Interfacial Enzymes Enable Gram-Positive Microbes to Eat Fatty Acids
Abstract
1. Introduction
1.1. Protein–Membrane Association
1.2. Interfacial Enzymes
1.3. Membrane Binding Experimental Methods
2. Bacterial Fatty Acid Metabolism
2.1. Bacterial Phospholipid Synthesis
2.2. Acyl-ACP:Phosphate Transacylase (PlsX)
2.3. Fatty Acid Kinase (FakAB)
3. Conclusions
4. Discussion
Funding
Data Availability Statement
Conflicts of Interest
References
- Strahl, H.; Errington, J. Bacterial membranes: Structure, domains, and function. Annu. Rev. Microbiol. 2017, 71, 519–538. [Google Scholar] [CrossRef] [PubMed]
- Lu, G.; Xu, Y.; Zhang, K.; Xiong, Y.; Li, H.; Cui, L.; Wang, X.; Lou, J.; Zhai, Y.; Sun, F.; et al. Crystal structure of E. coli apolipoprotein N-acyl transferase. Nat. Commun. 2017, 8, 15948. [Google Scholar] [CrossRef]
- Gardiner, J.H.t.; Komazin, G.; Matsuo, M.; Cole, K.; Gotz, F.; Meredith, T.C. Lipoprotein N-Acylation in Staphylococcus aureus Is Catalyzed by a Two-Component Acyl Transferase System. mBio 2020, 11, 01619–01620. [Google Scholar] [CrossRef] [PubMed]
- Chen, X.; Alonzo, F., 3rd. Bacterial lipolysis of immune-activating ligands promotes evasion of innate defenses. Proc. Natl. Acad. Sci. USA 2019, 116, 3764–3773. [Google Scholar] [CrossRef] [PubMed]
- Seelig, J. Thermodynamics of lipid-peptide interactions. Biochim. Biophys. Acta 2004, 1666, 40–50. [Google Scholar] [CrossRef] [PubMed]
- Whited, A.M.; Johs, A. The interactions of peripheral membrane proteins with biological membranes. Chem. Phys. Lipids 2015, 192, 51–59. [Google Scholar] [CrossRef] [PubMed]
- Malmberg, N.J.; Van Buskirk, D.R.; Falke, J.J. Membrane-docking loops of the cPLA2 C2 domain: Detailed structural analysis of the protein-membrane interface via site-directed spin-labeling. Biochemistry 2003, 42, 13227–13240. [Google Scholar] [CrossRef] [PubMed]
- Gamsjaeger, R.; Johs, A.; Gries, A.; Gruber, H.J.; Romanin, C.; Prassl, R.; Hinterdorfer, P. Membrane binding of β2-glycoprotein I can be described by a two-state reaction model: An atomic force microscopy and surface plasmon resonance study. Biochem. J. 2005, 389, 665–673. [Google Scholar] [CrossRef]
- Verma, M.L.; Azmi, W.; Kanwar, S.S. Microbial lipases: At the interface of aqueous and non-aqueous media. A review. Acta Microbiol. Immunol. Hung. 2008, 55, 265–294. [Google Scholar] [CrossRef]
- Del Vecchio, K.; Stahelin, R.V. Using Surface Plasmon Resonance to Quantitatively Assess Lipid-Protein Interactions. Methods Mol. Biol. 2016, 1376, 141–153. [Google Scholar] [CrossRef]
- Sahu, I.D.; Lorigan, G.A. Electron paramagnetic resonance as a tool for studying membrane proteins. Biomolecules 2020, 10, 763. [Google Scholar] [CrossRef] [PubMed]
- Smirnova, T.I.; Smirnov, A.I. Peptide-membrane interactions by spin-labeling EPR. Methods Enzymol. 2015, 564, 219–258. [Google Scholar] [CrossRef] [PubMed]
- Opella, S.J.; Marassi, F.M. Applications of NMR to membrane proteins. Arch. Biochem. Biophys. 2017, 628, 92–101. [Google Scholar] [CrossRef] [PubMed]
