The Fe-S cluster biosynthesis in Enterococcus faecium is essential for anaerobic growth and gastrointestinal colonization

References

• Pöntinen AK, Top J, Arredondo-Alonso S, Tonkin-Hill G, Freitas AR, Novais C, Gladstone RA, Pesonen M, Meneses R, Pesonen H, et al. Apparent nosocomial adaptation of Enterococcus faecalis predates the modern hospital era. Nat Commun. 2021;12(1):1523. doi:10.1038/s41467-021-21749-5.
   PubMed Web of Science ®Google Scholar
• García-Solache M, Rice LB. The Enterococcus: a model of adaptability to its environment. Clin Microbiol Rev. 2019;32(2):e00058–17. doi:10.1128/cmr.00058-18.
   PubMed Web of Science ®Google Scholar
• Krawczyk B, Wityk P, Galecka M, Michalik M. The many faces of Enterococcus spp — commensal, probiotic, and opportunistic pathogen. Microorganisms. 2021;9(9):1900. doi:10.3390/microorganisms9091900.
   PubMed Web of Science ®Google Scholar
• Gilmore MS, Willems RJ, Lebreton F. Enterococcus diversity, origins in nature, and gut colonization. Enterococci: from commensals to leading causes of drug-resistant infection. 2014. [Internet]. Available online. https://www.ncbi.nlm.nih.gov/books/NBK190427/.
   Google Scholar
• Facklam R, Collins M. Identification of Enterococcus species isolated from human infections by a conventional test scheme. J Clin Microbiol. 1989;27(4):731–734. doi:10.1128/jcm.27.4.731-734.1989.
   PubMed Web of Science ®Google Scholar
• Bradley C, Fraise A. Heat and chemical resistance of enterococci. J Hosp Infect. 1996;34(3):191–196. doi:10.1016/S0195-6701(96)90065-1.
   PubMed Web of Science ®Google Scholar
• Boucher HW, Talbot GH, Bradley JS, Edwards JE, Gilbert D, Rice LB, Scheld M, Spellberg B, Bartlett J. Bad bugs, no drugs: no ESKAPE! An update from the infectious diseases society of America. Clin Infect Dis. 2009;48(1):1–12. doi:10.1086/595011.
   PubMed Web of Science ®Google Scholar
• Arias CA, Murray BE. The rise of the Enterococcus: beyond vancomycin resistance. Nat Rev Microbiol. 2012;10(4):266–278. doi:10.1038/nrmicro2761.
   PubMed Web of Science ®Google Scholar
• Zhang XL, Bierschenk D, Top J, Anastasiou I, Bonten MJM, Willems RJL, van Schaik W, Dyer TD, Comuzzie A, Curran JE. Functional genomic analysis of bile salt resistance in Enterococcus faecium. BMC Genomics. 2013;6(1):14. doi:10.1186/1755-8794-6-14.
   Google Scholar
• Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. Host-bacterial mutualism in the human intestine. Science. 2005;307(5717):1915–1920. doi:10.1126/science.1104816.
   PubMed Web of Science ®Google Scholar
• Jones SA, Gibson T, Maltby RC, Chowdhury FZ, Stewart V, Cohen PS, Conway T. Anaerobic respiration of Escherichia coli in the mouse intestine. Infect Immun. 2011;79(10):4218–4226. doi:10.1128/iai.05395-11.
   PubMed Web of Science ®Google Scholar
• Hooper LV, Wong MH, Thelin A, Hansson L, Falk PG, Gordon JI. Molecular analysis of commensal host-microbial relationships in the intestine. Science. 2001;291(5505):881–884. doi:10.1126/science.291.5505.881.
   PubMed Web of Science ®Google Scholar
• Wilson M. Microbial inhabitants of humans: their ecology and role in health and disease. Cambridge (UK): Cambridge University Press; 2005. p. 1–50. ISBN 9780511735080.
   Google Scholar
• Savage DC. Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol. 1977;3(12):107–133. doi:10.1146/annurev.mi.31.100177.000543.
   Google Scholar
• Jones SA, Chowdhury FZ, Fabich AJ, Anderson A, Schreiner DM, House AL, Autieri SM, Leatham MP, Lins JJ, Jorgensen M, et al. Respiration of Escherichia coli in the mouse intestine. Infect Immun. 2007;75(10):4891–4899. doi:10.1128/iai.00484-07.
