Plasmalogen Biosynthesis by Anaerobic Bacteria: Identification of a Two-Gene Operon Responsible for Plasmalogen Production in

Overview

Journal ACS Chem Biol

Publisher American Chemical Society

Specialties Biochemistry
Biology

Date 2020 Dec 22

PMID 33350306

Citations 24

Authors

David R Jackson

Chelsi D Cassilly

Damian R Plichta

Hera Vlamakis

Hualan Liu

Stephen B Melville

Ramnik J Xavier

Jon Clardy

Affiliations

Soon will be listed here.

Abstract

Plasmalogens are vinyl ether-containing lipids produced by mammals and bacteria. The aerobic biosynthetic pathway in eukaryotes and bacteria is known, but the anaerobic pathway has remained a mystery. Here, we describe a two-gene operon (plasmalogen synthase, ) responsible for plasmalogen production in the anaerobic bacterium . While aerobic plasmalogen biosynthesis involves an oxidative conversion of an ether to a vinyl ether, anaerobic plasmalogen biosynthesis uses the reductive conversion of an ester to an aldehyde equivalent. Heterologous expression of the operon in conferred the ability to produce plasmalogens. The operon is predicted to encode a multidomain complex similar to benzoyl-CoA reductase/hydroxylacyl-CoA dehydratase (BCR/HAD) enzymes. Versions of this operon can be found in a wide range of obligate and facultative anaerobic bacteria, including many human gut microbes.

Citing Articles

Discovering Hidden Archaeal and Bacterial Lipid Producers in a Euxinic Marine System.

Boukhchtaber D, von Meijenfeldt F, Sahonero Canavesi D, Dorhout D, Bale N, Hopmans E Environ Microbiol. 2025; 27(3):e70054.

PMID: 40016913 PMC: 11868695. DOI: 10.1111/1462-2920.70054.

Association between seizure reduction during ketogenic diet treatment of epilepsy and changes in circulatory metabolites and gut microbiota composition.

Dahlin M, Wheelock C, Prast-Nielsen S EBioMedicine. 2024; 109():105400.

PMID: 39500011 PMC: 11570732. DOI: 10.1016/j.ebiom.2024.105400.

The presence of plasmenyl ether lipids in suggests a premetazoan origin of plasmalogen biosynthesis in animals.

Costa J, Gabrielli M, Altabe S, Uttaro A Heliyon. 2024; 10(12):e32807.

PMID: 38975177 PMC: 11225845. DOI: 10.1016/j.heliyon.2024.e32807.

Homeocurvature adaptation of phospholipids to pressure in deep-sea invertebrates.

Winnikoff J, Milshteyn D, Vargas-Urbano S, Pedraza-Joya M, Armando A, Quehenberger O Science. 2024; 384(6703):1482-1488.

PMID: 38935710 PMC: 11593575. DOI: 10.1126/science.adm7607.

Gut microbiota, blood metabolites, and left ventricular diastolic dysfunction in US Hispanics/Latinos.

Luo K, Taryn A, Moon E, Peters B, Solomon S, Daviglus M Microbiome. 2024; 12(1):85.

PMID: 38725043 PMC: 11084054. DOI: 10.1186/s40168-024-01797-x.

References

Fiore E, Van Tyne D, Gilmore M . Pathogenicity of Enterococci. Microbiol Spectr. 2019; 7(4). PMC: 6629438. DOI: 10.1128/microbiolspec.GPP3-0053-2018. View

Goldfine H . The anaerobic biosynthesis of plasmalogens. FEBS Lett. 2017; 591(18):2714-2719. DOI: 10.1002/1873-3468.12714. View

Goldfine H . The appearance, disappearance and reappearance of plasmalogens in evolution. Prog Lipid Res. 2010; 49(4):493-8. DOI: 10.1016/j.plipres.2010.07.003. View

Werner E, Keller M, Sailer S, Lackner K, Koch J, Hermann M . The gene encodes plasmanylethanolamine desaturase which introduces the characteristic vinyl ether double bond into plasmalogens. Proc Natl Acad Sci U S A. 2020; 117(14):7792-7798. PMC: 7149458. DOI: 10.1073/pnas.1917461117. View

Nagan N, Zoeller R . Plasmalogens: biosynthesis and functions. Prog Lipid Res. 2001; 40(3):199-229. DOI: 10.1016/s0163-7827(01)00003-0. View

