Syntrophic bacterial and host–microbe interactions in bacterial vaginosis

Lee, Elliot M.; Srinivasan, Sujatha; Purvine, Samuel O.; Fiedler, Tina L.; Leiser, Owen P.; Proll, Sean C.; Minot, Samuel S.; Djukovic, Danijel; Raftery, Daniel; Johnston, Christine; Fredricks, David N.; Deatherage Kaiser, Brooke L.

doi:10.1093/ismejo/wraf055

Syntrophic bacterial and host–microbe interactions in bacterial vaginosis

Journal Article · Fri Jun 27 00:00:00 EDT 2025 · The ISME Journal

DOI:https://doi.org/10.1093/ismejo/wraf055· OSTI ID:2584069

Lee, Elliot M. ^[1]; Srinivasan, Sujatha ^[1]; ^[2]; Fiedler, Tina L. ^[1]; ^[3]; Proll, Sean C. ^[1]; Minot, Samuel S. ^[1]; ^[4]; Raftery, Daniel ^[4]; Johnston, Christine ^[5]; Fredricks, David N. ^[5]; Deatherage Kaiser, Brooke L. ^[3]

Fred Hutchinson Cancer Center, Seattle, WA (United States)
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Pacific Northwest National Laboratory (PNNL), Seattle, WA (United States)
Univ. of Washington, Seattle, WA (United States)
Fred Hutchinson Cancer Center, Seattle, WA (United States); Univ. of Washington, Seattle, WA (United States)

Bacterial vaginosis (BV) is a common, polymicrobial condition of the vaginal microbiota that is associated with symptoms such as malodor and excessive discharge, along with increased risk of various adverse sequelae. Host–bacteria and bacteria–bacteria interactions are thought to contribute to the condition, but many of these functions have yet to be elucidated. Using untargeted metaproteomics, we identified 1068 host and 1418 bacterial proteins in a set of cervicovaginal lavage samples collected from 20 participants with BV and 9 who were negative for the condition. We identified Dialister micraerophilus as a major producer of malodorous polyamines and identified a syntrophic interaction between this organism and Fannyhessea vaginae that leads to increased production of putrescine, a metabolite characteristic of BV. Although formate synthesis has not previously been noted in BV, we discovered diverse bacteria associated with the condition express pyruvate formate-lyase enzymes in vivo and confirm these organisms secrete formic acid in vitro. Sodium hypophosphite efficiently inhibited this function in multiple taxa. We also found that the fastidious organism Coriobacteriales bacterium DNF00809 can metabolize formic acid secreted by Gardnerella vaginalis, representing another syntrophic interaction. We noted an increased abundance of the host epithelial repair protein transglutaminase 3 in the metaproteomic data, which we confirmed by enzyme-linked immunosorbent assay. Other proteins identified in our samples implicate Finegoldia magna and Parvimonas micra in the production of malodorous trimethylamine. Some bacterial proteins identified represent novel targets for future therapeutics to disrupt BV communities and promote vaginal colonization by commensal lactobacilli.

View Accepted Manuscript (DOE)

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); National Institutes of Health (NIH); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 2584069

Report Number(s):: PNNL-SA--193226

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 1 Vol. 19; ISSN 1751-7362; ISSN 1751-7370

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (99)

