Analysis of Bacteriohopanoids from Thermophilic Bacteria by Liquid Chromatography-Mass Spectrometry
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic
Document type Journal Article
Grant support
RVO61388971
Institutional Research Concept
18-00036S
Czech Science Foundation
MZE-RO1918
Ministry of Agriculture of the Czech Republic
PubMed
34683383
PubMed Central
PMC8537080
DOI
10.3390/microorganisms9102062
PII: microorganisms9102062
Knihovny.cz E-resources
- Keywords
- Geobacillus stearothermophilus, hopanoids, liquid chromatography–high-resolution electrospray mass spectrometry, thermophilic bacteria,
- Publication type
- Journal Article MeSH
Background: Hopanoids modify plasma membrane properties in bacteria and are often compared to sterols that modulate membrane fluidity in eukaryotes. In some microorganisms, they can also allow adaptations to extreme environments. Methods: Hopanoids were identified by liquid chromatography-mass spectrometry in fourteen strains of thermophilic bacteria belonging to five genera, i.e., Alicyclobacillus, Brevibacillus, Geobacillus, Meiothermus, and Thermus. The bacteria were cultivated at temperatures from 42 to 70 °C. Results: Regardless of the source of origin, the strains have the same tendency to adapt the hopanoid content depending on the cultivation temperature. In the case of aminopentol, its content increases; aminotetrol does not show a significant change; and in the case of aminotriol the content decreases by almost a third. The content of bacteriohopanetetrol and bacteriohopanetetrol glycoside decreases with increasing temperature, while in the case of adenosylhopane the opposite trend was found. Conclusions: Changes in hopanoid content can be explained by increased biosynthesis, where adenosylhopane is the first intermediate in the biosynthesis of the hopanoid side chain.
Institute of Microbiology The Czech Academy of Sciences Vídeňská 1083 142 20 Prague Czech Republic
Research Institute of Brewing and Malting Lípová 511 120 44 Prague Czech Republic
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Paces T., Smejkal V. Magmatic and Fossil Components of Thermal and Mineral Waters in the Eger River Continental Rift (Bohemian Massif, Central Europe) In: Wanty R.B., Seal II R.R., editors. Water-Rock Interaction. Proceedings of the Eleventh International Symposium on Water-Rock Interaction. Taylor & Francis Group; Abingdon, UK: 2004. pp. 167–172.
Peckova M. Properties of a Hyperthermophilic Bacterium (Thermus sp.) Isolated from a Carlsbad Spring. Folia Microbiol. 1991;36:515–521. doi: 10.1007/BF02884029. DOI
Gharwalova L., Palyzova A., Maresova H., Kolouchova I., Kyselova L., Rezanka T. Identification of Homologous Polyprenols from Thermophilic Bacteria. Microorganisms. 2021;9:1168. doi: 10.3390/microorganisms9061168. PubMed DOI PMC
Mehta D., Satyanarayana T. Diversity of Hot Environments and Thermophilic Microbes. In: Satyanarayana T., Littlechild J., Kawarabayasi Y., editors. Thermophilic Microbes in Environmental and Industrial Biotechnology: Biotechnology of Thermophiles. Springer; Dordrecht, The Netherland: 2013. pp. 3–60.
Doree M., Terrine C. Enzymatic Synthesis of Ribonucleoside-5’-Phosphates from Some N6-Substituted Adenosines. Phytochemistry. 1973;12:1017–1023. doi: 10.1016/0031-9422(73)85008-3. DOI
Liu W., Sakr E., Schaeffer P., Talbot H.M., Donisi J., Härtner T., Kannenberg E., Takano E., Rohmer M. Ribosylhopane, a Novel Bacterial Hopanoid, as Precursor of C35 Bacteriohopanepolyols in Streptomyces coelicolor A3(2) Chembiochem. 2014;15:2156–2161. doi: 10.1002/cbic.201402261. PubMed DOI PMC