- Oxenoid, K.; Chou, J.J. A functional NMR for membrane proteins: Dynamics, ligand binding, and allosteric modulation. Protein Sci. 2016, 25, 959–973. [Google Scholar] [CrossRef]
- Pant, S.; Tajkhorshid, E. Microscopic characterization of GRP1 PH domain interaction with anionic membranes. J. Comput. Chem. 2020, 41, 489–499. [Google Scholar] [CrossRef]
- Gullett, J.M.; Cuypers, M.G.; Grace, C.R.; Pant, S.; Subramanian, C.; Tajkhorshid, E.; Rock, C.O.; White, S.W. Identification of structural transitions in bacterial fatty acid binding proteins that permit ligand entry and exit at membranes. J. Biol. Chem. 2022, 298, 101676. [Google Scholar] [CrossRef]
- Parsons, J.B.; Rock, C.O. Bacterial lipids: Metabolism and membrane homeostasis. Prog. Lipid Res. 2013, 52, 249–276. [Google Scholar] [CrossRef]
- White, S.W.; Zheng, J.; Zhang, Y.-M.; Rock, C.O. The structural biology of type II fatty acid biosynthesis. Annu. Rev. Biochem. 2005, 74, 791–831. [Google Scholar] [CrossRef]
- Radka, C.D.; Rock, C.O. Mining fatty acid biosynthesis for new antimicrobials. Annu. Rev. Microbiol. 2022, 76, 281–304. [Google Scholar] [CrossRef]
- Wittke, F.; Vincent, C.; Chen, J.; Heller, B.; Kabler, H.; Overcash, J.S.; Leylavergne, F.; Dieppois, G. Afabicin, a first-in-class antistaphylococcal antibiotic, in the treatment of acute bacterial skin and skin structure infections: Clinical noninferiority to vancomycin/linezolid. Antimicrob. Agents Chemother. 2020, 64, e00250-20. [Google Scholar] [CrossRef]
- Vuong, C.; Yeh, A.J.; Cheung, G.Y.; Otto, M. Investigational drugs to treat methicillin-resistant Staphylococcus aureus. Expert Opin. Investig. Drugs 2016, 25, 73–93. [Google Scholar] [CrossRef]
- Quehenberger, O.; Dennis, E.A. The human plasma lipidome. N. Engl. J. Med. 2011, 365, 1812–1823. [Google Scholar] [CrossRef] [PubMed]
- Radka, C.D.; Batte, J.L.; Frank, M.W.; Rosch, J.W.; Rock, C.O. Oleate hydratase (OhyA) is a virulence determinant in Staphylococcus aureus. Microbiol. Spectr. 2021, 9, e0154621. [Google Scholar] [CrossRef]
- Brinster, S.; Lamberet, G.; Staels, B.; Trieu-Cuot, P.; Gruss, A.; Poyart, C. Type II fatty acid synthesis is not a suitable antibiotic target for Gram-positive pathogens. Nature 2009, 458, 83–86. [Google Scholar] [CrossRef] [PubMed]
- Morvan, C.; Halpern, D.; Kenanian, G.; Pathania, A.; Anba-Mondoloni, J.; Lamberet, G.; Gruss, A.; Gloux, K. The Staphylococcus aureus FASII bypass escape route from FASII inhibitors. Biochimie 2017, 141, 40–46. [Google Scholar] [CrossRef]
- Kenanian, G.; Morvan, C.; Weckel, A.; Pathania, A.; Anba-Mondoloni, J.; Halpern, D.; Gaillard, M.; Solgadi, A.; Dupont, L.; Henry, C.; et al. Permissive fatty acid incorporation promotes staphylococcal adaptation to FASII antibiotics in host environments. Cell Rep. 2019, 29, 3974–3982.e3974. [Google Scholar] [CrossRef]
- Balemans, W.; Lounis, N.; Gilissen, R.; Guillemont, J.; Simmen, K.; Andries, K.; Koul, A. Essentiality of FASII pathway for Staphylococcus aureus. Nature 2010, 463, E3, discussion E4. [Google Scholar] [CrossRef] [PubMed]