A two-step database search method improves sensitivity in peptide sequence matches for metaproteomics and proteogenomics studies Jagtap, Pratik; Goslinga, Jill; Kooren, Joel A. PROTEOMICS, Vol. 13, Issue 8 https://doi.org/10.1002/pmic.201200352	journal	March 2013
Bacteriocin production and gene sequencing analysis from vaginal Lactobacillus strains Stoyancheva, Galina; Marzotto, Marta; Dellaglio, Franco Archives of Microbiology, Vol. 196, Issue 9 https://doi.org/10.1007/s00203-014-1003-1	journal	June 2014
Characterization of a novel type of glycogen-degrading amylopullulanase from Lactobacillus crispatus Zhang, Jie; Li, Lili; Zhang, Tong Applied Microbiology and Biotechnology, Vol. 106, Issue 11 https://doi.org/10.1007/s00253-022-11975-2	journal	May 2022
Vaginal microbiome and metabolome highlight specific signatures of bacterial vaginosis Vitali, B.; Cruciani, F.; Picone, G. European Journal of Clinical Microbiology & Infectious Diseases, Vol. 34, Issue 12 https://doi.org/10.1007/s10096-015-2490-y	journal	September 2015
Comparison of the Accuracy of Experimental and Predicted pKa Values of Basic and Acidic Compounds Settimo, Luca; Bellman, Krista; Knegtel, Ronald M. A. Pharmaceutical Research, Vol. 31, Issue 4 https://doi.org/10.1007/s11095-013-1232-z	journal	November 2013
Animal Models and Alternatives in Vaginal Research: a Comparative Review McCracken, Jennifer M.; Calderon, Gisele A.; Robinson, Andrew J. Reproductive Sciences, Vol. 28, Issue 6 https://doi.org/10.1007/s43032-021-00529-y	journal	April 2021
Nonspecific vaginitis Amsel, Richard; Totten, Patricia A.; Spiegel, Carol A. The American Journal of Medicine, Vol. 74, Issue 1 https://doi.org/10.1016/0002-9343(83)91112-9	journal	January 1983
High substrate specificity and induction characteristics of trimethylamine-N-oxide reductase of Escherichia coli Iobbi-Nivol, Chantal; Pommier, Janine; Simala-Grant, Joanne Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, Vol. 1294, Issue 1 https://doi.org/10.1016/0167-4838(95)00271-5	journal	May 1996
Transglutaminase: Mechanistic features of the active site as determined by kinetic and inhibitor studies Folk, J. E.; Cole, P. W. Biochimica et Biophysica Acta (BBA) - Enzymology and Biological Oxidation, Vol. 122, Issue 2 https://doi.org/10.1016/0926-6593(66)90066-x	journal	August 1966
Ornithine ingestion and growth hormone release in bodybuilders Bucci, Luke; Hickson, James F.; Pivarnik, James M. Nutrition Research, Vol. 10, Issue 3 https://doi.org/10.1016/S0271-5317(05)80265-9	journal	March 1990
Microbial Respiration and Formate Oxidation as Metabolic Signatures of Inflammation-Associated Dysbiosis Hughes, Elizabeth R.; Winter, Maria G.; Duerkop, Breck A. Cell Host & Microbe, Vol. 21, Issue 2 https://doi.org/10.1016/j.chom.2017.01.005	journal	February 2017
Buried Treasure: Evolutionary Perspectives on Microbial Iron Piracy Barber, Matthew F.; Elde, Nels C. Trends in Genetics, Vol. 31, Issue 11 https://doi.org/10.1016/j.tig.2015.09.001	journal	November 2015
Determination of pKa values and total proton distribution pattern of spermidine by carbon-13 nuclear magnetic resonance titrations Kimberly, Mary M.; Goldstein, J. H. Analytical Chemistry, Vol. 53, Issue 6 https://doi.org/10.1021/ac00229a011	journal	May 1981
Chemically Etched Open Tubular and Monolithic Emitters for Nanoelectrospray Ionization Mass Spectrometry Kelly, Ryan T.; Page, Jason S.; Luo, Quanzhou Analytical Chemistry, Vol. 78, Issue 22, p. 7796-7801 https://doi.org/10.1021/ac061133r	journal	November 2006
Structure and Function of the Acetylpolyamine Amidohydrolase from the Deep Earth Halophile Marinobacter subterrani Osko, Jeremy D.; Roose, Benjamin W.; Shinsky, Stephen A. Biochemistry, Vol. 58, Issue 36 https://doi.org/10.1021/acs.biochem.9b00582	journal	August 2019