Hippchen B., Röll A., Poralla K. Occurrence in Soil of Thermo-Acidophilic Bacilli Possessing ω-Cyclohexane Fatty Acids and Hopanoids. Arch. Microbiol. 1981;129:53–55. doi: 10.1007/BF00417180. DOI
Damsté J.S.S., Van Duin A.C.T., Hollander D., Kohnen M.E.L., De Leeuw J.W. Early Diagenesis of Bacteriohopanepolyol Derivatives: Formation of Fossil Homohopanoids. Geochim. Cosmochim. Acta. 1995;59:5141–5157. doi: 10.1016/0016-7037(95)00338-X. DOI
Poralla K., Härtner T., Kannenberg E. Effect of Temperature and pH on the Hopanoid Content of Bacillus acidocaldarius. FEMS Microbiol. Lett. 1984;23:253–256. doi: 10.1111/j.1574-6968.1984.tb01073.x. DOI
Caron B., Mark A.E., Poger D. Some like It Hot: The Effect of Sterols and Hopanoids on Lipid Ordering at High Temperature. J. Phys. Chem. Lett. 2014;5:3953–3957. doi: 10.1021/jz5020778. PubMed DOI
Sessions A.L., Zhang L., Welander P.V., Doughty D., Summons R.E., Newman D.K. Identification and Quantification of Polyfunctionalized Hopanoids by High Temperature Gas Chromatography-Mass Spectrometry. Org. Geochem. 2013;56:120–130. doi: 10.1016/j.orggeochem.2012.12.009. PubMed DOI PMC
Rezanka T., Kambourova M., Derekova A., Kolouchova I., Sigler K. LC-ESI-MS/MS Identification of Polar Lipids of Two Thermophilic Anoxybacillus Bacteria Containing a Unique Lipid Pattern. Lipids. 2012;47:729–739. doi: 10.1007/s11745-012-3675-0. PubMed DOI
Talbot H., Watson D., Murrell J., Carter J., Farrimond P. Analysis of Intact Bacteriohopanepolyols from Methanotrophic Bacteria by Reversed-Phase High-Performance Liquid Chromatography-Atmospheric Pressure Chemical Ionisation Mass Spectrometry. J. Chromatogr. A. 2001;921:175–185. doi: 10.1016/S0021-9673(01)00871-8. PubMed DOI
Talbot H.M., Summons R., Jahnke L., Farrimond P. Characteristic Fragmentation of Bacteriohopanepolyols during Atmospheric Pressure Chemical Ionisation Liquid Chromatography/Ion Trap Mass Spectrometry. Rapid Commun. Mass Spectrom. 2003;17:2788–2796. doi: 10.1002/rcm.1265. PubMed DOI
Talbot H.M., Rohmer M., Farrimond P. Rapid Structural Elucidation of Composite Bacterial Hopanoids by Atmospheric Pressure Chemical Ionisation Liquid Chromatography/Ion Trap Mass Spectrometry. Rapid Commun. Mass Spectrom. 2007;21:880–892. doi: 10.1002/rcm.2911. PubMed DOI
Talbot H.M., Rohmer M., Farrimond P. Structural Characterisation of Unsaturated Bacterial Hopanoids by Atmospheric Pressure Chemical Ionisation Liquid Chromatography/Ion Trap Mass Spectrometry. Rapid Commun. Mass Spectrom. 2007;21:1613–1622. doi: 10.1002/rcm.2997. PubMed DOI
Talbot H.M., Squier A.H., Keely B.J., Farrimond P. Atmospheric Pressure Chemical Ionisation Reversed-Phase Liquid Chromatography/Ion Trap Mass Spectrometry of Intact Bacteriohopanepolyols. Rapid Commun. Mass Spectrom. 2003;17:728–737. doi: 10.1002/rcm.974. PubMed DOI
Talbot H.M., Watson D.F., Pearson E.J., Farrimond P. Diverse Biohopanoid Compositions of Non-Marine Sediments. Org. Geochem. 2003;34:1353–1371. doi: 10.1016/S0146-6380(03)00159-1. DOI
Talbot H.M., Sidgwick F.R., Bischoff J., Osborne K.A., Rush D., Sherry A., Spencer-Jones C.L. Analysis of Non-Derivatised Bacteriohopanepolyols by Ultrahigh-Performance Liquid Chromatography/Tandem Mass Spectrometry. Rapid Commun. Mass Spectrom. 2016;30:2087–2098. doi: 10.1002/rcm.7696. PubMed DOI
Zarzycki P.K., Portka J.K. Recent Advances in Hopanoids Analysis: Quantification Protocols Overview, Main Research Targets and Selected Problems of Complex Data Exploration. J. Steroid Biochem. Mol. Biol. 2015;153:3–26. doi: 10.1016/j.jsbmb.2015.04.017. PubMed DOI
