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

Moss, Frank R.; Shuken, Steven R.; Mercer, Jaron A.  M.; Cohen, Carolyn M.; Weiss, Thomas M.; Boxer, Steven G.; Burns, Noah Z.

doi:10.1073/pnas.1810706115

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

Journal Article · Mon Aug 27 00:00:00 EDT 2018 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1810706115· OSTI ID:1476321

Moss, Frank R. ^[1]; Shuken, Steven R. ^[1]; Mercer, Jaron A. M. ^[1]; Cohen, Carolyn M. ^[1]; Weiss, Thomas M. ^[2]; Boxer, Steven G. ^[1]; Burns, Noah Z. ^[1]

Stanford Univ., CA (United States). Dept. of Chemistry
SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)

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.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: SLAC National Accelerator Lab., Menlo Park, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH); National Science Foundation (NSF)

Grant/Contract Number:: AC02-76SF00515; GM069630; GM118044; P41GM103393; ECCS-1542152

OSTI ID:: 1476321

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 115, Issue 37; ISSN 0027-8424

Publisher:: National Academy of Sciences, Washington, DC (United States)Copyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 37 works

Citation information provided by
Web of Science

References (46)

How to make a living from anaerobic ammonium oxidation Kartal, Boran; de Almeida, Naomi M.; Maalcke, Wouter J. FEMS Microbiology Reviews, Vol. 37, Issue 3 https://doi.org/10.1111/1574-6976.12014	journal	May 2013
Formation and properties of thin-walled phospholipid vesicles Reeves, John P.; Dowben, Robert M. Journal of Cellular Physiology, Vol. 73, Issue 1 https://doi.org/10.1002/jcp.1040730108	journal	February 1969
Giant Vesicles: Preparations and Applications Walde, Peter; Cosentino, Katia; Engel, Helen ChemBioChem, Vol. 11, Issue 7 https://doi.org/10.1002/cbic.201000010	journal	March 2010
Model Systems, Lipid Rafts, and Cell Membranes Simons, Kai; Vaz, Winchil L. C. Annual Review of Biophysics and Biomolecular Structure, Vol. 33, Issue 1 https://doi.org/10.1146/annurev.biophys.32.110601.141803	journal	June 2004
Attack of radicals and protons on ladderane lipids: quantum chemical calculations and biological implications Nouri, Dustin H.; Tantillo, Dean J. Organic & Biomolecular Chemistry, Vol. 10, Issue 29 https://doi.org/10.1039/c2ob25717c	journal	January 2012
Insights into the role of cyclic ladderane lipids in bacteria from computer simulations Chaban, Vitaly V.; Nielsen, Morten B.; Kopec, Wojciech Chemistry and Physics of Lipids, Vol. 181 https://doi.org/10.1016/j.chemphyslip.2014.04.002	journal	July 2014
Molecular mechanism of anaerobic ammonium oxidation Kartal, Boran; Maalcke, Wouter J.; de Almeida, Naomi M. Nature, Vol. 479, Issue 7371, p. 127-130 https://doi.org/10.1038/nature10453	journal	October 2011
Molecular Mechanisms of Water and Solute Transport across Archaebacterial Lipid Membranes Mathai, John C.; Sprott, G. Dennis; Zeidel, Mark L. Journal of Biological Chemistry, Vol. 276, Issue 29 https://doi.org/10.1074/jbc.M103265200	journal	May 2001
Biophysical properties of membrane lipids of anammox bacteria: II. Impact of temperature and bacteriohopanoids Boumann, Henry A.; Stroeve, Pieter; Longo, Marjorie L. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1788, Issue 7 https://doi.org/10.1016/j.bbamem.2009.04.005	journal	July 2009
A mixed ladderane/n-alkyl glycerol diether membrane lipid in an anaerobic ammonium-oxidizing bacterium Sinninghe Damsté, Jaap S.; Rijpstra, W. Irene C.; Strous, Marc Chem. Commun., Issue 22 https://doi.org/10.1039/B409806D	journal	January 2004
Permeability of small nonelectrolytes through lipid bilayer membranes Walter, Anne; Gutknecht, John The Journal of Membrane Biology, Vol. 90, Issue 3 https://doi.org/10.1007/BF01870127	journal	October 1986
Biophysical properties of membrane lipids of anammox bacteria: I. Ladderane phospholipids form highly organized fluid membranes Boumann, Henry A.; Longo, Marjorie L.; Stroeve, Pieter Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1788, Issue 7 https://doi.org/10.1016/j.bbamem.2009.04.008	journal	July 2009
