Skip to main content

Lipid A structural characterization from the LPS of the Siberian psychro-tolerant Psychrobacter arcticus 273-4 grown at low temperature

Abstract

Psychrobacter arcticus 273-4 is a Gram-negative bacterium isolated from a 20,000-to-30,000-year-old continuously frozen permafrost in the Kolyma region in Siberia. The survival strategies adopted to live at subzero temperatures include all the outer membrane molecules. A strategic involvement in the well-known enhancement of cellular membrane fluidity is attributable to the lipopolysaccharides (LPSs). These molecules covering about the 75% of cellular surface contribute to cold adaptation through structural modifications in their portions. In this work, we elucidated the exact structure of lipid A moiety obtained from the lipopolysaccharide of P. arcticus grown at 4 °C, to mimic the response to the real environment temperatures. The lipid A was obtained from the LPS by mild acid hydrolysis. The lipid A and its partially deacylated derivatives were exhaustively characterized by chemical analysis and by means of ESI Q-Orbitrap mass spectrometry. Moreover, biological assays indicated that P. arcticus 273-4 lipid A may behave as a weak TLR4 agonist.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Ayala-del-Río HL, Chain PS, Grzymski JJ et al (2010) The genome sequence of Psychrobacter arcticus 273-4, a psychroactive Siberian permafrost bacterium, reveals mechanisms for adaptation to low-temperature growth. Appl Environ Microbiol 76:2304–2312. https://doi.org/10.1128/AEM.02101-09

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. Beales N (2004) Adaptation of microorganisms to cold temperatures, weak acid preservatives, low pH, and osmotic stress: a review. Compr Rev Food Sci Food Saf 3:1–20

    CAS  Article  Google Scholar 

  3. Benforte FC, Colonnella MA, Ricardi MM, Solar Venero EC, Lizarraga L, López NI, Tribelli PM (2018) Novel role of the LPS core glycosyltransferase WapH for cold adaptation in the Antarctic bacterium Pseudomonas extremaustralis. PLoS ONE 13(2):e0192559. https://doi.org/10.1371/journal.pone.0192559

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  4. Carillo S, Pieretti G, Parrilli E, Tutino ML, Gemma S, Molteni M, Lanzetta R, Parrilli M, Corsaro MM (2011) Structural investigation and biological activity of the lipooligosaccharide from the psychrophilic bacterium Pseudoalteromonas haloplanktis TAB 23. Chem Eur J 17:7053–7060. https://doi.org/10.1002/chem.201100579

    CAS  Article  PubMed  Google Scholar 

  5. Carty SM, Sreekumar KR, Raetz CRH (1999) Effect of cold shock on lipid A biosynthesis in Escherichia coli. Induction at 12 °C of an acyltransferase specific for palmitoleoyl-acyl carrier protein. J Biol Chem 274:9677–9685. https://doi.org/10.1074/jbc.274.14.9677

    CAS  Article  PubMed  Google Scholar 

  6. Casillo A, Parrilli E, Sannino F, Lindner B, Lanzetta R, Parrilli M, Tutino ML, Corsaro MM (2015) Structural investigation of the oligosaccharide portion isolated from the lipooligosaccharide of the permafrost psychrophile Psychrobacter arcticus 273-4. Mar Drugs 13(7):4539–4555. https://doi.org/10.3390/md13074539

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. Casillo A, Parrilli E, Sannino F et al (2017a) Structure-activity relationship of the exopolysaccharide from a psychrophilic bacterium: a strategy for cryoprotection. Carbohydr Polym 156:364–371

    CAS  Article  PubMed  Google Scholar 

  8. Casillo A, Ziaco M, Lindner B, Parrilli E, Schwudke D, Holgado A, Verstrepen L, Sannino F, Beyaert E, Lanzetta R, Tutino ML, Corsaro MM (2017b) Unusual lipid A from a cold adapted bacterium: detailed structural characterization. ChemBioChem 18:1–11. https://doi.org/10.1002/cbic.201700287

    CAS  Article  Google Scholar 

  9. Chattopadhyay MK (2006) Mechanism of bacterial adaptation to low temperature. J Biosci 31:157–165

    CAS  Article  PubMed  Google Scholar 

  10. Chattopadhyay MK, Reddy GS, Shivaji S (2014) Psychrophilic bacteria: biodiversity, molecular basis of cold adaptation and biotechnological implications. Curr Opin Biotechnol 3:100–116

    CAS  Article  Google Scholar 

  11. Corsaro MM, Dal Piaz F, Lanzetta R, Parrilli M (2002) Lipid A structure of Pseudoalteromonas haloplanktis TAC 125: use of electrospray ionization tandem mass spectrometry for the determination of fatty acid distribution. J Mass Spectrom 37:481–488. https://doi.org/10.1002/jms.304