Rezanka T., Siristova L., Melzoch K., Sigler K. N-Acylated Bacteriohopanehexol-Mannosamides from the Thermophilic Bacterium Alicyclobacillus acidoterrestris. Lipids. 2011;46:249–261. doi: 10.1007/s11745-010-3482-4. PubMed DOI
Bligh E., Dyer W. A Rapid Method of Total Lipid Extraction and Purification. Can. J. Biochem. Physiol. 1959;37:911–917. doi: 10.1139/o59-099. PubMed DOI
Vitova M., Stranska M., Palyzova A., Rezanka T. Detailed Structural Characterization of Cardiolipins from Various Biological Sources Using a Complex Analytical Strategy Comprising Fractionation, Hydrolysis and Chiral Chromatography. J. Chromatogr. A. 2021;1648:462185. doi: 10.1016/j.chroma.2021.462185. PubMed DOI
Talbot H.M., Farrimond P., Schaeffer P., Pancost R.D. Bacteriohopanepolyols in Hydrothermal Vent Biogenic Silicates. Org. Geochem. 2005;36:663–672. doi: 10.1016/j.orggeochem.2004.10.015. DOI
Welander P.V., Coleman M.L., Sessions A.L., Summons R.E., Newman D.K. Identification of a Methylase Required for 2-Methylhopanoid Production and Implications for the Interpretation of Sedimentary Hopanes. Proc. Natl. Acad. Sci. USA. 2010;107:8537–8542. doi: 10.1073/pnas.0912949107. PubMed DOI PMC
Rohmer M., Bouvier-Nave P., Ourisson G. Distribution of Hopanoid Triterpenes in Prokaryotes. Microbiology. 1984;130:1137–1150. doi: 10.1099/00221287-130-5-1137. DOI
Simonin P., Jürgens U.J., Rohmer M. Bacterial Triterpenoids of the Hopane Series from the Prochlorophyte Prochlorothrix hollandica and Their Intracellular Localization. Eur. J. Biochem. 1996;241:865–871. doi: 10.1111/j.1432-1033.1996.00865.x. PubMed DOI
Summons R.E., Jahnke L.L., Hope J.M., Logan G.A. 2-Methylhopanoids as Biomarkers for Cyanobacterial Oxygenic Photosynthesis. Nature. 1999;400:554–557. doi: 10.1038/23005. PubMed DOI
Rashby S.E., Sessions A.L., Summons R.E., Newman D.K. Biosynthesis of 2-Methylbacteriohopanepolyols by an Anoxygenic Phototroph. Proc. Natl. Acad. Sci. USA. 2007;104:15099–15104. doi: 10.1073/pnas.0704912104. PubMed DOI PMC
Zundel M., Rohmer M. Prokaryotic Triterpenoids. Eur. J. Biochem. 1985;150:23–27. doi: 10.1111/j.1432-1033.1985.tb08980.x. PubMed DOI
Welander P.V., Summons R.E. Discovery, Taxonomic Distribution, and Phenotypic Characterization of a Gene Required for 3-Methylhopanoid Production. Proc. Natl. Acad. Sci. USA. 2012;109:12905–12910. doi: 10.1073/pnas.1208255109. PubMed DOI PMC
Elvert M., Niemann H. Occurrence of Unusual Steroids and Hopanoids Derived from Aerobic Methanotrophs at an Active Marine Mud Volcano. Org. Geochem. 2008;39:167–177. doi: 10.1016/j.orggeochem.2007.11.006. DOI
Damsté J.S.S., Rijpstra W.I.C., Dedysh S.N., Foesel B.U., Villanueva L. Pheno- and Genotyping of Hopanoid Production in Acidobacteria. Front. Microbiol. 2017;8:968. doi: 10.3389/fmicb.2017.00968. PubMed DOI PMC
Seemann M., Bisseret P., Tritz J.-P., Hooper A.B., Rohmer M. Novel Bacterial Triterpenoids of the Hopane Series from Nitrosomonas europaea and Their Significance for the Formation of the C35 Bacteriohopane Skeleton. Tetrahedron Lett. 1999;40:1681–1684. doi: 10.1016/S0040-4039(99)00064-7. DOI
Neunlist S., Holst O., Rohmer M. Prokaryotic Triterpenoids—the Hopanoids of the Purple Non-Sulfur Bacterium Rhodomicrobium vannielii—an Aminotriol and Its Aminoacyl Derivatives, N-Tryptophanyl and N-Ornithinyl Aminotriol. Eur. J. Biochem. 1985;147:561–568. doi: 10.1111/j.0014-2956.1985.00561.x. PubMed DOI
Bradley A.S., Pearson A., Saenz J.P., Marx C.J. Adenosylhopane: The First Intermediate in Hopanoid Side Chain Biosynthesis. Org. Geochem. 2010;41:1075–1081. doi: 10.1016/j.orggeochem.2010.07.003. DOI