Characterization of Choline Trimethylamine-Lyase Expands the Chemistry of Glycyl Radical Enzymes Craciun, Smaranda; Marks, Jonathan A.; Balskus, Emily P. ACS Chemical Biology, Vol. 9, Issue 7 https://doi.org/10.1021/cb500113p	journal	May 2014
Comprehensive Proteomic Study Identifies Serpin and Cystatin Antiproteases as Novel Correlates of HIV-1 Resistance in the Cervicovaginal Mucosa of Female Sex Workers Burgener, A.; Rahman, S.; Ahmad, R. Journal of Proteome Research, Vol. 10, Issue 11 https://doi.org/10.1021/pr200596r	journal	October 2011
Trimethylamine content in vaginal secretion and its relation to bacterial vaginosis Wolrath, Helen; BorÉN, Hans; HallÉN, Anders APMIS, Vol. 110, Issue 11 https://doi.org/10.1034/j.1600-0463.2002.1101108.x	journal	November 2002
Lactobacillus-dominated cervicovaginal microbiota associated with reduced HIV/STI prevalence and genital HIV viral load in African women Borgdorff, Hanneke; Tsivtsivadze, Evgeni; Verhelst, Rita The ISME Journal, Vol. 8, Issue 9 https://doi.org/10.1038/ismej.2014.26	journal	March 2014
MetaPhlAn2 for enhanced metagenomic taxonomic profiling Truong, Duy Tin; Franzosa, Eric A.; Tickle, Timothy L. Nature Methods, Vol. 12, Issue 10 https://doi.org/10.1038/nmeth.3589	journal	September 2015
DADA2: High-resolution sample inference from Illumina amplicon data Callahan, Benjamin J.; McMurdie, Paul J.; Rosen, Michael J. Nature Methods, Vol. 13, Issue 7 https://doi.org/10.1038/nmeth.3869	journal	May 2016
The cornified envelope: a model of cell death in the skin Candi, Eleonora; Schmidt, Rainer; Melino, Gerry Nature Reviews Molecular Cell Biology, Vol. 6, Issue 4 https://doi.org/10.1038/nrm1619	journal	April 2005
Bacterial amylases enable glycogen degradation by the vaginal microbiome Jenkins, Dominick J.; Woolston, Benjamin M.; Hood-Pishchany, M. Indriati Nature Microbiology, Vol. 8, Issue 9 https://doi.org/10.1038/s41564-023-01447-2	journal	August 2023
The vaginal microbiome and preterm birth Fettweis, Jennifer M.; Serrano, Myrna G.; Brooks, J. Paul Nature Medicine, Vol. 25, Issue 6 https://doi.org/10.1038/s41591-019-0450-2	journal	May 2019
Randomized Trial of Lactin-V to Prevent Recurrence of Bacterial Vaginosis Cohen, Craig R.; Wierzbicki, Michael R.; French, Audrey L. New England Journal of Medicine, Vol. 382, Issue 20 https://doi.org/10.1056/nejmoa1915254	journal	May 2020
Carnitine metabolism to trimethylamine by an unusual Rieske-type oxygenase from human microbiota Zhu, Y.; Jameson, E.; Crosatti, M. Proceedings of the National Academy of Sciences, Vol. 111, Issue 11 https://doi.org/10.1073/pnas.1316569111	journal	March 2014
Post-translational activation introduces a free radical into pyruvate formate-lyase. Knappe, J.; Neugebauer, F. A.; Blaschkowski, H. P. Proceedings of the National Academy of Sciences, Vol. 81, Issue 5 https://doi.org/10.1073/pnas.81.5.1332	journal	March 1984
Degradation, Foraging, and Depletion of Mucus Sialoglycans by the Vagina-adapted Actinobacterium Gardnerella vaginalis Lewis, Warren G.; Robinson, Lloyd S.; Gilbert, Nicole M. Journal of Biological Chemistry, Vol. 288, Issue 17 https://doi.org/10.1074/jbc.M113.453654	journal	April 2013
Hydrolysis of Secreted Sialoglycoprotein Immunoglobulin A (IgA) in ex Vivo and Biochemical Models of Bacterial Vaginosis Lewis, Warren G.; Robinson, Lloyd S.; Perry, Justin Journal of Biological Chemistry, Vol. 287, Issue 3 https://doi.org/10.1074/jbc.m111.278135	journal	January 2012
Structures of the Bacillus subtilis Glutamine Synthetase Dodecamer Reveal Large Intersubunit Catalytic Conformational Changes Linked to a Unique Feedback Inhibition Mechanism Murray, David S.; Chinnam, Nagababu; Tonthat, Nam Ky Journal of Biological Chemistry, Vol. 288, Issue 50 https://doi.org/10.1074/jbc.m113.519496	journal	December 2013
