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Title: Ladderane phospholipids form a densely packed membrane with normal hydrazine and anomalously low proton/hydroxide permeability

Abstract

Ladderane lipids are unique to anaerobic ammonium-oxidizing (anammox) bacteria and are enriched in the membrane of the anammoxosome, an organelle thought to compartmentalize the anammox process, which involves the toxic intermediate hydrazine (N 2H 4). Due to the slow growth rate of anammox bacteria and difficulty of isolating pure ladderane lipids, experimental evidence of the biological function of ladderanes is lacking. We have synthesized two natural and one unnatural ladderane phosphatidylcholine lipids and compared their thermotropic properties in self-assembled bilayers to distinguish between [3]- and [5]-ladderane function. We then developed a hydrazine transmembrane diffusion assay using a water-soluble derivative of a hydrazine sensor and determined that ladderane membranes are as permeable to hydrazine as straight-chain lipid bilayers. However, pH equilibration across ladderane membranes occurs 5–10 times more slowly than across straight-chain lipid membranes. Langmuir monolayer analysis and the rates of fluorescence recovery after photobleaching suggest that dense ladderane packing may preclude formation of proton/hydroxide-conducting water wires. These data support the hypothesis that ladderanes prevent the breakdown of the proton motive force rather than blocking hydrazine transmembrane diffusion in anammox bacteria.

Authors:
 [1];  [1];  [1];  [1];  [2];  [1];  [1]
  1. Stanford Univ., CA (United States). Dept. of Chemistry
  2. SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
Publication Date:
Research Org.:
SLAC National Accelerator Lab., Menlo Park, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); National Institutes of Health (NIH); National Science Foundation (NSF)
OSTI Identifier:
1476321
Grant/Contract Number:  
AC02-76SF00515; GM069630; GM118044; P41GM103393; ECCS-1542152
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 115; Journal Issue: 37; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; ladderane; anammox; lipid bilayer; proton permeability; membrane structure

Citation Formats

Moss, Frank R., Shuken, Steven R., Mercer, Jaron A. M., Cohen, Carolyn M., Weiss, Thomas M., Boxer, Steven G., and Burns, Noah Z. Ladderane phospholipids form a densely packed membrane with normal hydrazine and anomalously low proton/hydroxide permeability. United States: N. p., 2018. Web. doi:10.1073/pnas.1810706115.
Moss, Frank R., Shuken, Steven R., Mercer, Jaron A. M., Cohen, Carolyn M., Weiss, Thomas M., Boxer, Steven G., & Burns, Noah Z. Ladderane phospholipids form a densely packed membrane with normal hydrazine and anomalously low proton/hydroxide permeability. United States. doi:10.1073/pnas.1810706115.
Moss, Frank R., Shuken, Steven R., Mercer, Jaron A. M., Cohen, Carolyn M., Weiss, Thomas M., Boxer, Steven G., and Burns, Noah Z. Mon . "Ladderane phospholipids form a densely packed membrane with normal hydrazine and anomalously low proton/hydroxide permeability". United States. doi:10.1073/pnas.1810706115. https://www.osti.gov/servlets/purl/1476321.
@article{osti_1476321,
title = {Ladderane phospholipids form a densely packed membrane with normal hydrazine and anomalously low proton/hydroxide permeability},
author = {Moss, Frank R. and Shuken, Steven R. and Mercer, Jaron A. M. and Cohen, Carolyn M. and Weiss, Thomas M. and Boxer, Steven G. and Burns, Noah Z.},
abstractNote = {Ladderane lipids are unique to anaerobic ammonium-oxidizing (anammox) bacteria and are enriched in the membrane of the anammoxosome, an organelle thought to compartmentalize the anammox process, which involves the toxic intermediate hydrazine (N2H4). Due to the slow growth rate of anammox bacteria and difficulty of isolating pure ladderane lipids, experimental evidence of the biological function of ladderanes is lacking. We have synthesized two natural and one unnatural ladderane phosphatidylcholine lipids and compared their thermotropic properties in self-assembled bilayers to distinguish between [3]- and [5]-ladderane function. We then developed a hydrazine transmembrane diffusion assay using a water-soluble derivative of a hydrazine sensor and determined that ladderane membranes are as permeable to hydrazine as straight-chain lipid bilayers. However, pH equilibration across ladderane membranes occurs 5–10 times more slowly than across straight-chain lipid membranes. Langmuir monolayer analysis and the rates of fluorescence recovery after photobleaching suggest that dense ladderane packing may preclude formation of proton/hydroxide-conducting water wires. These data support the hypothesis that ladderanes prevent the breakdown of the proton motive force rather than blocking hydrazine transmembrane diffusion in anammox bacteria.},
doi = {10.1073/pnas.1810706115},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
issn = {0027-8424},
number = 37,
volume = 115,
place = {United States},
year = {2018},
month = {8}
}

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Works referenced in this record:

Molecular mechanism of anaerobic ammonium oxidation
journal, October 2011

  • Kartal, Boran; Maalcke, Wouter J.; de Almeida, Naomi M.
  • Nature, Vol. 479, Issue 7371, p. 127-130
  • DOI: 10.1038/nature10453