   PubMed Web of Science ®Google Scholar
• Marteyn B, West NP, Browning DF, Cole JA, Shaw JG, Palm F, Mounier J, Prévost M-C, Sansonetti P, Tang CM, et al. Modulation of Shigella virulence in response to available oxygen in vivo. Nature. 2010;465(7296):355–U113. doi:10.1038/nature08970.
   PubMed Web of Science ®Google Scholar
• Caballero-Flores G, Pickard JM, Núñez G. Microbiota-mediated colonization resistance: mechanisms and regulation. Nat Rev Microbiol. 2023;21(6):347–360. doi:10.1038/s41579-022-00833-7.
   PubMed Web of Science ®Google Scholar
• Litvak Y, Byndloss MX, Tsolis RM, Bäumler AJ. Dysbiotic Proteobacteria expansion: a microbial signature of epithelial dysfunction. Curr Opin Microbiol. 2017;39:1–6. doi:10.1016/j.mib.2017.07.003.
   PubMed Web of Science ®Google Scholar
• Winter SE, Winter MG, Xavier MN, Thiennimitr P, Poon V, Keestra AM, Laughlin RC, Gomez G, Wu J, Lawhon SD, et al. Host-derived nitrate boosts growth of E. coli in the inflamed gut. Science. 2013;339(6120):708–711. doi:10.1126/science.1232467.
   PubMed Web of Science ®Google Scholar
• Spees AM, Wangdi T, Lopez CA, Kingsbury DD, Xavier MN, Winter SE, Tsolis RM, Bäumler AJ. Streptomycin-induced inflammation enhances Escherichia coli gut colonization through nitrate respiration. Mbio. 2013;4(4):e00430–13. doi:10.1128/mbio.00430-13.
   PubMed Web of Science ®Google Scholar
• Herp S, Brugiroux S, Garzetti D, Ring D, Jochum LM, Beutler M, Eberl C, Hussain S, Walter S, Gerlach RG, et al. Mucispirillum schaedleri antagonizes salmonella virulence to protect mice against colitis. Cell Host Microbe. 2019;25(5):681–694.e8. doi:10.1016/j.chom.2019.03.004.
   PubMed Web of Science ®Google Scholar
• Rivera-Chávez F, Lopez CA, Bäumler AJ. Oxygen as a driver of gut dysbiosis. Freeradicalbiomed. 2017;105:93–101. doi:10.1016/j.freeradbiomed.2016.09.022.
   PubMed Web of Science ®Google Scholar
• Kelly CJ, Colgan SP. Breathless in the gut: implications of luminal O2 for microbial pathogenicity. Cell Host Microbe. 2016;19(4):427–428. doi:10.1016/j.chom.2016.03.014.
   PubMed Web of Science ®Google Scholar
• van Opijnen T, Bodi KL, Camilli A. Tn-seq: high-throughput parallel sequencing for fitness and genetic interaction studies in microorganisms. Nat Methods. 2009;6(10):767–U21. doi:10.1038/NMETH.1377.
   PubMed Web of Science ®Google Scholar
• Cain AK, Barquist L, Goodman AL, Paulsen IT, Parkhill J, van Opijnen T. A decade of advances in transposon-insertion sequencing. Nat Rev Genet. 2020;21(9):526–540. doi:10.1038/s41576-020-0244-x.
   PubMed Web of Science ®Google Scholar
• Powell JE, Leonard SP, Kwong WK, Engel P, Moran NA. Genome-wide screen identifies host colonization determinants in a bacterial gut symbiont. P Natl Acad Sci USA. 2016;113(48):13887–13892. doi:10.1073/pnas.1610856113.
   PubMed Web of Science ®Google Scholar
• Caballero-Flores G, Pickard JM, Fukuda S, Inohara N, Núñez G. An enteric pathogen subverts colonization resistance by evading competition for amino acids in the gut. Cell Host Microbe. 2020;28(4):526±. doi:10.1016/j.chom.2020.06.018.
   PubMed Web of Science ®Google Scholar
• Wang H, Xing XL, Wang JP, Pang B, Liu M, Larios-Valencia J, Liu T, Liu G, Xie S, Hao G, et al. Hypermutation-induced in vivo oxidative stress resistance enhances Vibrio cholerae host adaptation. PLOS Pathog. 2018;14(48):e1007413. doi:10.1371/journal.ppat.1007413.