Proton flux mechanisms in model and biological membranes Deamer, David W.; Nichols, J. Wylie The Journal of Membrane Biology, Vol. 107, Issue 2 https://doi.org/10.1007/BF01871715	journal	February 1989
The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms Strous, M.; Heijnen, J. J.; Kuenen, J. G. Applied Microbiology and Biotechnology, Vol. 50, Issue 5 https://doi.org/10.1007/s002530051340	journal	November 1998
In Vitro Permeability of Poorly Aqueous Soluble Compounds Using Different Solubilizers in the PAMPA Assay with Liquid Chromatography/Mass Spectrometry Detection Liu, Hanlan; Sabus, Chantel; Carter, Guy T. Pharmaceutical Research, Vol. 20, Issue 11 https://doi.org/10.1023/B:PHAM.0000003380.44755.5a	journal	November 2003
Anammox bacteria: from discovery to application Kuenen, J. Gijs Nature Reviews Microbiology, Vol. 6, Issue 4 https://doi.org/10.1038/nrmicro1857	journal	April 2008
Permeation of protons, potassium ions, and small polar molecules through phospholipid bilayers as a function of membrane thickness Paula, S.; Volkov, A. G.; Van Hoek, A. N. Biophysical Journal, Vol. 70, Issue 1 https://doi.org/10.1016/S0006-3495(96)79575-9	journal	January 1996
A new fluorescent and colorimetric sensor for hydrazine and its application in biological systems Sun, Mingda; Guo, Jing; Yang, Qingbiao J. Mater. Chem. B, Vol. 2, Issue 13 https://doi.org/10.1039/C3TB21753A	journal	January 2014
Ladderane phospholipids in anammox bacteria comprise phosphocholine and phosphoethanolamine headgroups Boumann, Henry A.; Hopmans, Ellen C.; van de Leemput, Ingrid FEMS Microbiology Letters, Vol. 258, Issue 2 https://doi.org/10.1111/j.1574-6968.2006.00233.x	journal	May 2006
Membrane lipids: where they are and how they behave van Meer, Gerrit; Voelker, Dennis R.; Feigenson, Gerald W. Nature Reviews Molecular Cell Biology, Vol. 9, Issue 2 https://doi.org/10.1038/nrm2330	journal	February 2008
Protons May Leak through Pure Lipid Bilayers via a Concerted Mechanism Tepper, Harald L.; Voth, Gregory A. Biophysical Journal, Vol. 88, Issue 5 https://doi.org/10.1529/biophysj.104.056184	journal	May 2005
They Came From the Deep: Syntheses, Applications, and Biology of Ladderanes Nouri, Dustin; Tantillo, Dean Current Organic Chemistry, Vol. 10, Issue 16 https://doi.org/10.2174/138527206778742678	journal	November 2006
Structural determinants of protein partitioning into ordered membrane domains and lipid rafts Lorent, Joseph Helmuth; Levental, Ilya Chemistry and Physics of Lipids, Vol. 192 https://doi.org/10.1016/j.chemphyslip.2015.07.022	journal	November 2015
Structural Determinants of Water Permeability through the Lipid Membrane Mathai, John C.; Tristram-Nagle, Stephanie; Nagle, John F. The Journal of General Physiology, Vol. 131, Issue 1 https://doi.org/10.1085/jgp.200709848	journal	December 2007
Modulation of Plasma Membrane Ca ²⁺ -ATPase by Neutral Phospholipids : EFFECT OF THE MICELLE-VESICLE TRANSITION AND THE BILAYER THICKNESS Pignataro, María Florencia; Dodes-Traian, Martín M.; González-Flecha, F. Luis Journal of Biological Chemistry, Vol. 290, Issue 10 https://doi.org/10.1074/jbc.M114.585828	journal	January 2015
Preparation of giant liposomes in physiological conditions and their characterization under an optical microscope Akashi, K.; Miyata, H.; Itoh, H. Biophysical Journal, Vol. 71, Issue 6 https://doi.org/10.1016/S0006-3495(96)79517-6	journal	December 1996
An intracellular pH gradient in the anammox bacterium Kuenenia stuttgartiensis as evaluated by 31P NMR van der Star, Wouter R. L.; Dijkema, Cor; de Waard, Pieter Applied Microbiology and Biotechnology, Vol. 86, Issue 1 https://doi.org/10.1007/s00253-009-2309-9	journal	October 2009
Structural identification of ladderane and other membrane lipids of planctomycetes capable of anaerobic ammonium oxidation (anammox): Membrane lipids of anammox bacteria Sinninghe Damsté, Jaap S.; Rijpstra, W. Irene C.; Geenevasen, Jan A. J. FEBS Journal, Vol. 272, Issue 16 https://doi.org/10.1111/j.1742-4658.2005.04842.x	journal	August 2005
The inner workings of the hydrazine synthase multiprotein complex Dietl, Andreas; Ferousi, Christina; Maalcke, Wouter J. Nature, Vol. 527, Issue 7578 https://doi.org/10.1038/nature15517	journal	October 2015
