme activities for proteins of unknown function. We used the MultiGeneBLAST tool to discover a putative gene cluster inMarinovumsp., a member of the marineRoseobacterclade, that encodes homologues of enzymes belonging to the sulfoquinovose monooxygenase pathway. This putative gene cluster lacks a gene encoding a classical family GH31 sulfoquinovosidase (SQase) candidate, but which instead includes an uncharacterized family GH13 protein (MsGH13). We show that recombinantMsGH13 lacks SQase activity but is a broad spectrum α-glucosidase active on a diverse array of α-linked disaccharides, including: maltose (100%), sucrose (7.9%), nigerose (52%), trehalose (20%), isomaltose (6.4%), and kojibiose (3.8%). Using AlphaFold, a 3D model for the MsGH13 enzyme was constructed that predicted its active site shared close similarity with a narrower specificity α-glucosidase fromHalomonassp. H11 of the same GH13 subfamily. This study supports recent findings that bacteria belonging to theRoseobacterclade can metabolize SQ without a classical SQase encoded in their genomes.

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A subfamily classification to choreograph the diverse activities within glycoside hydrolase family 31

Cited by 8 publications

References 62 publications

Structure–function analysis of bacterial GH31 α‐galactosidases specific for α‐(1→4)‐galactobiose

Structure–function analysis of bacterial GH31 α‐galactosidases specific for α‐(1→4)‐galactobiose

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

A broad-spectrum α-glucosidase of glycoside hydrolase family 13 fromMarinovumsp., a member of theRoseobacterclade

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A subfamily classification to choreograph the diverse activities within glycoside hydrolase family 31

Cited by 8 publications

References 62 publications

Structure–function analysis of bacterial GH31 α‐galactosidases specific for α‐(1→4)‐galactobiose

Structure–function analysis of bacterial GH31 α‐galactosidases specific for α‐(1→4)‐galactobiose

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

A broad-spectrum α-glucosidase of glycoside hydrolase family 13 fromMarinovumsp., a member of theRoseobacterclade

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