Amino Acid Catabolic Pathways of Lactic Acid Bacteria Fernández, María; Zúñiga, Manuel Critical Reviews in Microbiology, Vol. 32, Issue 3 https://doi.org/10.1080/10408410600880643	journal	January 2006
Vaginal lactoferrin in prevention of preterm birth in women with bacterial vaginosis Miranda, Marilena; Saccone, Gabriele; Ammendola, Alessandra The Journal of Maternal-Fetal & Neonatal Medicine, Vol. 34, Issue 22 https://doi.org/10.1080/14767058.2019.1690445	journal	November 2019
Metaproteomic data analysis at a glance: advances in computational microbial community proteomics Muth, Thilo; Renard, Bernhard Y.; Martens, Lennart Expert Review of Proteomics, Vol. 13, Issue 8 https://doi.org/10.1080/14789450.2016.1209418	journal	July 2016
Indications for Therapy and Treatment Recommendations for Bacterial Vaginosis in Nonpregnant and Pregnant Women: A Synthesis of Data Koumans, Emilia H.; Markowitz, Lauri E.; Hogan, Vijaya Clinical Infectious Diseases, Vol. 35, Issue s2 https://doi.org/10.1086/342103	journal	October 2002
Bacterial Vaginosis and Anaerobic Bacteria Are Associated with Endometritis Haggerty, Catherine L.; Hillier, Sharon L.; Bass, Debra C. Clinical Infectious Diseases, Vol. 39, Issue 7 https://doi.org/10.1086/423963	journal	October 2004
High Recurrence Rates of Bacterial Vaginosis over the Course of 12 Months after Oral Metronidazole Therapy and Factors Associated with Recurrence Bradshaw, Catriona S.; Morton, Anna N.; Hocking, Jane The Journal of Infectious Diseases, Vol. 193, Issue 11 https://doi.org/10.1086/503780	journal	June 2006
Mucosal Integrity Factors Are Perturbed during Bacterial Vaginosis: A Proteomic Analysis Arnold, Kelly; Birse, Kenzie; Mckinnon, Lyle AIDS Research and Human Retroviruses, Vol. 30, Issue S1 https://doi.org/10.1089/aid.2014.5046.abstract	journal	October 2014
Heme Scavenging and the Other Facets of Hemopexin Tolosano, Emanuela; Fagoonee, Sharmila; Morello, Noemi Antioxidants & Redox Signaling, Vol. 12, Issue 2 https://doi.org/10.1089/ars.2009.2787	journal	January 2010
Prokka: rapid prokaryotic genome annotation Seemann, T. Bioinformatics, Vol. 30, Issue 14 https://doi.org/10.1093/bioinformatics/btu153	journal	March 2014
Lactate physiology in health and disease Phypers, Barrie; Pierce, JM Tom Continuing Education in Anaesthesia Critical Care & Pain, Vol. 6, Issue 3 https://doi.org/10.1093/bjaceaccp/mkl018	journal	June 2006
Stool Microbiota at Neutrophil Recovery Is Predictive for Severe Acute Graft vs Host Disease After Hematopoietic Cell Transplantation Golob, Jonathan L.; Pergam, Steven A.; Srinivasan, Sujatha Clinical Infectious Diseases, Vol. 65, Issue 12 https://doi.org/10.1093/cid/cix699	journal	August 2017
Evidence for a Commensal, Symbiotic Relationship between Gardnerella vaginalis and Prevotella bivia Involving Ammonia: Potential Significance for Bacterial Vaginosis Pybus, V.; Onderdonk, A. B. Journal of Infectious Diseases, Vol. 175, Issue 2 https://doi.org/10.1093/infdis/175.2.406	journal	February 1997
Role of Gardnerella vaginalis in the Pathogenesis of Bacterial Vaginosis: A Conceptual Model Schwebke, Jane R.; Muzny, Christina A.; Josey, William E. The Journal of Infectious Diseases, Vol. 210, Issue 3 https://doi.org/10.1093/infdis/jiu089	journal	February 2014
Human α-amylase Present in Lower-Genital-Tract Mucosal Fluid Processes Glycogen to Support Vaginal Colonization by Lactobacillus Spear, Gregory T.; French, Audrey L.; Gilbert, Douglas The Journal of Infectious Diseases, Vol. 210, Issue 7 https://doi.org/10.1093/infdis/jiu231	journal	April 2014
More Easily Cultivated Than Identified: Classical Isolation With Molecular Identification of Vaginal Bacteria Srinivasan, Sujatha; Munch, Matthew M.; Sizova, Maria V. Journal of Infectious Diseases, Vol. 214, Issue suppl 1 https://doi.org/10.1093/infdis/jiw192	journal	July 2016
