Skip to main content
SpringerLink
Log in

Ornithine Lipids and Other Amino Acid-Containing Acyloxyacyl Lipids

  • Reference work entry
  • First Online:
Biogenesis of Fatty Acids, Lipids and Membranes

Part of the book series: Handbook of Hydrocarbon and Lipid Microbiology ((HHLM))

Abstract

Ornithine lipids (OLs) are phosphorus-free membrane lipids relatively common in eubacteria, but apparently absent from archaea and eukaryotes. It has been predicted that about 50% of the sequenced bacterial species have the capacity to synthesize OLs at least under certain growth conditions. Structurally, they are composed of a 3-hydroxy fatty acid amide bound to the α-amino group of ornithine and of a second fatty acyl group ester linked to the 3-hydroxy position of the first fatty acid forming an acyloxyacyl structure. This basic structure of OLs can be modified by hydroxylations in different positions, by N-methylation, or by taurine transfer. The presence of OL and/or modified OLs often seems to form part of a stress response to (changing) environmental conditions. OL modification allows the bacteria to adjust membrane properties by converting already existing membrane lipids into membrane lipids with distinct properties without de novo synthesis. In addition to ornithine, other amino acids (and dipeptides) such as glycine, serineglycine, glutamine, and lysine have been described as headgroups of these lipids in some bacterial species.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 489.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 549.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Anstadt EJ, Fujiwara M, Wasko N, Nichols F, Clark RB (2016) TLR tolerance as a treatment for central nervous system autoimmunity. J Immunol 197:2110–2118

    Article  CAS  Google Scholar 

  • Asselineau J (1991) Bacterial lipids containing amino acids or peptides linked by amide bonds. Fortschr Chem Org Naturst 56:1–85

    CAS  PubMed  Google Scholar 

  • Aygun-Sunar S, Mandaci S, Koch HG, Murria IVJ, Goldfine H, Daldai F (2006) Ornithine lipid is required for optimal steady-state amounts of c-type cytochromes in Rhodobacter capsulatus. Mol Microbiol 61:418–435

    Article  CAS  Google Scholar 

  • Batrakov SG, Nikitin DI, Sheichenko VI, Ruzhitsky AO (1998) A novel sulfonic-acid analogue of ceramide is the major extractable lipid of the Gram-negative marine bacterium Cyclobacterium marinus WH. Biochim Biophys Acta 1391:79–91

    Article  CAS  Google Scholar 

  • Batrakov SG, Nikitin DI, Mosezhnyi AE, Ruzhitsky AO (1999) A glycine-containing phosphorus-free lipoaminoacid from the Gram-negative marine bacterium Cyclobacterium marinus WH. Chem Phys Lipids 99:139–143

    Article  CAS  Google Scholar 

  • Benning C, Huang ZH, Gage DA (1995) Accumulation of a novel glycolipid and a betaine lipid in cells of Rhodobacter sphaeroides grown under phosphate limitation. Arch Biochem Biophys 317:103–111

    Article  CAS  Google Scholar 

  • Clark RB, Cervantes JL, Maciejewski MW, Farrokhi V, Nemati R, Yao X, Anstadt E, Fujiwara M, Wright KT, Riddle C, La Vake CJ, Salazar JC, Finegold S, Nichols FC (2013) Serine lipids of Porphyromonas gingivalis are human and mouse toll-like receptor 2 ligands. Infect Immun 81:3479–3489

    Article  CAS  Google Scholar 

  • Dees C, Shively JM (1982) Localization and quantitation of the ornithine lipid of Thiobacillus thiooxidans. J Bacteriol 149:798–799

    CAS  PubMed  PubMed Central  Google Scholar 

  • Diercks H, Semeniuk A, Gisch N, Moll H, Duda KA, Hölzl G (2015) Accumulation of novel glycolipids and ornithine lipids in Mesorhizobium loti under phosphate deprivation. J Bacteriol 197:497–509

    Article  Google Scholar 

  • Escobedo-Hinojosa WI, Vences-Guzmán MA, Schubotz F, Sandoval-Calderón M, Summons RE, López-Lara IM, Geiger O, Sohlenkamp C (2015) OlsG (Sinac_1600) is an ornithine lipid N-methyltransferase from the planctomycete Singulisphaera acidophila. J Biol Chem 290:15102–15111

