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Linearly concatenated cyclobutane lipids form a dense bacterial membrane

Nature volume 419, pages 708–712 (2002)Cite this article

Abstract

Lipid membranes are essential to the functioning of cells, enabling the existence of concentration gradients of ions and metabolites. Microbial membrane lipids can contain three-, five-, six- and even seven-membered aliphatic rings1,2,3, but four-membered aliphatic cyclobutane rings have never been observed. Here we report the discovery of cyclobutane rings in the dominant membrane lipids of two anaerobic ammonium-oxidizing (anammox) bacteria. These lipids contain up to five linearly fused cyclobutane moieties with cis ring junctions. Such ‘ladderane’ molecules are unprecedented in nature but are known as promising building blocks in optoelectronics4. The ladderane lipids occur in the membrane of the anammoxosome, the dedicated intracytoplasmic compartment where anammox catabolism takes place. They give rise to an exceptionally dense membrane, a tight barrier against diffusion. We propose that such a membrane is required to maintain concentration gradients during the exceptionally slow anammox metabolism and to protect the remainder of the cell from the toxic anammox intermediates. Our results further illustrate that microbial membrane lipid structures are far more diverse than previously recognized5,6,7.

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Figure 1: Structures of the anammox ladderane membrane lipids.
Figure 2: Model of the anammox cell and its anammoxosome membrane.
Figure 3: Microscopy of anammoxosomes.

References

  1. Grogan, D. W. et al. Cyclopropane ring formation in membrane lipids of bacteria. Microbiol. Mol. Biol. Rev. 61, 446–449 (1997)

    Google Scholar 

  2. DeRosa, M. & Gambacorta, A. The lipids of archaebacteria. Prog. Lipid Res. 27, 153–175 (1988)

    Article  CAS  Google Scholar 

  3. Wisotzkey, J. D., Jurtshuk, P. Jr, Fox, G. E., Deinhard, G. & Poralla, K. Comparative sequence analyses on the 16S rRNA (rDNA) of Bacillus acidocaldarius, Bacillus acidoterestris, and Bacillus cycloheptanicus and proposal for creation of a new genus, Alicyclobacillus gen. nov. Int. J. Syst. Bacteriol. 42, 263–269 (1992)

    Article  CAS  Google Scholar 

  4. Li, W. & Fox, M. A. Syntheses, characterization, and photophysics studies of photoactive chromophore 2-naphthyl-labelled [n]-ladderanes. J. Am. Chem. Soc. 118, 11752–11758 (1996)

    Article  CAS  Google Scholar 

  5. Schouten, S., Hopmans, E. C., Pancost, R. D. & Sinninghe Damsté, J. S. Widespread occurrence of structurally diverse tetraether membrane lipids: Evidence for the ubiquitous presence of low-temperature relatives of hyperthermophiles. Proc. Natl Acad. Sci. USA 97, 14421–14426 (2000)

    Article  ADS  CAS  Google Scholar 

  6. Pancost, R. D., Bouloubassi, I., Aloisi, V., Sinninghe Damsté, J. S. & the MEDINAUT Shipboard Scientific Party Three series of non-isoprenoidal dialkyl glycerol diethers in cold-seep carbonate crusts. Org. Geochem. 32, 695–707 (2001)

    Article  CAS  Google Scholar 

  7. Sinninghe Damsté, J. S., Hopmans, E. C., Pancost, R. D., Schouten, S. & Geenevasen, J. A. J. Newly discovered non-isoprenoid dialkyl diglycerol tetraether lipids in sediments. J. Chem. Soc. Chem. Commun. 1683–1684 (2000)

  8. Strous, M. et al. Missing lithotroph identified as new planctomycete. Nature 400, 446–449 (1999)

    Article  ADS  CAS  Google Scholar 

  9. Schmid, M. et al. Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Syst. Appl. Microbiol. 23, 93–106 (2000)

    Article  CAS  Google Scholar 

  10. Egli, K. et al. Enrichment and characterization of an anammox bacterium from a rotating biological contactor treating ammonium-rich leachate. Arch. Microbiol. 175, 198–207 (2001)

    Article  CAS  Google Scholar 

  11. Lindsay, M. R. et al. Cell compartmentalisation in planctomycetes: novel types of structural organisation for the bacterial cell. Arch. Microbiol. 175, 413–429 (2001)

    Article  CAS  Google Scholar 

  12. van de Graaf, A. A., de Bruijn, P., Robertson, L. A., Jetten, M. S. M. & Kuenen, J. G. Metabolic pathway of anaerobic ammonium oxidation on basis of 15N-studies in a fluidized bed reactor. Microbiology 143, 2415–2421 (1997)

    Article  CAS  Google Scholar 

  13. Olsen, G. J. What's eating the free lunch? Nature 400, 403–404 (1999)

    Article  ADS  CAS  Google Scholar 

  14. Miller, M. A. & Schulman, J. M. AM1, MNDO and MM2 studies on concatenated cyclobutanes: Prismans, ladderanes and asteranes. J. Mol. Struct. 163, 133–141 (1988)

    Article  Google Scholar 

  15. Sittig, M. & Schlesner, H. Chemotaxonomic investigation of various prosthecate and/or budding bacteria. Syst. Appl. Microbiol. 16, 92–103 (1993)