Gardnerella and Prevotella: Co-conspirators in the Pathogenesis of Bacterial Vaginosis Randis, Tara M.; Ratner, Adam J. The Journal of Infectious Diseases, Vol. 220, Issue 7 https://doi.org/10.1093/infdis/jiy705	journal	February 2019
Proteome profiles of vaginal fluids from women affected by bacterial vaginosis and healthy controls: outcomes of rifaximin treatment Cruciani, F.; Wasinger, V.; Turroni, S. Journal of Antimicrobial Chemotherapy, Vol. 68, Issue 11 https://doi.org/10.1093/jac/dkt244	journal	June 2013
eggNOG-mapper v2: Functional Annotation, Orthology Assignments, and Domain Prediction at the Metagenomic Scale Cantalapiedra, Carlos P.; Hernández-Plaza, Ana; Letunic, Ivica Molecular Biology and Evolution, Vol. 38, Issue 12 https://doi.org/10.1093/molbev/msab293	journal	October 2021
The PRIDE database resources in 2022: a hub for mass spectrometry-based proteomics evidences Perez-Riverol, Yasset; Bai, Jingwen; Bandla, Chakradhar Nucleic Acids Research, Vol. 50, Issue D1 https://doi.org/10.1093/nar/gkab1038	journal	November 2021
eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses Huerta-Cepas, Jaime; Szklarczyk, Damian; Heller, Davide Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky1085	journal	November 2018
Genital Herpes Simplex Virus Type 2 Suppression With Valacyclovir Is Not Associated With Changes in Nugent Score or Absolute Abundance of Key Vaginal Bacteria Babu, Tara M.; Srinivasan, Sujatha; Magaret, Amalia Open Forum Infectious Diseases, Vol. 10, Issue 3 https://doi.org/10.1093/ofid/ofad099	journal	March 2023
Effect of Putrescine on Tissue Transglutaminase Activity in Wounds Dolynchuk, Kenneth N.; Bendor-Samuel, Richard; Michael Bowness, J. Plastic and Reconstructive Surgery, Vol. 93, Issue 3 https://doi.org/10.1097/00006534-199493030-00020	journal	March 1994
Vulvovaginal Symptoms in Women With Bacterial Vaginosis Klebanoff, Mark A.; Schwebke, Jane R.; Zhang, Jun Obstetrics & Gynecology, Vol. 104, Issue 2 https://doi.org/10.1097/01.AOG.0000134783.98382.b0	journal	August 2004
The Prevalence of Bacterial Vaginosis in the United States, 2001–2004; Associations With Symptoms, Sexual Behaviors, and Reproductive Health Koumans, Emilia H.; Sternberg, Maya; Bruce, Carol Sexually Transmitted Diseases, Vol. 34, Issue 11 https://doi.org/10.1097/OLQ.0b013e318074e565	journal	November 2007
Prevalence and Risks for Bacterial Vaginosis in Women Who Have Sex With Women Marrazzo, Jeanne M.; Thomas, Katherine K.; Agnew, Kathy Sexually Transmitted Diseases, Vol. 37, Issue 5 https://doi.org/10.1097/OLQ.0b013e3181ca3cac	journal	May 2010
Emended description of Gardnerella vaginalis and description of Gardnerella leopoldii sp. nov., Gardnerella piotii sp. nov. and Gardnerella swidsinskii sp. nov., with delineation of 13 genomic species within the genus Gardnerella Vaneechoutte, Mario; Guschin, Alexander; Van Simaey, Leen International Journal of Systematic and Evolutionary Microbiology, Vol. 69, Issue 3 https://doi.org/10.1099/ijsem.0.003200	journal	March 2019
Amygdalobacter indicium gen. nov., sp. nov., and Amygdalobacter nucleatus sp. nov., gen. nov.: novel bacteria from the family Oscillospiraceae isolated from the female genital tract Srinivasan, Sujatha; Austin, Michele N.; Fiedler, Tina L. International Journal of Systematic and Evolutionary Microbiology, Vol. 73, Issue 10 https://doi.org/10.1099/ijsem.0.006017	journal	October 2023
metaSPAdes: a new versatile metagenomic assembler Nurk, Sergey; Meleshko, Dmitry; Korobeynikov, Anton Genome Research, Vol. 27, Issue 5 https://doi.org/10.1101/gr.213959.116	journal	March 2017
Formate cross-feeding and cooperative metabolic interactions revealed by transcriptomics in co-cultures of acetogenic and amylolytic human colonic bacteria: Coculture of acetogenic and amylolytic human gut bacteria Laverde Gomez, Jenny A.; Mukhopadhya, Indrani; Duncan, Sylvia H. Environmental Microbiology, Vol. 21, Issue 1 https://doi.org/10.1111/1462-2920.14454	journal	November 2018