Pasolli E, Asnicar F, Manara S, Zolfo M, Karcher N, Armanini F . Extensive Unexplored Human Microbiome Diversity Revealed by Over 150,000 Genomes from Metagenomes Spanning Age, Geography, and Lifestyle. Cell. 2019; 176(3):649-662.e20. PMC: 6349461. DOI: 10.1016/j.cell.2019.01.001. View

Boll M . Key enzymes in the anaerobic aromatic metabolism catalysing Birch-like reductions. Biochim Biophys Acta. 2005; 1707(1):34-50. DOI: 10.1016/j.bbabio.2004.01.009. View

Braverman N, Moser A . Functions of plasmalogen lipids in health and disease. Biochim Biophys Acta. 2012; 1822(9):1442-52. DOI: 10.1016/j.bbadis.2012.05.008. View

Johnston N, Baker J, Goldfine H . Phospholipids of Clostridium perfringens: a reexamination. FEMS Microbiol Lett. 2004; 233(1):65-8. DOI: 10.1016/j.femsle.2004.01.048. View

10.

Liu H, Bouillaut L, Sonenshein A, Melville S . Use of a mariner-based transposon mutagenesis system to isolate Clostridium perfringens mutants deficient in gliding motility. J Bacteriol. 2012; 195(3):629-36. PMC: 3554012. DOI: 10.1128/JB.01288-12. View

11.

Han X, Holtzman D, McKeel Jr D . Plasmalogen deficiency in early Alzheimer's disease subjects and in animal models: molecular characterization using electrospray ionization mass spectrometry. J Neurochem. 2001; 77(4):1168-80. DOI: 10.1046/j.1471-4159.2001.00332.x. View

12.

Zou Y, Palte M, Deik A, Li H, Eaton J, Wang W . A GPX4-dependent cancer cell state underlies the clear-cell morphology and confers sensitivity to ferroptosis. Nat Commun. 2019; 10(1):1617. PMC: 6453886. DOI: 10.1038/s41467-019-09277-9. View

13.

Hill E, Lands W . Formation of acyl and alkenyl glycerol derivatives in Clostridium butyricum. Biochim Biophys Acta. 1970; 202(1):209-11. DOI: 10.1016/0005-2760(70)90239-0. View

14.

Dean J, Lodhi I . Structural and functional roles of ether lipids. Protein Cell. 2017; 9(2):196-206. PMC: 5818364. DOI: 10.1007/s13238-017-0423-5. View

15.

Nariya H, Miyata S, Suzuki M, Tamai E, Okabe A . Development and application of a method for counterselectable in-frame deletion in Clostridium perfringens. Appl Environ Microbiol. 2010; 77(4):1375-82. PMC: 3067250. DOI: 10.1128/AEM.01572-10. View

16.

Jones P, Binns D, Chang H, Fraser M, Li W, McAnulla C . InterProScan 5: genome-scale protein function classification. Bioinformatics. 2014; 30(9):1236-40. PMC: 3998142. DOI: 10.1093/bioinformatics/btu031. View

17.

Buckel W, Kung J, Boll M . The benzoyl-coenzyme a reductase and 2-hydroxyacyl-coenzyme a dehydratase radical enzyme family. Chembiochem. 2014; 15(15):2188-94. DOI: 10.1002/cbic.201402270. View

18.

Kim J, Hetzel M, Boiangiu C, Buckel W . Dehydration of (R)-2-hydroxyacyl-CoA to enoyl-CoA in the fermentation of alpha-amino acids by anaerobic bacteria. FEMS Microbiol Rev. 2004; 28(4):455-68. DOI: 10.1016/j.femsre.2004.03.001. View

19.

Paltauf F . Plasmalogen biosynthesis in a cell-free system. Enzymic desaturation of 1-O-alkyl (2-acyl) glycerophosphoryl ethanolamine. FEBS Lett. 1972; 20(1):79-82. DOI: 10.1016/0014-5793(72)80021-8. View

20.

Buckel W . Enzymatic Reactions Involving Ketyls: From a Chemical Curiosity to a General Biochemical Mechanism. Biochemistry. 2019; 58(52):5221-5233. DOI: 10.1021/acs.biochem.9b00171. View