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Structure and Function of ArnD. A Deformylase Essential for Lipid A Modification with 4-Amino-4-deoxy-l-arabinose and Polymyxin Resistance

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논문

Structure and Function of ArnD. A Deformylase Essential for Lipid A Modification with 4-Amino-4-deoxy-l-arabinose and Polymyxin Resistance

학술지

Biochemistry

저자명

Muñ oz-Escudero, Daniel; Breazeale, Steven D.; Lee, Myeongseon; Guan, Ziqiang; Raetz, Christian R. H.; Sousa, Marcelo C.

초록

<P>Covalent modification of lipid A with 4-deoxy-4-amino-<SMALL>L</SMALL>-arabinose (Ara4N) mediates resistance to cationic antimicrobial peptides and polymyxin antibiotics in Gram-negative bacteria. The proteins required for Ara4N biosynthesis are encoded in the <I>pmrE</I> and <I>arnBCADTEF</I> loci, with ArnT ultimately transferring the amino sugar from undecaprenyl-phospho-4-deoxy-4-amino-<SMALL>L</SMALL>-arabinose (C55P-Ara4N) to lipid A. However, Ara4N is N-formylated prior to its transfer to undecaprenyl-phosphate by ArnC, requiring a deformylase activity downstream in the pathway to generate the final C55P-Ara4N donor. Here, we show that deletion of the <I>arnD</I> gene in an <I>Escherichia coli</I> mutant that constitutively expresses the <I>arnBCADTEF</I> operon leads to accumulation of the formylated ArnC product undecaprenyl-phospho-4-deoxy-4-formamido-<SMALL>L</SMALL>-arabinose (C55P-Ara4FN), suggesting that ArnD is the downstream deformylase. Purification of <I>Salmonella typhimurium</I> ArnD (stArnD) shows that it is membrane-associated. We present the crystal structure of stArnD revealing a NodB homology domain structure characteristic of the metal-dependent carbohydrate esterase family 4 (CE4). However, ArnD displays several distinct features: a 44 amino acid insertion, a C-terminal extension in the NodB fold, and sequence divergence in the five motifs that define the CE4 family, suggesting that ArnD represents a new family of carbohydrate esterases. The insertion is responsible for membrane association as its deletion results in a soluble ArnD variant. The active site retains a metal coordination H-H-D triad, and in the presence of Co<SUP>2+</SUP> or Mn<SUP>2+</SUP>, purified stArnD efficiently deformylates C55P-Ara4FN confirming its role in Ara4N biosynthesis. Mutations D9N and H233Y completely inactivate stArnD implicating these two residues in a metal-assisted acid-base catalytic mechanism.</P><BR>[FIG OMISSION]</BR>

발행연도

2023

발행기관

American Chemical Society

ISSN

0006-2960

ISSN

1520-4995

62

20

페이지

pp.2970-2981

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1 2023-12-11
2 2023-12-11

논문; 2023-10-17

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