Purification and Characterization of Protein PB of Betaine Reductase and its Relationship to the Corresponding Proteins Glycine Reductase and Sarcosine Reductase from Eubacterium Acidaminophilum Meyer, Manfred; Granderath, Katrin; Andreesen, Jan R. European Journal of Biochemistry, Vol. 234, Issue 1 https://doi.org/10.1111/j.1432-1033.1995.184_c.x	journal	November 1995
A commensal symbiosis betweenPrevotella biviaandPeptostreptococcus anaerobiusinvolves amino acids: potential significance to the pathogenesis of bacterial vaginosis Pybus, Vivien; Onderdonk, Andrew B. FEMS Immunology & Medical Microbiology, Vol. 22, Issue 4 https://doi.org/10.1111/j.1574-695x.1998.tb01221.x	journal	December 1998
A radical-chemical route to acetyl-CoA: the anaerobically induced pyruvate formate-lyase system of Escherichia coli Knappe, Joachim; Sawers, Gary FEMS Microbiology Letters, Vol. 75, Issue 4 https://doi.org/10.1111/j.1574-6968.1990.tb04108.x	journal	August 1990
Pharmacological and Clinical Aspects of Heme Oxygenase Abraham, Nader G.; Kappas, Attallah Pharmacological Reviews, Vol. 60, Issue 1 https://doi.org/10.1124/pr.107.07104	journal	March 2008
Analysis of Bacterial Vaginosis-Related Amines in Vaginal Fluid by Gas Chromatography and Mass Spectrometry Wolrath, Helen; Forsum, Urban; Larsson, P. G. Journal of Clinical Microbiology, Vol. 39, Issue 11 https://doi.org/10.1128/JCM.39.11.4026-4031.2001	journal	November 2001
Interaction of Gardnerella vaginalis and Vaginolysin with the Apical versus Basolateral Face of a Three-Dimensional Model of Vaginal Epithelium Garcia, Erin M.; Kraskauskiene, Vita; Koblinski, Jennifer E. Infection and Immunity, Vol. 87, Issue 4 https://doi.org/10.1128/iai.00646-18	journal	April 2019
Acquisition of Iron byGardnerella vaginalis Jarosik, Gregory P.; Land, Carol Beth; Duhon, Patrice Infection and Immunity, Vol. 66, Issue 10 https://doi.org/10.1128/iai.66.10.5041-5047.1998	journal	October 1998
Glycogen-Degrading Activities of Catalytic Domains of α-Amylase and α-Amylase-Pullulanase Enzymes Conserved in Gardnerella spp. from the Vaginal Microbiome Bhandari, Pashupati; Tingley, Jeffrey; Abbott, D. Wade Journal of Bacteriology, Vol. 205, Issue 2 https://doi.org/10.1128/jb.00393-22	journal	February 2023
Identification of elements involved in transcriptional regulation of the Escherichia coli cad operon by external pH Watson, N.; Dunyak, D. S.; Rosey, E. L. Journal of Bacteriology, Vol. 174, Issue 2 https://doi.org/10.1128/jb.174.2.530-540.1992	journal	January 1992
Functional Analysis and Regulation of the Divergent spuABCDEFGH-spuI Operons for Polyamine Uptake and Utilization in Pseudomonas aeruginosa PAO1 Lu, Chung-Dar; Itoh, Yoshifumi; Nakada, Yuji Journal of Bacteriology, Vol. 184, Issue 14 https://doi.org/10.1128/jb.184.14.3765-3773.2002	journal	July 2002
Quantitative PCR Assessments of Bacterial Species in Women with and without Bacterial Vaginosis Zozaya-Hinchliffe, Marcela; Lillis, Rebecca; Martin, David H. Journal of Clinical Microbiology, Vol. 48, Issue 5 https://doi.org/10.1128/jcm.00851-09	journal	May 2010
Targeted PCR for Detection of Vaginal Bacteria Associated with Bacterial Vaginosis Fredricks, David N.; Fiedler, Tina L.; Thomas, Katherine K. Journal of Clinical Microbiology, Vol. 45, Issue 10 https://doi.org/10.1128/jcm.01272-07	journal	October 2007
Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation Nugent, R. P.; Krohn, M. A.; Hillier, S. L. Journal of Clinical Microbiology, Vol. 29, Issue 2 https://doi.org/10.1128/jcm.29.2.297-301.1991	journal	February 1991