- Antimicrobial Resistance, C. Global burden of bacterial antimicrobial resistance in 2019: A systematic analysis. Lancet 2022, 399, 629–655. [Google Scholar] [CrossRef]
- Lu, Y.-J.; Zhang, Y.-M.; Grimes, K.D.; Qi, J.; Lee, R.E.; Rock, C.O. Acyl-phosphates initiate membrane phospholipid synthesis in Gram-positive pathogens. Mol. Cell 2006, 23, 765–772. [Google Scholar] [CrossRef] [PubMed]
- Yao, J.; Rock, C.O. Phosphatidic acid synthesis in bacteria. Biochim. Biophys. Acta 2013, 1831, 495–502. [Google Scholar] [CrossRef] [PubMed]
- Paoletti, L.; Lu, Y.-J.; Schujman, G.E.; de Mendoza, D.; Rock, C.O. Coupling of fatty acid and phospholipid synthesis in Bacillus subtilis. J. Bacteriol. 2007, 189, 5816–5824. [Google Scholar] [CrossRef]
- Zhang, Y.-M.; Rock, C.O. Acyltransferases in bacterial glycerophospholipid synthesis. J. Lipid Res 2008, 49, 1867–1874. [Google Scholar] [CrossRef] [PubMed]
- Parsons, J.B.; Broussard, T.C.; Bose, J.L.; Rosch, J.W.; Jackson, P.; Subramanian, C.; Rock, C.O. Identification of a two-component fatty acid kinase responsible for host fatty acid incorporation by Staphylococcus aureus. Proc. Natl. Acad. Sci. USA 2014, 111, 10532–10537. [Google Scholar] [CrossRef]
- Li, Z.; Tang, Y.; Wu, Y.; Zhao, S.; Bao, J.; Luo, Y.; Li, D. Structural insights into the committed step of bacterial phospholipid biosynthesis. Nat. Commun. 2017, 8, 1691. [Google Scholar] [CrossRef] [PubMed]
- Robertson, R.M.; Yao, J.; Gajewski, S.; Kumar, G.; Martin, E.W.; Rock, C.O.; White, S.W. A two-helix motif positions the lysophosphatidic acid acyltransferase active site for catalysis within the membrane bilayer. Nat. Struct. Mol. Biol. 2017, 24, 666–671. [Google Scholar] [CrossRef] [PubMed]
- Jiang, Y.; Dai, X.; Qin, M.; Guo, Z. Identification of an amphipathic peptide sensor of the Bacillus subtilis fluid membrane microdomains. Commun. Biol. 2019, 2, 316. [Google Scholar] [CrossRef]
- Sastre, D.E.; Bisson-Filho, A.; de Mendoza, D.; Gueiros-Filho, F.J. Revisiting the cell biology of the acyl-ACP: Phosphate transacylase PlsX suggests that the phospholipid synthesis and cell division machineries are not coupled in Bacillus subtilis. Mol. Microbiol. 2016, 100, 621–634. [Google Scholar] [CrossRef]
- Badger, J.; Sauder, J.M.; Adams, J.M.; Antonysamy, S.; Bain, K.; Bergseid, M.G.; Buchanan, S.G.; Buchanan, M.D.; Batiyenko, Y.; Christopher, J.A.; et al. Structural analysis of a set of proteins resulting from a bacterial genomics project. Proteins 2005, 60, 787–796. [Google Scholar] [CrossRef]
- Kim, Y.; Li, H.; Binkowski, T.A.; Holzle, D.; Joachimiak, A. Crystal structure of fatty acid/phospholipid synthesis protein PlsX from Enterococcus faecalis. J. Struct. Funct. Genomics 2009, 10, 157–163. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Sastre, D.E.; Pulschen, A.A.; Basso, L.G.M.; Benites Pariente, J.S.; Marques Netto, C.G.C.; Machinandiarena, F.; Albanesi, D.; Navarro, M.; de Mendoza, D.; Gueiros-Filho, F.J. The phosphatidic acid pathway enzyme PlsX plays both catalytic and channeling roles in bacterial phospholipid synthesis. J. Biol. Chem. 2020, 295, 2148–2159. [Google Scholar] [CrossRef] [PubMed]
