Glycogen availability and pH variation in a medium simulating vaginal fluid influence the growth of vaginal Lactobacillus species and Gardnerella vaginalis.

Gardnerella vaginalis Glucose Glycogen Lactobacillus crispatus Lactobacillus gasseri Lactobacillus jensenii Medium simulating vaginal fluid pH

Journal

BMC microbiology
ISSN: 1471-2180
Titre abrégé: BMC Microbiol
Pays: England
ID NLM: 100966981

Informations de publication

Date de publication:
13 07 2023
Historique:
received: 10 03 2023
accepted: 27 06 2023
medline: 17 7 2023
pubmed: 14 7 2023
entrez: 13 7 2023
Statut: epublish

Résumé

Glycogen metabolism by Lactobacillus spp. that dominate the healthy vaginal microbiome contributes to a low vaginal pH (3.5-4.5). During bacterial vaginosis (BV), strict and facultative anaerobes including Gardnerella vaginalis become predominant, leading to an increase in the vaginal pH (> 4.5). BV enhances the risk of obstetrical complications, acquisition of sexually transmitted infections, and cervical cancer. Factors critical for the maintenance of the healthy vaginal microbiome or the transition to the BV microbiome are not well defined. Vaginal pH may affect glycogen metabolism by the vaginal microflora, thus influencing the shift in the vaginal microbiome. The medium simulating vaginal fluid (MSVF) supported growth of L. jensenii 62G, L. gasseri 63 AM, and L. crispatus JV-V01, and G. vaginalis JCP8151A at specific initial pH conditions for 30 d. L. jensenii at all three starting pH levels (pH 4.0, 4.5, and 5.0), G. vaginalis at pH 4.5 and 5.0, and L. gasseri at pH 5.0 exhibited the long-term stationary phase when grown in MSVF. L. gasseri at pH 4.5 and L. crispatus at pH 5.0 displayed an extended lag phase over 30 d suggesting inefficient glycogen metabolism. Glycogen was essential for the growth of L. jensenii, L. crispatus, and G. vaginalis; only L. gasseri was able to survive in MSVF without glycogen, and only at pH 5.0, where it used glucose. All four species were able to survive for 15 d in MSVF with half the glycogen content but only at specific starting pH levels - pH 4.5 and 5.0 for L. jensenii, L. gasseri, and G. vaginalis and pH 5.0 for L. crispatus. These results suggest that variations in the vaginal pH critically influence the colonization of the vaginal tract by lactobacilli and G. vaginalis JCP8151A by affecting their ability to metabolize glycogen. Further, we found that L. jensenii 62G is capable of glycogen metabolism over a broader pH range (4.0-5.0) while L. crispatus JV-V01 glycogen utilization is pH sensitive (only functional at pH 5.0). Finally, our results showed that G. vaginalis JCP8151A can colonize the vaginal tract for an extended period as long as the pH remains at 4.5 or above.

Sections du résumé

BACKGROUND
Glycogen metabolism by Lactobacillus spp. that dominate the healthy vaginal microbiome contributes to a low vaginal pH (3.5-4.5). During bacterial vaginosis (BV), strict and facultative anaerobes including Gardnerella vaginalis become predominant, leading to an increase in the vaginal pH (> 4.5). BV enhances the risk of obstetrical complications, acquisition of sexually transmitted infections, and cervical cancer. Factors critical for the maintenance of the healthy vaginal microbiome or the transition to the BV microbiome are not well defined. Vaginal pH may affect glycogen metabolism by the vaginal microflora, thus influencing the shift in the vaginal microbiome.
RESULTS
The medium simulating vaginal fluid (MSVF) supported growth of L. jensenii 62G, L. gasseri 63 AM, and L. crispatus JV-V01, and G. vaginalis JCP8151A at specific initial pH conditions for 30 d. L. jensenii at all three starting pH levels (pH 4.0, 4.5, and 5.0), G. vaginalis at pH 4.5 and 5.0, and L. gasseri at pH 5.0 exhibited the long-term stationary phase when grown in MSVF. L. gasseri at pH 4.5 and L. crispatus at pH 5.0 displayed an extended lag phase over 30 d suggesting inefficient glycogen metabolism. Glycogen was essential for the growth of L. jensenii, L. crispatus, and G. vaginalis; only L. gasseri was able to survive in MSVF without glycogen, and only at pH 5.0, where it used glucose. All four species were able to survive for 15 d in MSVF with half the glycogen content but only at specific starting pH levels - pH 4.5 and 5.0 for L. jensenii, L. gasseri, and G. vaginalis and pH 5.0 for L. crispatus.
CONCLUSIONS
These results suggest that variations in the vaginal pH critically influence the colonization of the vaginal tract by lactobacilli and G. vaginalis JCP8151A by affecting their ability to metabolize glycogen. Further, we found that L. jensenii 62G is capable of glycogen metabolism over a broader pH range (4.0-5.0) while L. crispatus JV-V01 glycogen utilization is pH sensitive (only functional at pH 5.0). Finally, our results showed that G. vaginalis JCP8151A can colonize the vaginal tract for an extended period as long as the pH remains at 4.5 or above.