    Article  CAS  Google Scholar 

  • Farrokhi V, Nemati R, Nichols FC, Yao X, Anstadt E, Fujiwara M, Grady J, Wakefield D, Castro W, Donaldson J, Clark RB (2013) Bacterial lipodipeptide, lipid 654, is a microbiome-associated biomarker for multiple sclerosis. Clin Transl Immunol 2:e8

    Article  CAS  Google Scholar 

  • Galbraith L, Jonsson MH, Rudhe LC, Wilkinson SG (1999) Lipids and fatty acids of Burkholderia and Ralstonia species. FEMS Microbiol Lett 173:359–364

    Article  CAS  Google Scholar 

  • Gao JL, Weissenmayer B, Taylor AM, Thomas-Oates J, López-Lara IM, Geiger O (2004) Identification of a gene required for the formation of lyso-ornithine lipid, an intermediate in the biosynthesis of ornithine-containing lipids. Mol Microbiol 53:1757–1770

    Article  CAS  Google Scholar 

  • Geiger O, Röhrs V, Weissenmayer B, Finan TM, Thomas-Oates JE (1999) The regulator gene phoB mediates phosphate stress-controlled synthesis of the membrane lipid diacylglycerol-N,N,N-trimethylhomoserine in Rhizobium (Sinorhizobium) meliloti. Mol Microbiol 32:63–73

    Article  CAS  Google Scholar 

  • Geiger O, Gónzalez-Silva N, López-Lara IM, Sohlenkamp C (2010) Amino acid-containing membrane lipids in bacteria. Prog Lipid Res 49:46–60

    Article  CAS  Google Scholar 

  • Gibbons HS, Lin S, Cotter RJ, Raetz CRH (2000) Oxygen requirement for the biosynthesis of the S-2-hydroxymyristate moiety in Salmonella typhimurium lipid A. Function of LpxO, a new Fe(II)/alpha-ketoglutarate-dependent dioxygenase homologue. J Biol Chem 275:32940–32949

    Article  CAS  Google Scholar 

  • Gomi K, Kawasaki K, Kawai Y, Shiozaki M, Nishijima M (2002) Toll-like receptor 4-MD-2 complex mediates the signal transduction induced by flavolipin, an amino acid-containing lipid unique to Flavobacterium meningosepticum. J Immunol 168:2939–2943

    Article  CAS  Google Scholar 

  • Gónzalez-Silva N, López-Lara IM, Reyes-Lamothe R, Taylor AM, Sumpton D, Thomas-Oates J, Geiger O (2011) The dioxygenase-encoding olsD gene from Burkholderia cenocepacia causes the hydroxylation of the amide-linked fatty acyl moiety of ornithine-containing membrane lipids. Biochemistry 50:6396–6408

    Article  Google Scholar 

  • Hölzl G, Dörmann P (2007) Structure and function of glycoglycerolipids in plants and bacteria. Prog Lipid Res 46:225–246

    Article  Google Scholar 

  • Kato H, Goto N (1997) Adjuvanticity of an ornithine-containing lipid of Flavobacterium meningosepticum as a candidate vaccine adjuvant. Microbiol Immunol 41:101–106

    Article  CAS  Google Scholar 

  • Kawai Y, Yano I, Kaneda K (1988) Various kinds of lipoamino acids including a novel serine-containing lipid in an opportunistic pathogen Flavobacterium. Their structures and biological activities on erythrocytes. Eur J Biochem 171:73–80

    Article  CAS  Google Scholar 

  • Kawai Y, Kaneda K, Morisawa Y, Akagawa K (1991a) Protection of mice from lethal endotoxemia by use of an ornithine-containing lipid or a serine-containing lipid. Infect Immun 59:2560–2566. (Erratum: Infect Immunol 1992, 60:320)

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kawai Y, Kamoshita K, Akagawa K (1991b) B-lymphocyte mitogenicity and adjuvanticity of an ornithine-containing lipid or a serine-containing lipid. FEMS Microbiol Lett 67:127–129