    Article  CAS  Google Scholar 

  16. Van de Graaf, A. A. et al. Autotrophic growth of anaerobic ammonium-oxidizing micro-organisms in a fluidized bed reactor. Microbiology 142, 2187–2196 (1996)

    Article  CAS  Google Scholar 

  17. Langworthy, T. A. & Pond, J. L. Archaebacterial ether lipids and chemotaxonomy. Syst. Appl. Microbiol. 7, 253–257 (1986)

    Article  CAS  Google Scholar 

  18. Langworthy, T. A., Holzer, G., Zeikus, J. G. & Tornabene, T. G. Iso- and anteiso-branched glycerol diethers of the thermophilic anaerobe Thermodesulfobacterium commune. System. Appl. Microbiol. 4, 1–17 (1983)

    Article  CAS  Google Scholar 

  19. Huber, R. et al. Formation of ammonium from nitrate during chemolithoautotrophic growth of the extremely thermophilic bacterium Ammonifex degensii gen. nov. sp. nov. Syst. Appl. Microbiol. 19, 40–49 (1996)

    Article  CAS  Google Scholar 

  20. Huber, R. et al. Aquifex pyrophilus, new genus new species, represents a novel group of marine hyperthermophilic hydrogen-oxidizing bacteria. Syst. Appl. Microbiol. 15, 340–351 (1992)

    Article  Google Scholar 

  21. DeRosa, M., et al. Microbiology of Extreme Environments and its Potential for Biotechnology (eds Da Costa, M. S., Duarte, J. C. & Williams, R. A. D.) 167–173 (Elsevier, London, 1989)

    Google Scholar 

  22. Van den Vossenberg, J. C. M., Driessen, A. J. M. & Konings, W. N. The essence of being extremophilic: the role of the unique archaeal membrane lipids. Extremophiles 2, 163–170 (1998)

    Article  Google Scholar 

  23. Rütters, H., Sass, H., Cypionka, H. & Rullkötter, J. Monoalkylether phospholipids in the sulfate-reducing bacteria Desulfosarcina variabilis and Desulforhabdus amnigenus. Arch. Microbiol. 176, 435–442 (2001)

    Article  Google Scholar 

  24. Mehta, G. et al. Quest for higher ladderanes: Oligomerization of a cyclobutadiene derivative. Angew. Chem. Int. Ed. 31, 1488–1490 (1992)

    Article  Google Scholar 

  25. Strous, M., Heijnen, J. J., Kuenen, J. G. & Jetten, M. S. M. The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms. Appl. Microbiol. Biotechnol. 50, 589–596 (1998)

    Article  CAS  Google Scholar 

  26. Thamdrup, B. & Dalsgaard, T. Production of N2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl. Environ. Microbiol. 68, 1312–1318 (2002)

    Article  CAS  Google Scholar 

  27. Schalk, J., de Vries, S., Kuenen, J. G. & Jetten, M. S. M. Involvement of a novel hydroxylamine oxidoreductase in anaerobic ammonium oxidation. Biochemistry 39, 5405–5412 (2000)

    Article  CAS  Google Scholar 

  28. van Duin, A. C. T. & Larter, S. A computational chemical study of penetration and displacement of water films near mineral surfaces. Geochem. Trans. 006 (2001)

  29. Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A. & Haak, J. R. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81, 3684–3690 (1984)

    Article  ADS  CAS  Google Scholar 

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Acknowledgements

We thank J. G. Kuenen, H. Hiemstra, S. Schouten and W. Konings for stimulating discussions, C. Erkelens (University of Leiden) for access to the 600- and 750-MHz NMR instruments, J. A. Fuerst for cells of Gemmata obscuriglobus and Pirellula sp. and training of L.A.v.N., M. Wolters-Arts for help with electron microscopy, and K. T. van de Pas-Schoonen for help with immunofluorescence.

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Author notes

  1. Mike S. M. Jetten

    Present address: Department of Microbiology, University of Nijmegen, Toernooiveld 1, 6525 ED, Nijmegen, The Netherlands

Authors and Affiliations

  1. Department of Marine Biogeochemistry and Toxicology, Royal Netherlands Institute for Sea Research (NIOZ), PO Box 59, 1790 AB, Den Burg, The Netherlands

    Jaap S. Sinninghe Damsté, W. Irene C. Rijpstra & Ellen C. Hopmans

  2. Department of Microbiology, University of Nijmegen, Toernooiveld 1, 6525 ED, Nijmegen, The Netherlands

    Marc Strous & Laura A. van Niftrik

  3. University of Amsterdam, Institute of Molecular Chemistry (IMC), Nieuwe Achtergracht 129, 1018 WS, Amsterdam, The Netherlands

    Jan A. J. Geenevasen

  4. Department of Fossil Fuels and Environmental Geochemistry, Newcastle University, Drummond Building, NE1 7RU, Newcastle upon Tyne, UK

    Adri C. T. van Duin

  5. Department of Biotechnology, Delft University of Technology, Julianalaan 67, 2628 BC, Delft, The Netherlands

    Mike S. M. Jetten

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Correspondence to Jaap S. Sinninghe Damsté.

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Sinninghe Damsté, J., Strous, M., Rijpstra, W. et al. Linearly concatenated cyclobutane lipids form a dense bacterial membrane. Nature 419, 708–712 (2002). https://doi.org/10.1038/nature01128

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