   PubMedGoogle Scholar
• Stacy A, Andrade-Oliveira V, McCulloch JA, Hild B, Oh JH, Perez-Chaparro PJ, Sim CK, Lim AI, Link VM, Enamorado M, et al. Infection trains the host for microbiota-enhanced resistance to pathogens. Cell. 2021;184(3):615–627.e17. doi:10.1016/j.cell.2020.12.011.
   PubMed Web of Science ®Google Scholar
• Boyd ES, Thomas KM, Dai YY, Boyd JM, Outten FW. Interplay between oxygen and Fe-S cluster biogenesis: insights from the Suf Pathway. Biochemistry. 2014;53(37):5834–5847. doi:10.1021/bi500488r.
   PubMed Web of Science ®Google Scholar
• Przybyla-Toscano J, Roland M, Gaymard F, Couturier J, Rouhier N. Roles and maturation of iron-sulfur proteins in plastids. J Biol Inorg Chem. 2018;23(4):545–566. doi:10.1007/s00775-018-1532-1.
   PubMed Web of Science ®Google Scholar
• Rouault TA. The indispensable role of mammalian iron sulfur proteins in function and regulation of multiple diverse metabolic pathways. Biometals. 2019;32(3):343–353. doi:10.1007/s10534-019-00191-7.
   PubMed Web of Science ®Google Scholar
• Ayala-Castro C, Saini A, Outten FW. Fe-S cluster assembly pathways in bacteria. Microbiol Mol Biol R. 2008;72(1):110–125. doi:10.1128/mmbr.00034-07.
   PubMed Web of Science ®Google Scholar
• Riboldi GP, Verli H, Frazzon J. Structural studies of the Enterococcus faecalis SufU [Fe-S] cluster protein. BMC Biochem. 2009;10(1):10. doi:10.1186/1471-2091-10-3.
   PubMedGoogle Scholar
• Riboldi GP, Larson TJ, Frazzon J. Enterococcus faecalis sufCDSUB complements Escherichia coli sufABCDSE. FEMS Microbiol Lett. 2011;320(1):15–24. doi:10.1111/j.1574-6968.2011.02284.x.
   PubMed Web of Science ®Google Scholar
• Riboldi GP, de Oliveira JS, Frazzon J. Enterococcus faecalis SufU scaffold protein enhances SufS desulfurase activity by acquiring sulfur from its cysteine-153. Bba-Proteins Proteom. 2011;1814(12):1910–1918. doi:10.1016/j.bbapap.2011.06.016.
   PubMed Web of Science ®Google Scholar
• Zhang XL, de Maat V, Prieto AMG, Prajsnar TK, Bayjanov JR, de Been M, Rogers MRC, Bonten MJM, Mesnage S, Willems RJL, et al. RNA-seq and Tn-seq reveal fitness determinants of vancomycin-resistant Enterococcus faecium during growth in human serum. BMC Genomics. 2017;18(1):18. doi:10.1186/s12864-017-4299-9.
   PubMedGoogle Scholar
• Zhang XL, Paganelli FL, Bierschenk D, Kuipers A, Bonten MJM, Willems RJL, van Schaik W, Hughes D. Genome-wide identification of ampicillin resistance determinants in Enterococcus faecium. PLOS Genet. 2012;8(6):e1002804. doi:10.1371/journal.pgen.1002804.
   PubMed Web of Science ®Google Scholar
• Liu XY, Liu GY, Wu YS, Pang X, Wu YQ, Niu J, Chen Q, Zhang X. Transposon sequencing: A powerful tool for the functional genomic study of food-borne pathogens. Trends Food Sci Tech. 2021;118:679–687. doi:10.1016/j.tifs.2021.06.032.
   Web of Science ®Google Scholar
• Zhang XL, Rogers M, Bierschenk D, Bonten MJM, Willems RJL, van Schaik W, Manganelli R. A lacI-family regulator activates maltodextrin metabolism of Enterococcus faecium. PLOS ONE. 2013;8(8):e72285. doi:10.1371/journal.pone.0072285.
   PubMed Web of Science ®Google Scholar
• Wu YS, Pang XX, Liu XY, Wu YJ, Zhang XL, Cocolin L. Functional genomics identified novel genes involved in growth at low temperatures in Listeria monocytogenes. Microbiol Spectr. 2022;10(4). doi:10.1128/spectrum.00710-22.
   Web of Science ®Google Scholar
• Pang XX, Wu YS, Liu XY, Wu YJ, Shu Q, Niu JR, Chen QH, Zhang XL, Power P. The lipoteichoic acid-related proteins YqgS and LafA contribute to the resistance of listeria monocytogenes to nisin. Microbiol Spectr. 2022;10(1). doi:10.1128/spectrum.02095-21.
