The Intraperitoneal Transcriptome of the Opportunistic Pathogen Enterococcus faecalis in Mice

Muller C, Cacaci M, Sauvageot N, Sanguinetti M, Rattei T, Eder T, Giard J-C, Kalinowski J, Hain T, Hartke A (2015)
PLoS ONE 10(5): e0126143.

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Zeitschriftenaufsatz | Veröffentlicht | Englisch
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Abstract / Bemerkung
Enterococcus faecalis is a Gram-positive lactic acid intestinal opportunistic bacterium with virulence potential. For a better understanding of the adapation of this bacterium to the host conditions, we performed a transcriptome analysis of bacteria isolated from an infection site (mouse peritonitis) by RNA-sequencing. We identified a total of 211 genes with significantly higher transcript levels and 157 repressed genes. Our in vivo gene expression database reflects well the infection process since genes encoding important virulence factors like cytolysin, gelatinase or aggregation substance as well as stress response proteins, are significantly induced. Genes encoding metabolic activities are the second most abundant in vivo induced genes demonstrating that the bacteria are metabolically active and adapt to the special nutrient conditions of the host. alpha- and beta-glucosides seem to be important substrates for E. faecalis inside the host. Compared to laboratory conditions, the flux through the upper part of glycolysis seems to be reduced and more carbon may enter the pentose phosphate pathway. This may reflect the need of the bacteria under infection conditions to produce more reducing power for biosynthesis. Another important substrate is certainly glycerol since both pathways of glycerol catabolism are strongly induced. Strongly in vivo induced genes should be important for the infection process. This assumption has been verified in a virulence test using well characterized mutants affected in glycerol metabolism. This showed indeed that mutants unable to metabolize this sugar alcohol are affected in organ colonisation in a mouse model.
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PLoS ONE
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10
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5
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e0126143
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Muller C, Cacaci M, Sauvageot N, et al. The Intraperitoneal Transcriptome of the Opportunistic Pathogen Enterococcus faecalis in Mice. PLoS ONE. 2015;10(5): e0126143.
Muller, C., Cacaci, M., Sauvageot, N., Sanguinetti, M., Rattei, T., Eder, T., Giard, J. - C., et al. (2015). The Intraperitoneal Transcriptome of the Opportunistic Pathogen Enterococcus faecalis in Mice. PLoS ONE, 10(5), e0126143. doi:10.1371/journal.pone.0126143
Muller, C., Cacaci, M., Sauvageot, N., Sanguinetti, M., Rattei, T., Eder, T., Giard, J. - C., Kalinowski, J., Hain, T., and Hartke, A. (2015). The Intraperitoneal Transcriptome of the Opportunistic Pathogen Enterococcus faecalis in Mice. PLoS ONE 10:e0126143.
Muller, C., et al., 2015. The Intraperitoneal Transcriptome of the Opportunistic Pathogen Enterococcus faecalis in Mice. PLoS ONE, 10(5): e0126143.
C. Muller, et al., “The Intraperitoneal Transcriptome of the Opportunistic Pathogen Enterococcus faecalis in Mice”, PLoS ONE, vol. 10, 2015, : e0126143.
Muller, C., Cacaci, M., Sauvageot, N., Sanguinetti, M., Rattei, T., Eder, T., Giard, J.-C., Kalinowski, J., Hain, T., Hartke, A.: The Intraperitoneal Transcriptome of the Opportunistic Pathogen Enterococcus faecalis in Mice. PLoS ONE. 10, : e0126143 (2015).
Muller, Cecile, Cacaci, Margherita, Sauvageot, Nicolas, Sanguinetti, Maurizio, Rattei, Thomas, Eder, Thomas, Giard, Jean-Christophe, Kalinowski, Jörn, Hain, Torsten, and Hartke, Axel. “The Intraperitoneal Transcriptome of the Opportunistic Pathogen Enterococcus faecalis in Mice”. PLoS ONE 10.5 (2015): e0126143.

