• This record comes from PubMed

Analysis of Bacteriohopanoids from Thermophilic Bacteria by Liquid Chromatography-Mass Spectrometry

. 2021 Sep 30 ; 9 (10) : . [epub] 20210930

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

Links

PubMed 34683383
PubMed Central PMC8537080
DOI 10.3390/microorganisms9102062
PII: microorganisms9102062
Knihovny.cz E-resources

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.

See more in PubMed

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

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...