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Structural and biochemical insights into the function and evolution of sulfoquinovosidases

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Author(s)

  • Palika Abayakoon
  • Yi Jin
  • James P. Lingford
  • Marija Petricevic
  • Alan John
  • Eileen Ryan
  • Douglas E.V. Pires
  • David B. Ascher
  • Gideon J. Davies
  • Ethan D. Goddard-Borger
  • Spencer J. Williams

Department/unit(s)

Publication details

JournalACS Central Science
DateAccepted/In press - 23 Aug 2018
DateE-pub ahead of print - 5 Sep 2018
DatePublished (current) - 26 Sep 2018
Issue number9
Volume4
Number of pages8
Pages (from-to)1266–1273
Early online date5/09/18
Original languageEnglish

Abstract

An estimated 10 billion tonnes of sulfoquinovose (SQ) are produced and degraded each year. Prokaryotic sulfoglycolytic pathways catabolize sulfoquinovose (SQ) liberated from plant sulfolipid, or its delipidated form α-d-sulfoquinovosyl glycerol (SQGro), through the action of a sulfoquinovosidase (SQase), but little is known about the capacity of SQ glycosides to support growth. Structural studies of the first reported SQase (Escherichia coli YihQ) have identified three conserved residues that are essential for substrate recognition, but crossover mutations exploring active-site residues of predicted SQases from other organisms have yielded inactive mutants casting doubt on bioinformatic functional assignment. Here, we show that SQGro can support the growth of E. coli on par with d-glucose, and that the E. coli SQase prefers the naturally occurring diastereomer of SQGro. A predicted, but divergent, SQase from Agrobacterium tumefaciens proved to have highly specific activity toward SQ glycosides, and structural, mutagenic, and bioinformatic analyses revealed the molecular coevolution of catalytically important amino acid pairs directly involved in substrate recognition, as well as structurally important pairs distal to the active site. Understanding the defining features of SQases empowers bioinformatic approaches for mapping sulfur metabolism in diverse microbial communities and sheds light on this poorly understood arm of the biosulfur cycle.

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