11 Zitationen in Europe PMC

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Fighting Pathogenic Bacteria on Two Fronts: Phages and Antibiotics as Combined Strategy.
Tagliaferri TL, Jansen M, Horz HP., Front Cell Infect Microbiol 9(), 2019
PMID: 30834237
Manganese acquisition is essential for virulence of Enterococcus faecalis.
Colomer-Winter C, Flores-Mireles AL, Baker SP, Frank KL, Lynch AJL, Hultgren SJ, Kitten T, Lemos JA., PLoS Pathog 14(9), 2018
PMID: 30235334
In vivo expression technology and 5' end mapping of the Borrelia burgdorferi transcriptome identify novel RNAs expressed during mammalian infection.
Adams PP, Flores Avile C, Popitsch N, Bilusic I, Schroeder R, Lybecker M, Jewett MW., Nucleic Acids Res 45(2), 2017
PMID: 27913725
Enterococcus faecalis Uses a Phosphotransferase System Permease and a Host Colonization-Related ABC Transporter for Maltodextrin Uptake.
Sauvageot N, Mokhtari A, Joyet P, Budin-Verneuil A, Blancato VS, Repizo GD, Henry C, Pikis A, Thompson J, Magni C, Hartke A, Deutscher J., J Bacteriol 199(9), 2017
PMID: 28242718
Subinhibitory Concentrations of Ciprofloxacin Enhance Antimicrobial Resistance and Pathogenicity of Enterococcus faecium.
Sinel C, Cacaci M, Meignen P, Guérin F, Davies BW, Sanguinetti M, Giard JC, Cattoir V., Antimicrob Agents Chemother 61(5), 2017
PMID: 28193670
Model systems for the study of Enterococcal colonization and infection.
Goh HMS, Yong MHA, Chong KKL, Kline KA., Virulence 8(8), 2017
PMID: 28102784
Global Regulation of Gene Expression by the MafR Protein of Enterococcus faecalis.
Ruiz-Cruz S, Espinosa M, Goldmann O, Bravo A., Front Microbiol 6(), 2015
PMID: 26793169
Characterization of Two Metal Binding Lipoproteins as Vaccine Candidates for Enterococcal Infections.
Romero-Saavedra F, Laverde D, Budin-Verneuil A, Muller C, Bernay B, Benachour A, Hartke A, Huebner J., PLoS One 10(8), 2015
PMID: 26322633

71 References

Daten bereitgestellt von Europe PubMed Central.

The European Centre for Disease Prevention and Control (ECDC) pilot point prevalence survey of healthcare-associated infections and antimicrobial use
AUTHOR UNKNOWN, 2012
Antimicrobial-resistant pathogens associated with healthcare-associated infections: summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2009-2010.
Sievert DM, Ricks P, Edwards JR, Schneider A, Patel J, Srinivasan A, Kallen A, Limbago B, Fridkin S; National Healthcare Safety Network (NHSN) Team and Participating NHSN Facilities., Infect Control Hosp Epidemiol 34(1), 2012
PMID: 23221186
Emergence and spread of vancomycin resistance among enterococci in Europe
AUTHOR UNKNOWN, 2008
Physiological and molecular aspects of bile salt response in Enterococcus faecalis.
Rince A, Le Breton Y, Verneuil N, Giard JC, Hartke A, Auffray Y., Int. J. Food Microbiol. 88(2-3), 2003
PMID: 14596992
The Enterococci and Related Streptococci.
Sherman JM., J. Bacteriol. 35(2), 1938
PMID: 16560094
How long do nosocomial pathogens persist on inanimate surfaces? A systematic review.
Kramer A, Schwebke I, Kampf G., BMC Infect. Dis. 6(), 2006
PMID: 16914034
Starvation-induced multiresistance in Enterococcus faecalis JH2-2.
Giard JC, Hartke A, Flahaut S, Benachour A, Boutibonnes P, Auffray Y., Curr. Microbiol. 32(5), 1996
PMID: 8857273