    Article  CAS  Google Scholar 

  • Kawai Y, Nakagawa Y, Matuyama T, Akagawa K, Itagawa K, Eukase K, Kusumoto S, Nishijima M, Yano I (1999) A typical bacterial ornithine-containing lipid Nα-(D)-[3-(hexadecanoyloxy)hexadecanoyl]-ornithine is a strong stimulant for macrophages and a useful adjuvant. FEMS Immunol Med Microbiol 23:67–73

    CAS  PubMed  Google Scholar 

  • Kawai Y, Takasuka N, Inoue K, Akagawa K, Nishijima M (2000a) Ornithine-containing lipids stimulate CD14-dependent TNF-α production from murine macrophage-like J7774.1 and RAW 264.7 cells. FEMS Immunol Med Microbiol 28:197–203

    CAS  PubMed  Google Scholar 

  • Kawai Y, Okawarab AI, Okuyama H, Kura F, Suzuki K (2000b) Modulation of chemotaxis, O2− production and myeloperoxidase release from human polymorphonuclear leukocytes by the ornithine-containing lipid and the serineglycine-containing lipid of Flavobacterium. FEMS Immunol Med Microbiol 28:205–209

    CAS  PubMed  Google Scholar 

  • Kawai Y, Watanabe M, Matsuura M, Nishijima M, Kawahara K (2002) The partially degraded lipopolysaccharide of Burkholderia cepacia and ornithine-containing lipids derived from some Gram-negative bacteria are useful complex lipid adjuvants. FEMS Immunol Med Microbiol 34:173–179

    Article  CAS  Google Scholar 

  • Kawazoe R, Okuyama H, Reichardt W, Sasaki S (1991) Phospholipids and a novel glycine-containing lipoamino acid in Cytophaga johnsonae Stanier strain C21. J Bacteriol 173:5470–5475

    Article  CAS  Google Scholar 

  • Knoche HW, Shively JM (1972) The structure of an ornithine-containing lipid from Thiobacillus thiooxidans. J Biol Chem 247:170–178

    CAS  PubMed  Google Scholar 

  • Lewenza S, Falsafi R, Bains M, Rohs P, Stupak J, Sprott GD, Hancock RE (2011) The olsA gene mediates the synthesis of an ornithine lipid in Pseudomonas aeruginosa during growth under phosphate-limiting conditions, but is not involved in antimicrobial peptide susceptibility. FEMS Microbiol Lett 320:95–102

    Article  CAS  Google Scholar 

  • López-Lara IM, Gao JL, Soto MJ, Solares-Pérez A, Weissenmayer B, Sohlenkamp C, Verroios GP, Thomas-Oates JE, Geiger O (2005) Phosphorus-free membrane lipids of Sinorhizobium meliloti are not required for the symbiosis with alfalfa but contribute to increased cell yields under phosphorus-limiting conditions of growth. Mol Plant Microbe Interact 18:973–982

    Article  Google Scholar 

  • Minnikin DE, Abdolrahimzadeh H (1974) The replacement of phosphatidylethanolamine and acidic phospholipids by an ornithine-amide lipid and a minor phosphorus-free lipid in Pseudomonas fluorescence NCMB 129. FEBS Lett 43:257–260

    Article  CAS  Google Scholar 

  • Minnikin DE, Abdolrahimzadeh H, Baddiley J (1972) Variation of polar lipid composition of Bacillus subtilis Marburg with different growth conditions. FEBS Lett 27:16–18

    Article  CAS  Google Scholar 

  • Minnikin DE, Abdolrahimzadeh H, Baddiley J (1974) Replacement of acidic phospholipids by acidic glycolipids in Pseudomonas diminuta. Nature 249:268–269

    Article  CAS  Google Scholar 

  • Mirucki CS, Abedi M, Jiang J, Zhu Q, Wang Y-H, Safavi KE, Clark RB, Nichols FC (2014) Basic activity of Porphyromonas endodontalis complex lipids. J Endod 40:1342–1348