Identifiants

pubmed: 37442975
doi: 10.1186/s12866-023-02916-8
pii: 10.1186/s12866-023-02916-8
pmc: PMC10339506
doi:

Substances chimiques

Glycogen 9005-79-2

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

186

Informations de copyright

© 2023. The Author(s).

Références

Am J Reprod Immunol. 2014 Jun;71(6):618-23
pubmed: 24661416
Contraception. 1999 Feb;59(2):91-5
pubmed: 10361623
Front Microbiol. 2012 Sep 26;3:340
pubmed: 23055996
Appl Environ Microbiol. 2017 May 31;83(12):
pubmed: 28411221
Appl Environ Microbiol. 2021 Nov 24;87(24):e0186021
pubmed: 34613759
Nat Commun. 2019 Mar 21;10(1):1305
pubmed: 30899005
Contraception. 2016 Apr;93(4):337-346
pubmed: 26585883
BJOG. 2017 Mar;124(4):606-611
pubmed: 28224747
Front Cell Infect Microbiol. 2020 Feb 12;10:23
pubmed: 32117800
Front Physiol. 2015 Jun 02;6:164
pubmed: 26082720
Microbiome. 2014 Feb 03;2(1):4
pubmed: 24484853
Health Lab Sci. 1973 Apr;10(2):44-54
pubmed: 4633802
J Bacteriol. 1994 May;176(10):3007-12
pubmed: 8188601
PLoS One. 2016 Mar 02;11(3):e0150540
pubmed: 26934359
Sci Transl Med. 2012 May 2;4(132):132ra52
pubmed: 22553250
Nucleic Acids Res. 2021 Jan 8;49(D1):D498-D508
pubmed: 33211880
Nat Commun. 2020 Feb 26;11(1):940
pubmed: 32103005
Antimicrob Agents Chemother. 2017 Nov 22;61(12):
pubmed: 28893789
Front Cell Infect Microbiol. 2021 Jul 13;11:676114
pubmed: 34327149
Proteomics. 2017 Mar;17(5):
pubmed: 28045221
Front Med (Lausanne). 2018 Jun 13;5:181
pubmed: 29951482
Arch Gynecol Obstet. 2006 Jan;273(4):195-202
pubmed: 16208476
J Infect Dis. 2014 Oct 1;210(7):1019-28
pubmed: 24737800
Annu Rev Microbiol. 2012;66:371-89
pubmed: 22746335
Am J Obstet Gynecol. 2011 Feb;204(2):120.e1-5
pubmed: 20832044
Am J Reprod Immunol. 2014 Jun;71(6):531-6
pubmed: 24661438
J Theor Biol. 2007 Feb 7;244(3):511-7
pubmed: 17028032
Sci Rep. 2019 Oct 1;9(1):14095
pubmed: 31575935
J Bacteriol. 2021 Aug 9;203(17):e0021321
pubmed: 34124938
PLoS One. 2016 Apr 19;11(4):e0153553
pubmed: 27093050
Microbiome. 2019 Mar 29;7(1):49
pubmed: 30925932
J Med Microbiol. 1969 Aug;2(3):363-6
pubmed: 4996481
Biochem J. 1993 Oct 15;295 ( Pt 2):477-83
pubmed: 8240246
mSphere. 2020 Dec 9;5(6):
pubmed: 33298571
J Biomed Mater Res. 1982 Nov;16(6):839-50
pubmed: 6960000
FEMS Microbiol Lett. 2005 Nov 1;252(1):175-81
pubmed: 16198511
PLoS One. 2014 Jul 17;9(7):e102467
pubmed: 25033265
mSphere. 2020 Aug 12;5(4):
pubmed: 32817455
J Bacteriol. 2023 Feb 22;205(2):e0039322
pubmed: 36744900
Int J Mol Sci. 2022 May 17;23(10):
pubmed: 35628398
Clin Microbiol Rev. 2016 Apr;29(2):223-38
pubmed: 26864580
Proc Natl Acad Sci U S A. 2011 Mar 15;108 Suppl 1:4680-7
pubmed: 20534435
Int Microbiol. 2008 Dec;11(4):261-6
pubmed: 19204898
BJOG. 2020 Jan;127(2):171-180
pubmed: 31237400