AUTHOR UNKNOWN, 2014
Advances in bacterial transcriptome and transposon insertion-site profiling using second-generation sequencing.
Febrer M, McLay K, Caccamo M, Twomey KB, Ryan RP., Trends Biotechnol. 29(11), 2011
PMID: 21764162
RNA-Seq: a revolutionary tool for transcriptomics.
Wang Z, Gerstein M, Snyder M., Nat. Rev. Genet. 10(1), 2009
PMID: 19015660
Probing bacterial metabolism during infection using high-resolution transcriptomics.
Jorth P, Trivedi U, Rumbaugh K, Whiteley M., J. Bacteriol. 195(22), 2013
PMID: 23974023
Mapping the Burkholderia cenocepacia niche response via high-throughput sequencing.
Yoder-Himes DR, Chain PS, Zhu Y, Wurtzel O, Rubin EM, Tiedje JM, Sorek R., Proc. Natl. Acad. Sci. U.S.A. 106(10), 2009
PMID: 19234113
The primary transcriptome of the major human pathogen Helicobacter pylori.
Sharma CM, Hoffmann S, Darfeuille F, Reignier J, Findeiss S, Sittka A, Chabas S, Reiche K, Hackermuller J, Reinhardt R, Stadler PF, Vogel J., Nature 464(7286), 2010
PMID: 20164839
Deep sequencing-based discovery of the Chlamydia trachomatis transcriptome.
Albrecht M, Sharma CM, Reinhardt R, Vogel J, Rudel T., Nucleic Acids Res. 38(3), 2009
PMID: 19923228
RNA-Seq-based monitoring of infection-linked changes in Vibrio cholerae gene expression.
Mandlik A, Livny J, Robins WP, Ritchie JM, Mekalanos JJ, Waldor MK., Cell Host Microbe 10(2), 2011
PMID: 21843873
3D Structure Modeling of Alpha-Amino Acid Ester Hydrolase from Xanthomonas rubrilineans.
Zarubina SA, Uporov IV, Fedorchuk EA, Fedorchuk VV, Sklyarenko AV, Yarotsky SV, Tishkov VI., Acta Naturae 5(4), 2013
PMID: 24455184