   Web of Science ®Google Scholar
• Chen SF, Zhou YQ, Chen YR, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018;34(17):884–890. doi:10.1093/bioinformatics/bty560.
   PubMed Web of Science ®Google Scholar
• Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4):357–U54. doi:10.1038/NMETH.1923.
   PubMed Web of Science ®Google Scholar
• Kayala MA, Baldi P. Cyber-T web server: differential analysis of high-throughput data. Nucleic Acids Res. 2012;40(W1). doi:10.1093/nar/gks420.
   PubMed Web of Science ®Google Scholar
• Bryant P, Pozzati G, Elofsson A. Improved prediction of protein-protein interactions using AlphaFold2. Nat Commun. 2022;13(1). doi:10.1038/s41467-022-28865-w.
   Web of Science ®Google Scholar
• Zhang Y, Skolnick J. TM-align: a protein structure alignment algorithm based on the TM-score. Nucleic Acids Res. 2005;33(7):2302–2309. doi:10.1093/nar/gki524. Print 2005.
   PubMed Web of Science ®Google Scholar
• Hung CL, Lin YS, Lin CY, Chung YC, Chung YF. CUDA ClustalW: An efficient parallel algorithm for progressive multiple sequence alignment on Multi-GPUs. Comput Biol Chem. 2015;58:62–68. doi:10.1016/j.compbiolchem.2015.05.004.
   PubMed Web of Science ®Google Scholar
• Singh R, Gurao A, Rajesh C, Mishra S, Rani S, Behl A, Kumar V, Kataria RS. Comparative modeling and mutual docking of structurally uncharacterized heat shock protein 70 and heat shock factor-1 proteins in water buffalo. Vet World. 2019;12(12):2036–2045. doi:10.14202/vetworld.2019.2036-2045.
   PubMed Web of Science ®Google Scholar
• Rice L. Antibiotics and gastrointestinal colonization by vancomycin-resistant enterococci. Eur J Clin Microbiol Infect Dis. 2005;24(12):804–814. doi:10.1007/s10096-005-0057-z.
   PubMed Web of Science ®Google Scholar
• Zhang XL, Vrijenhoek JEP, Bonten MJM, Willems RJL, van Schaik W. A genetic element present on megaplasmids allows Enterococcus faecium to use raffinose as carbon source. Environ Microbiol. 2011;13(2):518–528. doi:10.1111/j.1462-2920.2010.02355.x.
   PubMed Web of Science ®Google Scholar
• Zhang XL, Top J, de Been M, Bierschenk D, Rogers M, Leendertse M, Bonten MJM, van der Poll T, Willems RJL, van Schaik W. Identification of a genetic determinant in clinical Enterococcus faecium strains that contributes to intestinal colonization during antibiotic treatment. J Infect Dis. 2013;207(11):1780–1786. doi:10.1093/infdis/jit076.
   PubMed Web of Science ®Google Scholar
• Liu XY, Pang XX, Wu YS, Wu YJ, Xu LA, Chen QH, Niu J, Zhang X. New insights into the lactic acid resistance determinants of listeria monocytogenes based on transposon sequencing and transcriptome sequencing analyses. Microbiol Spectr. 2023;11(1). doi:10.1128/spectrum.02750-22.
   Web of Science ®Google Scholar
• Krueger WA, Krueger-Rameck S, Koch S, Carey V, Pier GB, Huebner J. Assessment of the role of antibiotics and enterococcal virulence factors in a mouse model of extraintestinal translocation. Crit Care Med. 2004;32(2):467–471. doi:10.1097/01.CCM.0000109447.04893.48.
   PubMed Web of Science ®Google Scholar
• Kuss SK, Best GT, Etheredge CA, Pruijssers AJ, Frierson JM, Hooper LV, Dermody TS, Pfeiffer JK. Intestinal microbiota promotes enteric Virus replication and systemic pathogenesis. Science. 2011;334(6053):249–252. doi:10.1126/science.1211057.
   PubMed Web of Science ®Google Scholar
• Blahut M, Sanchez E, Fisher CE, Outten FW. Fe-S cluster biogenesis by the bacterial Suf pathway. Bba-Mol Cell Res. 2020;1867(11):118829. doi:10.1016/j.bbamcr.2020.118829.