Kannenberg E.L., Poralla K. Hopanoid Biosynthesis and Function in Bacteria. Naturwissenschaften. 1999;86:168–176. doi: 10.1007/s001140050592. DOI
Welander P.V., Hunter R.C., Zhang L., Sessions A.L., Summons R.E., Newman D.K. Hopanoids Play a Role in Membrane Integrity and pH Homeostasis in Rhodopseudomonas palustris TIE-1. J. Bacteriol. 2009;191:6145–6156. doi: 10.1128/JB.00460-09. PubMed DOI PMC
van Winden J.F., Reichart G.-J., McNamara N.P., Benthien A., Damste J.S.S. Temperature-Induced Increase in Methane Release from Peat Bogs: A Mesocosm Experiment. PLoS ONE. 2012;7:e39614. doi: 10.1371/journal.pone.0039614. PubMed DOI PMC
van Winden J.F., Talbot H.M., Kip N., Reichart G.-J., Pol A., McNamara N.P., Jetten M.S.M., Op den Camp H.J.M., Sinninghe Damsté J.S. Bacteriohopanepolyol Signatures as Markers for Methanotrophic Bacteria in Peat Moss. Geochim. Cosmochim. Acta. 2012;77:52–61. doi: 10.1016/j.gca.2011.10.026. DOI
Osborne K.A., Gray N.D., Sherry A., Leary P., Mejeha O., Bischoff J., Rush D., Sidgwick F.R., Birgel D., Kalyuzhnaya M.G., et al. Methanotroph-Derived Bacteriohopanepolyol Signatures as a Function of Temperature Related Growth, Survival, Cell Death and Preservation in the Geological Record. Environ. Microbiol. Rep. 2017;9:492–500. doi: 10.1111/1758-2229.12570. PubMed DOI
Jahnke L.L., Summons R.E., Hope J.M., Marais D.J.D. Carbon Isotopic Fractionation in Lipids from Methanotrophic Bacteria II: The Effects of Physiology and Environmental Parameters on the Biosynthesis and Isotopic Signatures of Biomarkers. Geochim. Cosmochim. Acta. 1999;63:79–93. doi: 10.1016/S0016-7037(98)00270-1. PubMed DOI
Bale N.J., Rijpstra W.I.C., Sahonero-Canavesi D.X., Oshkin I.Y., Belova S.E., Dedysh S.N., Sinninghe Damsté J.S. Fatty Acid and Hopanoid Adaption to Cold in the Methanotroph Methylovulum psychrotolerans. Front. Microbiol. 2019;10:589. doi: 10.3389/fmicb.2019.00589. PubMed DOI PMC
Schmidt A., Bringer-Meyer S., Poralla K., Sahm H. Effect of Alcohols and Temperature on the Hopanoid Content of Zymomonas mobilis. Appl. Microbiol. Biotechnol. 1986;25:32–36. doi: 10.1007/BF00252509. DOI
Joyeux C., Fouchard S., Llopiz P., Neunlist S. Influence of the Temperature and the Growth Phase on the Hopanoids and Fatty Acids Content of Frateuria aurantia (DSMZ 6220) FEMS Microbiol. Ecol. 2004;47:371–379. doi: 10.1016/S0168-6496(03)00302-7. PubMed DOI
Cvejic J.H., Bodrossy L., Kovács K.L., Rohmer M. Bacterial Triterpenoids of the Hopane Series from the Methanotrophic Bacteria Methylocaldum spp.: Phylogenetic Implications and First Evidence for an Unsaturated Aminobacteriohopanepolyol. FEMS Microbiol. Lett. 2000;182:361–365. doi: 10.1111/j.1574-6968.2000.tb08922.x. PubMed DOI
Flesch G., Rohmer M. Prokaryotic Hopanoids—the Biosynthesis of the Bacteriohopane Skeleton—Formation of Isoprenic Units from 2 Distinct Acetate Pools and a Novel Type of Carbon Carbon Linkage between a Triterpene and D-Ribose. Eur. J. Biochem. 1988;175:405–411. doi: 10.1111/j.1432-1033.1988.tb14210.x. PubMed DOI
Pearson A., Leavitt W.D., Saenz J.P., Summons R.E., Tam M.C.-M., Close H.G. Diversity of Hopanoids and Squalene-Hopene Cyclases across a Tropical Land-Sea Gradient. Environ. Microbiol. 2009;11:1208–1223. doi: 10.1111/j.1462-2920.2008.01817.x. PubMed DOI
Pearson A., Page S.R.F., Jorgenson T.L., Fischer W.W., Higgins M.B. Novel Hopanoid Cyclases from the Environment. Environ. Microbiol. 2007;9:2175–2188. doi: 10.1111/j.1462-2920.2007.01331.x. PubMed DOI