AUTHOR UNKNOWN, 0
Cutadapt removes adapter sequences from high-throughput sequencing reads
AUTHOR UNKNOWN, 2011
EMBOSS: the European Molecular Biology Open Software Suite.
Rice P, Longden I, Bleasby A., Trends Genet. 16(6), 2000
PMID: 10827456
Fast and accurate long-read alignment with Burrows-Wheeler transform.
Li H, Durbin R., Bioinformatics 26(5), 2010
PMID: 20080505
The Sequence Alignment/Map format and SAMtools.
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R; 1000 Genome Project Data Processing Subgroup., Bioinformatics 25(16), 2009
PMID: 19505943
Model-based analysis of ChIP-Seq (MACS).
Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, Liu XS., Genome Biol. 9(9), 2008
PMID: 18798982
Differential expression in RNA-seq: a matter of depth.
Tarazona S, Garcia-Alcalde F, Dopazo J, Ferrer A, Conesa A., Genome Res. 21(12), 2011
PMID: 21903743
Integrative genomics viewer.
Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP., Nat. Biotechnol. 29(1), 2011
PMID: 21221095
Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration.
Thorvaldsdottir H, Robinson JT, Mesirov JP., Brief. Bioinformatics 14(2), 2012
PMID: 22517427
Structure, function, and biology of the Enterococcus faecalis cytolysin.
Van Tyne D, Martin MJ, Gilmore MS., Toxins (Basel) 5(5), 2013
PMID: 23628786
Manganese-dependent regulation of the endocarditis-associated virulence factor EfaA of Enterococcus faecalis.
Low YL, Jakubovics NS, Flatman JC, Jenkinson HF, Smith AW., J. Med. Microbiol. 52(Pt 2), 2003
PMID: 12543916
Generation and testing of mutants of Enterococcus faecalis in a mouse peritonitis model.
Singh KV, Qin X, Weinstock GM, Murray BE., J. Infect. Dis. 178(5), 1998
PMID: 9780263
Effects of Enterococcus faecalis fsr genes on production of gelatinase and a serine protease and virulence.
Qin X, Singh KV, Weinstock GM, Murray BE., Infect. Immun. 68(5), 2000
PMID: 10768947
Cell density—dependent regulation: basic principles and effects on the virulence of Gram-positive cocci
AUTHOR UNKNOWN, 2004
The Fsr quorum-sensing system of Enterococcus faecalis modulates surface display of the collagen-binding MSCRAMM Ace through regulation of gelE.
Pinkston KL, Gao P, Diaz-Garcia D, Sillanpaa J, Nallapareddy SR, Murray BE, Harvey BR., J. Bacteriol. 193(17), 2011
PMID: 21705589
LPxTG surface proteins of enterococci.
Hendrickx AP, Willems RJ, Bonten MJ, van Schaik W., Trends Microbiol. 17(9), 2009
PMID: 19726195
Plasmid-associated hemolysin and aggregation substance production contribute to virulence in experimental enterococcal endocarditis.
Chow JW, Thal LA, Perri MB, Vazquez JA, Donabedian SM, Clewell DB, Zervos MJ., Antimicrob. Agents Chemother. 37(11), 1993
PMID: 8285637
Neutrophils are essential for rapid clearance of Enterococcus faecium in mice.
Leendertse M, Willems RJ, Giebelen IA, Roelofs JJ, Bonten MJ, van der Poll T., Infect. Immun. 77(1), 2008
PMID: 19001080
The Enterococcus faecalis gene encoding the novel general stress protein Gsp62
AUTHOR UNKNOWN, 2002
Iron and proteins for iron storage and detoxification
AUTHOR UNKNOWN, 2004
Trigger Factor and DnaK possess overlapping substrate pools and binding specificities.
Deuerling E, Patzelt H, Vorderwulbecke S, Rauch T, Kramer G, Schaffitzel E, Mogk A, Schulze-Specking A, Langen H, Bukau B., Mol. Microbiol. 47(5), 2003
PMID: 12603737
clpB, a class III heat-shock gene regulated by CtsR, is involved in thermotolerance and virulence of Enterococcus faecalis.
de Oliveira NE, Abranches J, Gaca AO, Laport MS, Damaso CR, Bastos Mdo C, Lemos JA, Giambiagi-deMarval M., Microbiology (Reading, Engl.) 157(Pt 3), 2010
PMID: 21148206
Implication of hypR in the virulence and oxidative stress response of Enterococcus faecalis.
Verneuil N, Rince A, Sanguinetti M, Auffray Y, Hartke A, Giard JC., FEMS Microbiol. Lett. 252(1), 2005
PMID: 16216443
Implication of (Mn)superoxide dismutase of Enterococcus faecalis in oxidative stress responses and survival inside macrophages.
Verneuil N, Maze A, Sanguinetti M, Laplace JM, Benachour A, Auffray Y, Giard JC, Hartke A., Microbiology (Reading, Engl.) 152(Pt 9), 2006
