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Journal Articles Applied Microbiology and Biotechnology Year : 2023

Unique alcohol dehydrogenases involved in algal sugar utilization by marine bacteria

Stefan Brott
Ki Hyun Nam
Theresa Dutschei
Lukas Reisky
Maike Behrens
Hanna Grimm
Gurvan Michel
Thomas Schweder
Uwe Bornscheuer

Abstract

Abstract Marine algae produce complex polysaccharides, which can be degraded by marine heterotrophic bacteria utilizing carbohydrate-active enzymes. The red algal polysaccharide porphyran contains the methoxy sugar 6- O -methyl- d -galactose (G6Me). In the degradation of porphyran, oxidative demethylation of this monosaccharide towards d -galactose and formaldehyde occurs, which is catalyzed by a cytochrome P450 monooxygenase and its redox partners. In direct proximity to the genes encoding for the key enzymes of this oxidative demethylation, genes encoding for zinc-dependent alcohol dehydrogenases (ADHs) were identified, which seem to be conserved in porphyran utilizing marine Flavobacteriia . Considering the fact that dehydrogenases could play an auxiliary role in carbohydrate degradation, we aimed to elucidate the physiological role of these marine ADHs. Although our results reveal that the ADHs are not involved in formaldehyde detoxification, a knockout of the ADH gene causes a dramatic growth defect of Zobellia galactanivorans with G6Me as a substrate. This indicates that the ADH is required for G6Me utilization. Complete biochemical characterizations of the ADHs from Formosa agariphila KMM 3901 T (FoADH) and Z. galactanivorans Dsij T (ZoADH) were performed, and the substrate screening revealed that these enzymes preferentially convert aromatic aldehydes. Additionally, we elucidated the crystal structures of FoADH and ZoADH in complex with NAD + and showed that the strict substrate specificity of these new auxiliary enzymes is based on a narrow active site. Key points • Knockout of the ADH-encoding gene revealed its role in 6-O-methyl-D-galactose utilization, suggesting a new auxiliary activity in marine carbohydrate degradation. • Complete enzyme characterization indicated no function in a subsequent reaction of the oxidative demethylation, such as formaldehyde detoxification. • These marine ADHs preferentially convert aromatic compounds, and their strict substrate specificity is based on a narrow active site.
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Dates and versions

hal-04234624 , version 1 (10-10-2023)

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Stefan Brott, Ki Hyun Nam, François Thomas, Theresa Dutschei, Lukas Reisky, et al.. Unique alcohol dehydrogenases involved in algal sugar utilization by marine bacteria. Applied Microbiology and Biotechnology, 2023, 107 (7-8), pp.2363-2384. ⟨10.1007/s00253-023-12447-x⟩. ⟨hal-04234624⟩
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