    CAS  Article  PubMed  Google Scholar 

  12. Corsaro MM, Lanzetta R, Parrilli E, Parrilli M, Tutino ML, Ummarino S (2004) Influence of growth temperature on lipid and phosphate contents of surface polysaccharides from Antarctic Pseudoalteromonas haloplanktis TAC 125 bacterium. J Bacteriol 186:29–34. https://doi.org/10.1128/JB.186.1.29-34.2004

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. Corsaro MM, Pieretti G, Lindner B, Lanzetta R, Parrilli E, Tutino ML, Parrilli M (2008) Highly phosphorylated core oligosaccaride structures from cold-adapted Psychromonas arctica. Chem Eur J 14:9368–9376. https://doi.org/10.1002/chem.200800117

    CAS  Article  PubMed  Google Scholar 

  14. D’Amico S, Collins T, Marx JC, Feller G, Gerday C (2006) Psychrophilic microorganisms: challenges for life. EMBO Rep 7:385–389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. De Mayeer P, Anderson D, Cary C, Cowan DA (2014) Some like it cold: understanding the survival strategies of psychrophiles. EMBO Rep 15:508–517. https://doi.org/10.1002/embr.201338170

    CAS  Article  Google Scholar 

  16. Domon B, Costello CE (1988) A systematic nomenclature for carbohydrate fragmentations in FAB-MS/MS spectra of glycoconjugates. Glycoconj J 5:397–409

    CAS  Article  Google Scholar 

  17. Gilichinsky DA, Wilson GS, Friedmann EI et al (2007) Microbial populations in Antarctic permafrost: biodiversity, state, age and implication for astrobiology. Astrobiology 7:275–311

    CAS  Article  PubMed  Google Scholar 

  18. Graumann PL, Marahiel MA (1999) Cold schock response in Bacillus subtilis. J Mol Microbiol Biotechnol 1:203–209

    CAS  PubMed  Google Scholar 

  19. Korneev KV, Kondakova AN, Arbatsky NP et al (2014) Distinct biological activity of lipopolysaccharides with different lipid a acylation status from mutant strains of Yersinia pestis and some members of genus Psychrobacter. Biochem (Mosc) 79:1333

    CAS  Article  Google Scholar 

  20. Park BS, Song DH, Kim HM, Choi B, Lee H, Lee J (2009) The structural basis of lipopolysaccharide recognition by the TLR4–MD-2 complex. Nature 458:1191–1195. https://doi.org/10.1038/nature07830

    CAS  Article  PubMed  Google Scholar 

  21. Silipo A, Lanzetta R, Amoresano A, Parrilli M, Molinaro A (2002) Ammonium hydroxide hydrolysis a valuable support in the MALDI-TOF mass spectrometry analysis of lipid A fatty acid distribution. J Lipid Res 43:2188–2195. https://doi.org/10.1194/jlr.D200021-JLR200

    CAS  Article  PubMed  Google Scholar 

  22. Sweet CR, Alpuche GM, Landis CA, Sandman BC (2014) Endotoxin structures in the psychrophiles Psychromonas marina and Psychrobacter cryohalolentis contain distinctive acyl features. Mar Drugs 12:4126–4147. https://doi.org/10.3390/md12074126

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. Sweet CR, Watson RE, Landis CA, Smith JP (2015) Temperature-dependence of lipid A acyl structure in Psychrobacter cryohalolentis and Arctic isolates of Colwellia hornerae and Colwellia piezophila. Mar Drugs 13:4701–4720. https://doi.org/10.3390/md13084701

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. Vishnivetskaya TA, Kathariou S, McGrath J, Gilichinsky DA, Tiedje JM (2000) Low-temperature recovery strategies for the isolation of bacteria from ancient permafrost sediments. Extremophiles 4:165–173. https://doi.org/10.1007/s007920070031

    CAS  Article  PubMed  Google Scholar 

  25. Westphal O, Jann K (1965) Bacterial lipopolysaccharides: extraction with phenol–water and further applications of the procedure. Methods Carbohydr Chem 5:83–91

    CAS  Google Scholar 

  26. Zhang YM, Rock CO (2008) Membrane lipid homeostasis in bacteria. Nat Rev Microbiol 6:222–233. https://doi.org/10.1038/nrmicro1839

    CAS  Article  PubMed  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Angela Casillo or Maria Michela Corsaro.

Additional information

Communicated by S. Albers.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 471 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Casillo, A., Ziaco, M., Lindner, B. et al. Lipid A structural characterization from the LPS of the Siberian psychro-tolerant Psychrobacter arcticus 273-4 grown at low temperature. Extremophiles 22, 955–963 (2018). https://doi.org/10.1007/s00792-018-1051-6

Download citation

Keywords

  • Psychrobacter arcticus 273-4
  • Lipid A
  • Mass spectrometry
  • Psychrotolerant
  • Permafrost