Proton transport across transient single-file water pores in a lipid membrane studied by molecular dynamics simulations Marrink, S. J.; Jähnig, F.; Berendsen, H. J. Biophysical Journal, Vol. 71, Issue 2 https://doi.org/10.1016/S0006-3495(96)79264-0	journal	August 1996
Cation permeability induced by valinomycin, gramicidin D and amphotericin B in large lipidic unilamellar vesicles studied by 31P-NMR Herv�, M.; Cybulska, B.; Gary-Bobo, C. M. European Biophysics Journal, Vol. 12, Issue 3 https://doi.org/10.1007/BF00254070	journal	August 1985
The anammoxosome: an intracytoplasmic compartment in anammox bacteria Niftrik, Laura A.; Fuerst, John A.; DamstÃ©, Jaap S. Sinninghe FEMS Microbiology Letters, Vol. 233, Issue 1 https://doi.org/10.1016/j.femsle.2004.01.044	journal	April 2004
Cyclohexane Rings Reduce Membrane Permeability to Small Ions in Archaea-Inspired Tetraether Lipids Koyanagi, Takaoki; Leriche, Geoffray; Onofrei, David Angewandte Chemie International Edition, Vol. 55, Issue 5 https://doi.org/10.1002/anie.201510445	journal	December 2015
Diffusion of univalent ions across the lamellae of swollen phospholipids Bangham, A. D.; Standish, M. M.; Watkins, J. C. Journal of Molecular Biology, Vol. 13, Issue 1 https://doi.org/10.1016/S0022-2836(65)80093-6	journal	August 1965
Nature Utilizes Unusual High London Dispersion Interactions for Compact Membranes Composed of Molecular Ladders Wagner, J. Philipp; Schreiner, Peter R. Journal of Chemical Theory and Computation, Vol. 10, Issue 3 https://doi.org/10.1021/ct5000499	journal	February 2014
Separation of Liquid Phases in Giant Vesicles of Ternary Mixtures of Phospholipids and Cholesterol Veatch, Sarah L.; Keller, Sarah L. Biophysical Journal, Vol. 85, Issue 5 https://doi.org/10.1016/S0006-3495(03)74726-2	journal	November 2003
Linearly concatenated cyclobutane lipids form a dense bacterial membrane Sinninghe Damsté, Jaap S.; Strous, Marc; Rijpstra, W. Irene C. Nature, Vol. 419, Issue 6908 https://doi.org/10.1038/nature01128	journal	October 2002
Ladderane lipid distribution in four genera of anammox bacteria Rattray, Jayne E.; van de Vossenberg, Jack; Hopmans, Ellen C. Archives of Microbiology, Vol. 190, Issue 1 https://doi.org/10.1007/s00203-008-0364-8	journal	April 2008
Choose Your Label Wisely: Water-Soluble Fluorophores Often Interact with Lipid Bilayers Hughes, Laura D.; Rawle, Robert J.; Boxer, Steven G. PLoS ONE, Vol. 9, Issue 2 https://doi.org/10.1371/journal.pone.0087649	journal	February 2014
The membrane bioreactor: A novel tool to grow anammox bacteria as free cells van der Star, Wouter R. L.; Miclea, Andreea I.; van Dongen, Udo G. J. M. Biotechnology and Bioengineering, Vol. 101, Issue 2 https://doi.org/10.1002/bit.21891	journal	October 2008
Widespread distribution of encapsulin nanocompartments reveals functional diversity Giessen, Tobias W.; Silver, Pamela A. Nature Microbiology, Vol. 2, Issue 6 https://doi.org/10.1038/nmicrobiol.2017.29	journal	March 2017
Chemical Synthesis and Self-Assembly of a Ladderane Phospholipid Mercer, Jaron A. M.; Cohen, Carolyn M.; Shuken, Steven R. Journal of the American Chemical Society, Vol. 138, Issue 49 https://doi.org/10.1021/jacs.6b10706	journal	November 2016
Biochemistry and molecular biology of anammox bacteria Jetten, Mike S. M.; Niftrik, Laura van; Strous, Marc Critical Reviews in Biochemistry and Molecular Biology, Vol. 44, Issue 2-3 https://doi.org/10.1080/10409230902722783	journal	June 2009
Structural Determinants of Water Permeability through the Lipid Membrane Mathai, John C.; Tristram-Nagle, Stephanie; Nagle, John F. Carnegie Mellon University https://doi.org/10.1184/r1/6508142	text	January 2008
Cyclohexane Rings Reduce Membrane Permeability to Small Ions in Archaea-Inspired Tetraether Lipids Koyanagi, Takaoki; Leriche, Geoffray; Onofrei, David Angewandte Chemie, Vol. 128, Issue 5 https://doi.org/10.1002/ange.201510445	journal	December 2015
They Came from the Deep. Syntheses, Applications, and Biology of Ladderanes Nouri, Dustin H.; Tantillo, Dean J. ChemInform, Vol. 38, Issue 11 https://doi.org/10.1002/chin.200711267	journal	March 2007