    Article  Google Scholar 

  • Molinaro A, Holst O, Di Lorenzo F, Callaghan M, Nurisso A, D’Errico G, Zamyatina A, Peri F, Berisio R, Jerala R, Jiménez-Barbero J, Silipo A, Martín-Santamaría S (2015) Chemistry of Lipid A: at the heart of innate immunity. Chem Eur J 21:500–519

    Article  CAS  Google Scholar 

  • Moore EK, Hopmans EC, Rijpstra IC, Villanueva L, Dedysh SN, Kulichevskaya IS, Wienk H, Schoutsen F, Sinninghe Damsté JS (2013) Novel mono-, di-, and trimethylornithine membrane lipids in northern wetland planctomycetes. Environ Microbiol 79:6874–6884

    Article  CAS  Google Scholar 

  • Moore EK, Hopmans EC, Rijpstra IC, Sánchez-Andrea I, Villanueva L, Wienk H, Schoutsen F, Stams AJM, Sinninghe Damsté JS (2015a) Lysine and novel hydroxylysine lipids in soil bacteria: amino acid membrane lipid response to temperature and pH in Pseudopedobacter saltans. Front Microbiol 6:637

    Article  Google Scholar 

  • Moore EK, Villanueva L, Hopmans EC, Rijpstra IC, Mets A, Dedysh SN, Sinninghe Damsté JS (2015b) Abundant trimethylornithine lipids and specific gene sequences are indicative of planctomycete importance at the oxic/anoxic interface in Sphagnum-dominated northern wetlands. Appl Environ Microbiol 81:6333–6344

    Article  CAS  Google Scholar 

  • Moore EK, Hopmans EC, Rijpstra IC, Villanueva L, Sinninghe Damsté JS (2016) Elucidation and identification of amino acid containing membrane lipids using liquid chromatography/high-resolution mass spectrometry. Rapid Commun Mass Spectrom 30:739–750

    Article  Google Scholar 

  • Nikaido H (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67:593–656

    Article  CAS  Google Scholar 

  • Palacios-Chaves L, Conde-Álvarez R, Gil-Ramírez Y, Zuñiga-Ripa A, Barquero-Calvo E, Chacón-Díaz C, Chaves-Olarte E, Arce-Gorvel V, Gorvel JP, Moreno E, de Miguel MJ, Grilló MJ, Moriyón I, Iriarte M (2011) Brucella abortus ornithine lipids are dispensable outer membrane components devoid of a marked pathogen-associated molecular pattern. PLoS ONE 6:e16030

    Article  CAS  Google Scholar 

  • Rojas-Jiménez K, Sohlenkamp C, Geiger O, Martínez-Romero E, Werner D, Vinuesa P (2005) A ClC chloride channel homolog and ornithine-containing membrane lipids of Rhizobium tropici CIAT899 are involved in symbiotic efficiency and acid tolerance. Mol Plant-Microbe Interact 18:1175–1185

    Article  Google Scholar 

  • de Rudder KE, López-Lara IM, Geiger O (2000) Inactivation of the gene for phospholipid N-methyltransferase in Sinorhizobium meliloti: phosphatidylcholine is required for normal growth. Mol Microbiol 37:763–772

    Article  Google Scholar 

  • Sainz F, Mas A, Torija MJ (2016) Draft genome sequences of Gluconobacter cerinus CECT 9110 and Gluconobacter japonicus CECT 8443, acetic acid bacteria isolated from grape must. Genome Announc 4(3):e00621–e00616. https://doi.org/10.1128/genomeA.00621-16

    Article  PubMed  PubMed Central  Google Scholar 

  • Sandoval-Calderón M, Nguyen DD, Kapono CA, Herron P, Dorrestein PC, Sohlenkamp C (2015) Plasticity of Streptomyces coelicolor membrane composition under different growth conditions and during development. Front Microbiol 6:1465

    Article  Google Scholar 

  • Sohlenkamp C, Geiger O (2016) Bacterial membrane lipids: Diversity in structures and pathways. FEMS Microbiol Rev 40:133–159

    Article  CAS  Google Scholar 

  • Tahara Y, Yamada Y, Kondo K (1976a) New lysine-containing lipid isolated from Agrobacterium tumefaciens. Agric Biol Chem 40:1449–1450

