Identification of an Essential LolD-Like Protein in Helicobacter pylori

J Bacteriol. 2023 Apr 25;205(4):e0005223. doi: 10.1128/jb.00052-23. Epub 2023 Mar 27.

Abstract

The localization of lipoprotein (Lol) system is used by Gram-negative bacteria to export lipoproteins to the outer membrane. Lol proteins and models of how Lol transfers lipoproteins from the inner to the outer membrane have been extensively characterized in the model organism Escherichia coli, but in numerous bacterial species, lipoprotein synthesis and export pathways deviate from the E. coli paradigm. For example, in the human gastric bacterium Helicobacter pylori, a homolog of the E. coli outer membrane component LolB is not found, E. coli LolC and LolE correspond to a single inner membrane component (LolF), and a homolog of the E. coli cytoplasmic ATPase LolD has not been identified. In the present study, we sought to identify a LolD-like protein in H. pylori. We used affinity-purification mass spectrometry to identify interaction partners of the H. pylori ATP-binding cassette (ABC) family permease LolF and identified the ABC family ATP-binding protein HP0179 as its interaction partner. We engineered H. pylori to conditionally express HP0179 and showed that HP0179 and its conserved ATP binding and ATP hydrolysis motifs are essential for H. pylori growth. We then performed affinity purification-mass spectrometry using HP0179 as the bait and identified LolF as its interaction partner. These results indicate that H. pylori HP0179 is a LolD-like protein and provide a more complete understanding of lipoprotein localization processes in H. pylori, a bacterium in which the Lol system deviates from the E. coli paradigm. IMPORTANCE Lipoproteins are critical in Gram-negative-bacteria for cell surface assembly of LPS, insertion of outer membrane proteins, and sensing envelope stress. Lipoproteins also contribute to bacterial pathogenesis. For many of these functions, lipoproteins must localize to the Gram-negative outer membrane. Transporting lipoproteins to the outer membrane involves the Lol sorting pathway. Detailed analyses of the Lol pathway have been performed in the model organism Escherichia coli, but many bacteria utilize altered components or are missing essential components of the E. coli Lol pathway. Identifying a LolD-like protein in Helicobacter pylori is important to better understand the Lol pathway in diverse bacterial classes. This becomes particularly relevant as lipoprotein localization is targeted for antimicrobial development.

Keywords: ATP-binding cassette; ATP-binding cassette transporters; ATP-binding proteins; Helicobacter pylori; affinity purification-mass spectrometry; lipoprotein; post-translational protein modification.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, N.I.H., Extramural

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Bacterial Outer Membrane Proteins / metabolism
  • Escherichia coli / metabolism
  • Escherichia coli Proteins* / metabolism
  • Gram-Negative Bacteria / metabolism
  • Helicobacter pylori* / genetics
  • Helicobacter pylori* / metabolism
  • Humans
  • Lipoproteins / genetics
  • Lipoproteins / metabolism
  • Protein Transport

Substances

  • Escherichia coli Proteins
  • Lipoproteins
  • Adenosine Triphosphate
  • Bacterial Outer Membrane Proteins