Cited By (12)

Lessons in Strain and Stability: Enantioselective Synthesis of (+)‐[5]‐Ladderanoic Acid Hancock, Erin N.; Kuker, Erin L.; Tantillo, Dean J. Angewandte Chemie, Vol. 132, Issue 1 https://doi.org/10.1002/ange.201910901	journal	November 2019
Lessons in Strain and Stability: Enantioselective Synthesis of (+)-[5]-Ladderanoic Acid Hancock, Erin N.; Kuker, Erin L.; Tantillo, Dean J. Angewandte Chemie International Edition, Vol. 59, Issue 1 https://doi.org/10.1002/anie.201910901	journal	November 2019
Anaerobic ammonium oxidation in marine environments: contribution to biogeochemical cycles and biotechnological developments for wastewater treatment Rios-Del Toro, E. Emilia; Cervantes, Francisco J. Reviews in Environmental Science and Bio/Technology, Vol. 18, Issue 1 https://doi.org/10.1007/s11157-018-09489-3	journal	January 2019
The Discovery of Twenty-Eight New Encapsulin Sequences, Including Three in Anammox Bacteria Tracey, John C.; Coronado, Maricela; Giessen, Tobias W. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-56533-5	journal	December 2019
Photodriven solid-state multiple [2 + 2] cycloaddition strategies for the construction of polycyclobutane derivatives Yu, Jian-Gang; Gan, Ming-Ming; Bai, Sha CrystEngComm, Vol. 21, Issue 32 https://doi.org/10.1039/c9ce00971j	journal	January 2019
An effective reagent to functionalize alcohols with phosphocholine Xu, Lianyan L.; Berg, Lawrence J.; Jamin Keith, D. Organic & Biomolecular Chemistry, Vol. 18, Issue 4 https://doi.org/10.1039/c9ob02582k	journal	January 2020
Recent advances in the total synthesis of cyclobutane-containing natural products Li, Jinshan; Gao, Kai; Bian, Ming Organic Chemistry Frontiers, Vol. 7, Issue 1 https://doi.org/10.1039/c9qo01178a	journal	January 2020
The microbial exometabolome: ecological resource and architect of microbial communities Douglas, Angela E. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 375, Issue 1798 https://doi.org/10.1098/rstb.2019.0250	journal	March 2020
Performance of Anammox Processes for Wastewater Treatment: A Critical Review on Effects of Operational Conditions and Environmental Stresses Cho, Sunja; Kambey, Cicilia; Nguyen, Van Water, Vol. 12, Issue 1 https://doi.org/10.3390/w12010020	journal	December 2019
Membrane constriction and thinning by sequential ESCRT-III polymerization Nguyen, Henry C.; Talledge, Nathaniel; McCullough, John Nature Structural & Molecular Biology, Vol. 27, Issue 4 https://doi.org/10.1038/s41594-020-0404-x	journal	April 2020
Quantitative three-dimensional nondestructive imaging of whole anaerobic ammonium-oxidizing bacteria Peng, Meng-Wen; Guan, Yong; Liu, Jian-Hong Journal of Synchrotron Radiation, Vol. 27, Issue 3 https://doi.org/10.1107/S1600577520002349	journal	April 2020
Membrane Constriction and Thinning by Sequential ESCRT-III Polymerization Nguyen, Henry C.; Talledge, Nathaniel; McCullough, John Biophysical Journal, Vol. 118, Issue 3 https://doi.org/10.1016/j.bpj.2019.11.647	journal	February 2020

Similar Records

Investigation of Proposed Ladderane Biosynthetic Genes from Anammox Bacteria by Heterologous Expression in E. coli

Journal Article · Mon Mar 14 00:00:00 EDT 2016 · PLoS ONE · OSTI ID:1476321

Javidpour, Pouya; Deutsch, Samuel; Mutalik, Vivek K.; +5 more

Halogenation-Dependent Effects of the Chlorosulfolipids of Ochromonas danica on Lipid Bilayers

Journal Article · Fri Oct 09 00:00:00 EDT 2020 · ACS Chemical Biology · OSTI ID:1476321

Moss III, Frank R.; Cabrera, Gabrielle E.; McKenna, Grace M.; +6 more

Phospholipid asymmetry in large unilamellar vesicles induced by transmembrane pH gradients

Journal Article · Tue May 16 00:00:00 EDT 1989 · Biochemistry; (USA) · OSTI ID:1476321

Hope, M J; Redelmeier, T E; Wong, K F; +2 more

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
ladderane
anammox
lipid bilayer
proton permeability
membrane structure

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

Citation Formats

References (46)

Cited By (12)

Similar Records

Related Subjects