    CAS  Google Scholar 

  • Tahara Y, Kameda M, Yamada Y, Kondo K (1976b) New lipid – Ornithine and taurine-containing cerilipin. Agric Biol Chem 40:243–244

    CAS  Google Scholar 

  • Tahara Y, Shinmoto K, Yamada Y, Kondo K (1978) Enzymatic synthesis of tauro-ornithine lipid in Gluconobacter cerinus. Agric Biol Chem 42:205–206

    CAS  Google Scholar 

  • Taylor CJ, Anderson AJ, Wilkinson SG (1998) Phenotypic variation of lipid composition in Burkholderia cepacia: a response to increased growth temperature is a greater content of 2-hydroxy acids in phosphatidylethanolamine and ornithine amide lipid. Microbiology 144:1737–1745

    Article  CAS  Google Scholar 

  • Vences-Guzmán MA, Guan Z, Ormeño-Orrillo E, González-Silva N, López-Lara IM, Martínez-Romero E, Geiger O, Sohlenkamp C (2011) Hydroxylated ornithine lipids increase stress tolerance in Rhizobium tropici CIAT899. Mol Microbiol 79:1496–1514

    Article  Google Scholar 

  • Vences-Guzmán MA, Geiger O, Sohlenkamp C (2012) Ornithine lipids and their structural modifications: from A to E and beyond. FEMS Microbiol Lett 335:1–10

    Article  Google Scholar 

  • Vences-Guzmán MA, Guan Z, Bermúdez-Barrientos JR, Geiger O, Sohlenkamp C (2013) Agrobacteria lacking ornithine lipids induce more rapid tumor formation. Environ Microbiol 15:895–906

    Article  Google Scholar 

  • Vences-Guzmán MA, Guan Z, Escobedo-Hinojosa WI, Bermúdez-Barrientes JR, Geiger O, Sohlenkamp C (2015) Discovery of a bifunctional acyltransferase responsible for ornithine lipid synthesis in Serratia proteamaculans. Environ Microbiol 17:1487–1496

    Article  Google Scholar 

  • Wang Y-H, Nemati R, Anstadt E, Liu Y, Son Y, Zhu Q, Yao X, Clark RB, Rowe DW, Nichols FC (2015) Serine dipeptide lipids of Porphyromonas gingivalis inhibit osteoblast differentiation: relationship to Toll-like receptor 2. Bone 81:654–661

    Article  CAS  Google Scholar 

  • Weissenmayer B, Gao JL, López-Lara IM, Geiger O (2002) Identification of a gene required for the biosynthesis of ornithine-derived lipids. Mol Microbiol 45:721–733

    Article  CAS  Google Scholar 

  • Zavaleta-Pastor M, Sohlenkamp C, Gao JL, Guan Z, Zaheer R, Finan TM, Raetz CRH, López-Lara IM, Geiger O (2010) Sinorhizobium meliloti phospholipase C required for lipid remodeling during phosphorus limitation. Proc Natl Acad Sci USA 107:302–307

    Article  CAS  Google Scholar 

  • Zhang X, Ferguson-Miller SM, Reid GE (2009) Characterization of ornithine and glutamine lipids extracted from cell membranes of Rhodobacter sphaeroides. J Am Soc Mass Spectrom 20:198–212

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Work in the laboratory was supported by grants to C.S. from SEP-CONACyT (237713) and PAPIIT-UNAM (IN202413, IN208116).

Author information

Authors and Affiliations

  1. Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, Mexico

    Christian Sohlenkamp

Authors
  1. Christian Sohlenkamp
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christian Sohlenkamp .

Editor information

Editors and Affiliations

  1. Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, Mexico

    Otto Geiger

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this entry

Check for updates. Verify currency and authenticity via CrossMark

Cite this entry

Sohlenkamp, C. (2019). Ornithine Lipids and Other Amino Acid-Containing Acyloxyacyl Lipids. In: Geiger, O. (eds) Biogenesis of Fatty Acids, Lipids and Membranes. Handbook of Hydrocarbon and Lipid Microbiology . Springer, Cham. https://doi.org/10.1007/978-3-319-50430-8_13

Download citation

Publish with us

Policies and ethics

Search

Navigation