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, log in via an institution to check access.
Similar content being viewed by others
References
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
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
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
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
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
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
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
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
Chattopadhyay MK (2006) Mechanism of bacterial adaptation to low temperature. J Biosci 31:157–165
Chattopadhyay MK, Reddy GS, Shivaji S (2014) Psychrophilic bacteria: biodiversity, molecular basis of cold adaptation and biotechnological implications. Curr Opin Biotechnol 3:100–116
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
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
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
D’Amico S, Collins T, Marx JC, Feller G, Gerday C (2006) Psychrophilic microorganisms: challenges for life. EMBO Rep 7:385–389
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
Domon B, Costello CE (1988) A systematic nomenclature for carbohydrate fragmentations in FAB-MS/MS spectra of glycoconjugates. Glycoconj J 5:397–409
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
Graumann PL, Marahiel MA (1999) Cold schock response in Bacillus subtilis. J Mol Microbiol Biotechnol 1:203–209
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
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
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
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
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
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
Westphal O, Jann K (1965) Bacterial lipopolysaccharides: extraction with phenol–water and further applications of the procedure. Methods Carbohydr Chem 5:83–91
Zhang YM, Rock CO (2008) Membrane lipid homeostasis in bacteria. Nat Rev Microbiol 6:222–233. https://doi.org/10.1038/nrmicro1839
Author information
Authors and Affiliations
Corresponding authors
Additional information
Communicated by S. Albers.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00792-018-1051-6