- Sastre, D.E.; Basso, L.G.M.; Trastoy, B.; Cifuente, J.O.; Contreras, X.; Gueiros-Filho, F.; de Mendoza, D.; Navarro, M.; Guerin, M.E. Membrane fluidity adjusts the insertion of the transacylase PlsX to regulate phospholipid biosynthesis in Gram-positive bacteria. J. Biol. Chem. 2020, 295, 2136–2147. [Google Scholar] [CrossRef]
- Subramanian, C.; Cuypers, M.G.; Radka, C.D.; White, S.W.; Rock, C.O. Domain architecture and catalysis of the Staphylococcus aureus fatty acid kinase. J. Biol. Chem. 2022, 298, 101993. [Google Scholar] [CrossRef] [PubMed]
- Shi, Y.; Zang, N.; Lou, N.; Xu, Y.; Sun, J.; Huang, M.; Zhang, H.; Lu, H.; Zhou, C.; Feng, Y. Structure and mechanism for streptococcal fatty acid kinase (Fak) system dedicated to host fatty acid scavenging. Sci. Adv. 2022, 8, eabq3944. [Google Scholar] [CrossRef] [PubMed]
- Gullett, J.M.; Cuypers, M.G.; Frank, M.W.; White, S.W.; Rock, C.O. A fatty acid-binding protein of Streptococcus pneumoniae facilitates the acquisition of host polyunsaturated fatty acids. J. Biol. Chem. 2019, 294, 16416–16428. [Google Scholar] [CrossRef] [PubMed]
- Cuypers, M.G.; Subramanian, C.; Gullett, J.M.; Frank, M.W.; White, S.W.; Rock, C.O. Acyl chain selectivity and physiological roles of Staphylococcus aureus fatty acid binding proteins. J. Biol. Chem. 2019, 294, 38–49. [Google Scholar] [CrossRef]
- Broussard, T.C.; Miller, D.J.; Jackson, P.; Nourse, A.; White, S.W.; Rock, C.O. Biochemical roles for conserved residues in the bacterial fatty acid binding protein family. J. Biol. Chem. 2016, 291, 6292–6303. [Google Scholar] [CrossRef]
- Bhardwaj, N.; Stahelin, R.V.; Langlois, R.E.; Cho, W.; Lu, H. Structural bioinformatics prediction of membrane-binding proteins. J. Mol. Biol. 2006, 359, 486–495. [Google Scholar] [CrossRef]
- Chatzigoulas, A.; Cournia, Z. Predicting protein-membrane interfaces of peripheral membrane proteins using ensemble machine learning. Brief. Bioinform. 2022, 23, bbab518. [Google Scholar] [CrossRef]
- Chatzigoulas, A.; Cournia, Z. DREAMM: A web-based server for drugging protein-membrane interfaces as a novel workflow for targeted drug design. Bioinformatics 2022, 38, 5449–5451. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Radka, C.D. Interfacial Enzymes Enable Gram-Positive Microbes to Eat Fatty Acids. Membranes 2023, 13, 423. https://doi.org/10.3390/membranes13040423
Radka CD. Interfacial Enzymes Enable Gram-Positive Microbes to Eat Fatty Acids. Membranes. 2023; 13(4):423. https://doi.org/10.3390/membranes13040423
Chicago/Turabian StyleRadka, Christopher D. 2023. "Interfacial Enzymes Enable Gram-Positive Microbes to Eat Fatty Acids" Membranes 13, no. 4: 423. https://doi.org/10.3390/membranes13040423
APA StyleRadka, C. D. (2023). Interfacial Enzymes Enable Gram-Positive Microbes to Eat Fatty Acids. Membranes, 13(4), 423. https://doi.org/10.3390/membranes13040423