PMID: 16946253
Enterococcus faecalis heme-dependent catalase.
Frankenberg L, Brugna M, Hederstedt L., J. Bacteriol. 184(22), 2002
PMID: 12399505
Contribution of a PerR-like regulator to the oxidative-stress response and virulence of Enterococcus faecalis.
Verneuil N, Rince A, Sanguinetti M, Posteraro B, Fadda G, Auffray Y, Hartke A, Giard JC., Microbiology (Reading, Engl.) 151(Pt 12), 2005
PMID: 16339944
Proteomic analysis of spontaneous mutants of Lactococcus lactis: Involvement of GAPDH and arginine deiminase pathway in H2O2 resistance.
Rochat T, Boudebbouze S, Gratadoux JJ, Blugeon S, Gaudu P, Langella P, Maguin E., Proteomics 12(11), 2012
PMID: 22623348
Iron/sulfur proteins biogenesis in prokaryotes: formation, regulation and diversity.
Roche B, Aussel L, Ezraty B, Mandin P, Py B, Barras F., Biochim. Biophys. Acta 1827(3), 2013
PMID: 23298813
Enterococcus faecalis SufU scaffold protein enhances SufS desulfurase activity by acquiring sulfur from its cysteine-153.
Riboldi GP, de Oliveira JS, Frazzon J., Biochim. Biophys. Acta 1814(12), 2011
PMID: 21835272
Enterococcus faecalis prophage dynamics and contributions to pathogenic traits.
Matos RC, Lapaque N, Rigottier-Gois L, Debarbieux L, Meylheuc T, Gonzalez-Zorn B, Repoila F, Lopes Mde F, Serror P., PLoS Genet. 9(6), 2013
PMID: 23754962
Maltose and maltodextrin utilization by Bacillus subtilis.
Schonert S, Seitz S, Krafft H, Feuerbaum EA, Andernach I, Witz G, Dahl MK., J. Bacteriol. 188(11), 2006
PMID: 16707683
Maltose and maltodextrin utilization by Listeria monocytogenes depend on an inducible ABC transporter which is repressed by glucose.
Gopal S, Berg D, Hagen N, Schriefer EM, Stoll R, Goebel W, Kreft J., PLoS ONE 5(4), 2010
PMID: 20436965
A LacI-family regulator activates maltodextrin metabolism of Enterococcus faecium.
Zhang X, Rogers M, Bierschenk D, Bonten MJ, Willems RJ, van Schaik W., PLoS ONE 8(8), 2013
PMID: 23951303
Characterization of the chitinolytic machinery of Enterococcus faecalis V583 and high-resolution structure of its oxidative CBM33 enzyme.
Vaaje-Kolstad G, Bohle LA, Gaseidnes S, Dalhus B, Bjoras M, Mathiesen G, Eijsink VG., J. Mol. Biol. 416(2), 2011
PMID: 22210154
The Listeria monocytogenes ChiA chitinase enhances virulence through suppression of host innate immunity.
Chaudhuri S, Gantner BN, Ye RD, Cianciotto NP, Freitag NE., MBio 4(2), 2013
PMID: 23512964
Glycerol is metabolized in a complex and strain-dependent manner in Enterococcus faecalis.
Bizzini A, Zhao C, Budin-Verneuil A, Sauvageot N, Giard JC, Auffray Y, Hartke A., J. Bacteriol. 192(3), 2009
PMID: 19966010
Transcriptome analysis of Enterococcus faecalis toward its adaption to surviving in the mouse intestinal tract.
Lindenstrauss AG, Ehrmann MA, Behr J, Landstorfer R, Haller D, Sartor RB, Vogel RF., Arch. Microbiol. 196(6), 2014
PMID: 24700373
Carbon metabolism of intracellular bacterial pathogens and possible links to virulence.
Eisenreich W, Dandekar T, Heesemann J, Goebel W., Nat. Rev. Microbiol. 8(6), 2010
PMID: 20453875
Identification of Listeria monocytogenes genes contributing to intracellular replication by expression profiling and mutant screening.
Joseph B, Przybilla K, Stuhler C, Schauer K, Slaghuis J, Fuchs TM, Goebel W., J. Bacteriol. 188(2), 2006
PMID: 16385046
Redox balance via lactate dehydrogenase is important for multiple stress resistance and virulence in Enterococcus faecalis.
Rana NF, Sauvageot N, Laplace JM, Bao Y, Nes I, Rince A, Posteraro B, Sanguinetti M, Hartke A., Infect. Immun. 81(8), 2013
PMID: 23649090
Transcriptome analysis of Enterococcus faecalis during mammalian infection shows cells undergo adaptation and exist in a stringent response state.
Frank KL, Colomer-Winter C, Grindle SM, Lemos JA, Schlievert PM, Dunny GM., PLoS ONE 9(12), 2014
PMID: 25545155
Screening of in vivo activated genes in Enterococcus faecalis during insect and mouse infections and growth in urine.
Hanin A, Sava I, Bao Y, Huebner J, Hartke A, Auffray Y, Sauvageot N., PLoS ONE 5(7), 2010
PMID: 20686694

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