PLoS One. 2014 Sep 12;9(9):e107758
pubmed: 25215504
Microb Cell Fact. 2018 May 9;17(1):69
pubmed: 29743073
J Bacteriol. 2019 Jun 10;201(13):
pubmed: 30988035
Microbiol Spectr. 2023 Mar 15;:e0443522
pubmed: 36920187
Am J Obstet Gynecol. 1964 Mar 1;88:676-9
pubmed: 14128200
J Infect Dis. 1997 Feb;175(2):406-13
pubmed: 9203662
Microb Pathog. 2020 Feb 24;142:104063
pubmed: 32061821
PLoS One. 2014 May 23;9(5):e96701
pubmed: 24858919
Ann Clin Microbiol Antimicrob. 2011 Feb 17;10:8
pubmed: 21329492
Nat Commun. 2019 Feb 21;10(1):890
pubmed: 30792386
Bioengineered. 2013 Nov-Dec;4(6):388-400
pubmed: 23645215
J Bacteriol. 2019 Mar 13;201(7):
pubmed: 30642990
Nucleic Acids Res. 2022 Jan 7;50(D1):D571-D577
pubmed: 34850161
J Infect Dis. 1999 Dec;180(6):1863-8
pubmed: 10558942
Appl Environ Microbiol. 2000 Dec;66(12):5316-21
pubmed: 11097908
Biochem J. 2012 Feb 1;441(3):763-87
pubmed: 22248338
Appl Microbiol Biotechnol. 2022 Jun;106(11):4053-4064
pubmed: 35612627
Am J Obstet Gynecol. 2021 Mar;224(3):251-257
pubmed: 33091407
Appl Environ Microbiol. 1990 Apr;56(4):1004-11
pubmed: 2187400
Reprod Sci. 2015 Nov;22(11):1393-8
pubmed: 25878210
Front Physiol. 2015 Mar 25;6:81
pubmed: 25859220
BMC Microbiol. 2010 Mar 12;10:77
pubmed: 20226062
Nat Rev Microbiol. 2006 Feb;4(2):113-20
pubmed: 16415927
Am J Med. 1983 Jan;74(1):14-22
pubmed: 6600371
BBA Clin. 2016 Feb 27;5:85-100
pubmed: 27051594
PLoS One. 2013 Nov 06;8(11):e80074
pubmed: 24223212
J Clin Microbiol. 1992 May;30(5):1323-6
pubmed: 1583140
mBio. 2015 Mar 24;6(2):
pubmed: 25805726
Hum Reprod. 2022 Jun 30;37(7):1525-1543
pubmed: 35553675

Auteurs

Stephany Navarro (S)

Department of Immunology and Molecular Microbiology, Texas Tech University Health Sciences Center, Lubbock, TX, USA.

Habib Abla (H)

School of Medicine, Texas Tech University Health Sciences Center, Lubbock, TX, USA.

Betsaida Delgado (B)

Honors College, Texas Tech University, Lubbock, TX, USA.
Woody L. Hunt School of Dental Medicine, Texas Tech University Health Sciences Center, Lubbock, TX, USA.

Jane A Colmer-Hamood (JA)

Department of Immunology and Molecular Microbiology, Texas Tech University Health Sciences Center, Lubbock, TX, USA.
Department of Medical Education, Texas Tech University Health Sciences Center, Lubbock, TX, USA.

Gary Ventolini (G)

Department of Obstetrics and Gynecology, Texas Tech University Health Sciences Center Permian Basin, Odessa, TX, USA.

Abdul N Hamood (AN)

Department of Immunology and Molecular Microbiology, Texas Tech University Health Sciences Center, Lubbock, TX, USA. abdul.hamood@ttuhsc.edu.
Department of Surgery, Texas Tech University Health Sciences Center, Lubbock, TX, USA. abdul.hamood@ttuhsc.edu.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH