Comparative analysis of proteomic adaptations in Enterococcus faecalis and Enterococcus faecium after long term bile acid exposure.

Publisher: BioMed Central Country of Publication: England NLM ID: 100966981 Publication Model: Electronic Cited Medium: Internet ISSN: 1471-2180 (Electronic) Linking ISSN: 14712180 NLM ISO Abbreviation: BMC Microbiol Subsets: MEDLINE

Original Publication: London : BioMed Central, [2001-

Bile Acids and Salts*/pharmacology ; Enterococcus faecium*/genetics ; Enterococcus faecium*/metabolism; Enterococcus faecalis/genetics ; Enterococcus faecalis/metabolism ; Deoxycholic Acid/pharmacology ; Proteomics ; Cholic Acid ; Chenodeoxycholic Acid/metabolism ; Enterococcus

Background: All gastrointestinal pathogens, including Enterococcus faecalis and Enterococcus faecium, undergo adaptation processes during colonization and infection. In this study, we investigated by data-independent acquisition mass spectrometry (DIA-MS) two crucial adaptations of these two Enterococcus species at the proteome level. Firstly, we examined the adjustments to cope with bile acid concentrations at 0.05% that the pathogens encounter during a potential gallbladder infection. Therefore, we chose the primary bile acids cholic acid (CA) and chenodeoxycholic acid (CDCA) as well as the secondary bile acid deoxycholic acid (DCA), as these are the most prominent bile acids. Secondly, we investigated the adaptations from an aerobic to a microaerophilic environment, as encountered after oral-fecal infection, in the absence and presence of deoxycholic acid (DCA).
Results: Our findings showed similarities, but also species-specific variations in the response to the different bile acids. Both Enterococcus species showed an IC 50 in the range of 0.01- 0.023% for DCA and CDCA in growth experiments and both species were resistant towards 0.05% CA. DCA and CDCA had a strong effect on down-expression of proteins involved in translation, transcription and replication in E. faecalis (424 down-expressed proteins with DCA, 376 down-expressed proteins with CDCA) and in E. faecium (362 down-expressed proteins with DCA, 391 down-expressed proteins with CDCA). Proteins commonly significantly altered in their expression in all bile acid treated samples were identified for both species and represent a "general bile acid response". Among these, various subunits of a V-type ATPase, different ABC-transporters, multi-drug transporters and proteins related to cell wall biogenesis were up-expressed in both species and thus seem to play an essential role in bile acid resistance. Most of the differentially expressed proteins were also identified when E. faecalis was incubated with low levels of DCA at microaerophilic conditions instead of aerobic conditions, indicating that adaptations to bile acids and to a microaerophilic atmosphere can occur simultaneously.
Conclusions: Overall, these findings provide a detailed insight into the proteomic stress response of two Enterococcus species and help to understand the resistance potential and the stress-coping mechanisms of these important gastrointestinal bacteria.
(© 2024. The Author(s).)

Mol Biol Evol. 2021 Dec 9;38(12):5825-5829. (PMID: 34597405)
J Clin Med. 2021 May 18;10(10):. (PMID: 34070003)
J Appl Microbiol. 2006 Apr;100(4):728-38. (PMID: 16553727)
Afr J Infect Dis. 2011;5(2):40-6. (PMID: 23878706)
Clin Gastroenterol Hepatol. 2023 May;21(5):1223-1232.e3. (PMID: 36116754)
J Biol Chem. 2008 Feb 8;283(6):3329-3337. (PMID: 18055462)
J Glob Antimicrob Resist. 2015 Jun;3(2):128-131. (PMID: 27873661)
HPB (Oxford). 2023 May;25(5):568-576. (PMID: 36804057)
Nucleic Acids Res. 2023 Jan 6;51(D1):D1539-D1548. (PMID: 36370099)
J Bacteriol. 2004 Dec;186(23):7829-35. (PMID: 15547253)
Endoscopy. 2022 Nov;54(11):1045-1052. (PMID: 35255518)
Appl Environ Microbiol. 2007 Nov;73(21):6757-67. (PMID: 17827318)
Genomics. 2021 May;113(3):1534-1542. (PMID: 33771633)
Microbiol Res. 2017 Mar;196:95-105. (PMID: 28164795)
Biochim Biophys Acta. 2000 Nov 23;1508(1-2):86-111. (PMID: 11090820)
J Bacteriol. 2005 Aug;187(16):5799-808. (PMID: 16077128)
BMC Bioinformatics. 2015 May 22;16:169. (PMID: 25994840)
Biochim Biophys Acta. 2000 May 31;1458(2-3):356-63. (PMID: 10838050)
J Mol Microbiol Biotechnol. 2007;13(1-3):140-6. (PMID: 17693721)
FEMS Microbiol Rev. 2005 Sep;29(4):625-51. (PMID: 16102595)
Proteome Sci. 2010 Jun 25;8:37. (PMID: 20579342)
Microbiol Spectr. 2019 Jul;7(4):. (PMID: 31298205)
J Appl Microbiol. 2003;94(6):947-52. (PMID: 12752801)
Proteomics. 2015 Apr;15(7):1215-23. (PMID: 25560523)
Antimicrob Agents Chemother. 2002 Jul;46(7):2124-31. (PMID: 12069964)
Eur J Drug Metab Pharmacokinet. 2006 Jul-Sep;31(3):135-43. (PMID: 17136858)
J Appl Microbiol. 2003;95(1):86-91. (PMID: 12807457)
Curr Opin Struct Biol. 2014 Apr;25:40-8. (PMID: 24878343)
Exp Ther Med. 2016 Sep;12(3):1732-1740. (PMID: 27602088)
J Exp Biol. 1965 Dec;43(3):473-8. (PMID: 5893422)
Mol Cell Proteomics. 2016 Jan;15(1):305-17. (PMID: 26545397)
Nature. 1967 Jun 10;214(5093):1152-4. (PMID: 4964057)
Infect Drug Resist. 2022 Dec 02;15:7095-7106. (PMID: 36483142)
Appl Environ Microbiol. 2009 May;75(10):3153-60. (PMID: 19304838)
Microbiome. 2021 Jun 14;9(1):140. (PMID: 34127070)
Drugs. 1999 Jan;57(1):81-91. (PMID: 9951953)
J Exp Med. 1899 Sep 1;4(5-6):521-34. (PMID: 19866921)
Ann Acad Med Singap. 2008 Oct;37(10):861-9. (PMID: 19037521)
Am Surg. 2012 Feb;78(2):220-4. (PMID: 22369833)
Proc Natl Acad Sci U S A. 1988 Nov;85(21):7972-6. (PMID: 2973058)
Gastroenterology. 2014 Nov;147(5):1055-63.e8. (PMID: 25046162)
Int J Food Microbiol. 2006 Dec 1;112(3):208-14. (PMID: 17046092)
F1000Res. 2017 Nov 20;6:2029. (PMID: 29188025)
EMBO Rep. 2004 Dec;5(12):1148-52. (PMID: 15540116)
Environ Microbiol. 2006 Oct;8(10):1825-33. (PMID: 16958763)
Infect Immun. 2020 Sep 18;88(10):. (PMID: 32661122)
J Bacteriol. 1997 Apr;179(8):2512-8. (PMID: 9098046)
J Mol Biol. 1977 Sep 25;115(3):335-54. (PMID: 338910)
BMC Genomics. 2013 May 03;14:299. (PMID: 23641968)
Appl Environ Microbiol. 2008 Mar;74(6):1812-9. (PMID: 18245259)
Evid Based Complement Alternat Med. 2022 Apr 13;2022:9255444. (PMID: 35463066)
J Exp Biol. 2000 Jan;203(Pt 1):89-95. (PMID: 10600677)
Mol Cancer Ther. 2017 Nov;16(11):2329-2339. (PMID: 28775146)
Biochim Biophys Acta. 2001 May 1;1505(1):75-81. (PMID: 11248190)
Gastroenterology. 1990 Nov;99(5):1452-9. (PMID: 2210252)
BMC Gastroenterol. 2020 Oct 31;20(1):363. (PMID: 33129276)
Infect Control Hosp Epidemiol. 2008 Nov;29(11):996-1011. (PMID: 18947320)
Nucleic Acids Res. 2022 Jan 7;50(D1):D543-D552. (PMID: 34723319)
Nat Commun. 2021 Mar 19;12(1):1782. (PMID: 33741963)
Proc Natl Acad Sci U S A. 2003 Aug 5;100(16):9440-5. (PMID: 12883005)
mBio. 2012 Mar 01;3(1):e00318-11. (PMID: 22354958)
Nat Methods. 2016 Sep;13(9):731-40. (PMID: 27348712)
Front Vet Sci. 2022 Oct 13;9:989606. (PMID: 36311649)
J Bacteriol. 2014 Jun;196(11):2012-22. (PMID: 24659768)
Appl Environ Microbiol. 2007 Sep;73(18):5767-74. (PMID: 17660310)
Dig Dis Sci. 2023 Feb;68(2):630-643. (PMID: 36562889)
Mol Biol Evol. 2017 Aug 1;34(8):2115-2122. (PMID: 28460117)
Antimicrob Agents Chemother. 2017 Jul 25;61(8):. (PMID: 28559254)
Nucleic Acids Res. 2019 Jan 8;47(D1):D309-D314. (PMID: 30418610)

Keywords: Enterococcus faecalis; Enterococcus faecium; Bile acids; DIA-MS; Proteomics; Resistance mechanisms

0 (Bile Acids and Salts)
005990WHZZ (Deoxycholic Acid)
G1JO7801AE (Cholic Acid)
0GEI24LG0J (Chenodeoxycholic Acid)

Date Created: 20240403 Date Completed: 20240405 Latest Revision: 20240406

20240406

PMC10988882

10.1186/s12866-024-03253-0

38570789