   PubMed Web of Science ®Google Scholar
• Vey JL, Yang J, Li M, Broderick WE, Broderick JB, Drennan CL. Structural basis for glycyl radical formation by pyruvate formate-lyase activating enzyme. P Natl A Sci India B. 2008;105(42):16137–16141. doi:10.1073/pnas.0806640105.
   Google Scholar
• Py B, Barras F. Building Fe-S proteins: bacterial strategies. Nat Rev Microbiol. 2010;8(6):436–446. doi:10.1038/nrmicro2356.
   PubMed Web of Science ®Google Scholar
• Pérard J, de Choudens SO. Iron-sulfur clusters biogenesis by the SUF machinery: close to the molecular mechanism understanding. J Biol Inorg Chem. 2018;23(4):581–596. doi:10.1007/s00775-017-1527-3.
   PubMed Web of Science ®Google Scholar
• Andrew AJ, Song J-Y, Schilke B, Craig EA, Fox TD. Posttranslational regulation of the scaffold for Fe-S cluster biogenesis, Isu. Mol Biol Cell. 2008;19(12):5259–5266. doi:10.1091/mbc.e08-06-0622.
   PubMed Web of Science ®Google Scholar
• Blanc B, Gerez C, de Choudens SO. Assembly of Fe/S proteins in bacterial systems: biochemistry of the bacterial ISC system. Bba-Mol Cell Res. 2015;1853(6):1436–1447. doi:10.1016/j.bbamcr.2014.12.009.
   PubMed Web of Science ®Google Scholar
• Garcia PS, D’Angelo F, de Choudens SO, Dussouchaud M, Bouveret E, Gribaldo S, Barras F. An early origin of iron-sulfur cluster biosynthesis machineries before Earth oxygenation. Nat Ecol Evol. 2022;6(10):1564–1572. doi:10.1038/s41559-022-01857-1.
   PubMed Web of Science ®Google Scholar
• Yokoyama N, Nonaka C, Ohashi Y, Shioda M, Terahata T, Chen W, Sakamoto K, Maruyama C, Saito T, Yuda E, et al. Distinct roles for U-type proteins in iron–sulfur cluster biosynthesis revealed by genetic analysis of the Bacillus subtilis sufCDSUB operon. Mol Microbiol. 2018;107(6):688–703. doi:10.1111/mmi.13907.
   PubMed Web of Science ®Google Scholar
• Albrecht AG, Netz DJA, Miethke M, Pierik AJ, Burghaus O, Peuckert F, Lill R, Marahiel MA. SufU is an essential iron-sulfur cluster scaffold protein in Bacillus subtilis. J Bacteriol. 2010;192(6):1643–1651. doi:10.1128/jb.01536-09.
   PubMed Web of Science ®Google Scholar
• Roberts CA, Al-Tameemi HM, Mashruwala AA, Rosario-Cruz Z, Chauhan U, Sause WE, Torres VJ, Belden WJ, Boyd JM. The Suf Iron-Sulfur cluster biosynthetic system is essential in staphylococcus aureus, and decreased suf function results in global metabolic defects and reduced survival in human neutrophils. Infect Immun. 2017;85(6). doi:10.1128/iai.00100-17.
   Web of Science ®Google Scholar
• Richardson DJ. Bacterial respiration: a flexible process for a changing environment 1999 Fleming Lecture (Delivered at the 144th meeting of the Society for General Microbiology, 8 September 1999). Microbiology. 2000;146(3):551–571. doi:10.1099/00221287-146-3-551.
   PubMedGoogle Scholar
• Tang YW. Molecular medical microbiology: chapter 11 - bacterial energy metabolism. Diagn Microbiol Infect Dis. 2002;43(2):173–174. doi:10.1016/S0732-8893(02)00377-2.
   Google Scholar
• Shisler KA, Hutcheson RU, Horitani M, Duschene KS, Crain AV, Byer AS, Shepard EM, Rasmussen A, Yang J, Broderick WE, et al. Monovalent cation activation of the radical SAM enzyme pyruvate formate-lyase activating enzyme. J Am Chem Soc. 2017;139(34):11803–11813. doi:10.1021/jacs.7b04883.
   PubMed Web of Science ®Google Scholar
• Boyington JC, Gladyshev VN, Khangulov SV, Stadtman TC, Sun PD. Crystal structure of formate dehydrogenase H: catalysis involving Mo, molybdopterin, selenocysteine, and an Fe4S4 cluster. Science. 1997;275(5304):1305–1308. doi:10.1126/science.275.5304.1305.
   PubMed Web of Science ®Google Scholar