Metabolic Signatures of Bacterial Vaginosis Srinivasan, Sujatha; Morgan, Martin T.; Fiedler, Tina L. mBio, Vol. 6, Issue 2 https://doi.org/10.1128/mbio.00204-15	journal	May 2015
Amylases in the Human Vagina Nunn, Kenetta L.; Clair, Geremy C.; Adkins, Joshua N. mSphere, Vol. 5, Issue 6 https://doi.org/10.1128/msphere.00943-20	journal	December 2020
Optimizing metaproteomics database construction: lessons from a study of the vaginal microbiome Lee, Elliot M.; Srinivasan, Sujatha; Purvine, Samuel O. mSystems https://doi.org/10.1128/msystems.00678-22	journal	June 2023
DoAtopobium vaginae, Megasphaerasp. andLeptotrichiasp. change the local innate immune response and sialidase activity in bacterial vaginosis? Marconi, Camila; Donders, Gilbert G.; Parada, Cristina M. G. L. Sexually Transmitted Infections, Vol. 89, Issue 2 https://doi.org/10.1136/sextrans-2012-050616	journal	October 2012
Arginase: A Multifaceted Enzyme Important in Health and Disease Caldwell, R. William; Rodriguez, Paulo C.; Toque, Haroldo A. Physiological Reviews, Vol. 98, Issue 2 https://doi.org/10.1152/physrev.00037.2016	journal	April 2018
Association Between Components of Exudates and Periwound Moisture-Associated Dermatitis in Breast Cancer Patients With Malignant Fungating Wounds Tamai, Nao; Akase, Tomoko; Minematsu, Takeo Biological Research For Nursing, Vol. 18, Issue 2 https://doi.org/10.1177/1099800415594452	journal	July 2015
pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree Matsen, Frederick A.; Kodner, Robin B.; Armbrust, E. Virginia BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-538	journal	October 2010
Genome sequence-based species delimitation with confidence intervals and improved distance functions Meier-Kolthoff, Jan P.; Auch, Alexander F.; Klenk, Hans-Peter BMC Bioinformatics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2105-14-60	journal	January 2013
Comparative genomics of Lactobacillus crispatus suggests novel mechanisms for the competitive exclusion of Gardnerella vaginalis Ojala, Teija; Kankainen, Matti; Castro, Joana BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-1070	journal	January 2014
Survey of bacterial diversity in chronic wounds using Pyrosequencing, DGGE, and full ribosome shotgun sequencing Dowd, Scot E.; Sun, Yan; Secor, Patrick R. BMC Microbiology, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2180-8-43	journal	January 2008
Bacterial vaginosis is associated with uterine cervical human papillomavirus infection: a meta-analysis Gillet, Evy; Meys, Joris FA; Verstraelen, Hans BMC Infectious Diseases, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2334-11-10	journal	January 2011
Development and optimization of quantitative PCR for the diagnosis of invasive aspergillosis with bronchoalveolar lavage fluid Khot, Prasanna D.; Ko, Daisy L.; Hackman, Robert C. BMC Infectious Diseases, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2334-8-73	journal	May 2008
Vaginal pH measured in vivo: lactobacilli determine pH and lactic acid concentration O’Hanlon, Deirdre Elizabeth; Come, Richard A.; Moench, Thomas R. BMC Microbiology, Vol. 19, Issue 1 https://doi.org/10.1186/s12866-019-1388-8	journal	January 2019
geneshot: gene-level metagenomics identifies genome islands associated with immunotherapy response Minot, Samuel S.; Barry, Kevin C.; Kasman, Caroline Genome Biology, Vol. 22, Issue 1 https://doi.org/10.1186/s13059-021-02355-6	journal	May 2021
Temporal Variability of Human Vaginal Bacteria and Relationship with Bacterial Vaginosis Srinivasan, Sujatha; Liu, Congzhou; Mitchell, Caroline M. PLoS ONE, Vol. 5, Issue 4 https://doi.org/10.1371/journal.pone.0010197	journal	April 2010
New Insight into the Transcarbamylase Family: The Structure of Putrescine Transcarbamylase, a Key Catalyst for Fermentative Utilization of Agmatine Polo, Luis Mariano; Gil-Ortiz, Fernando; Cantín, Angel PLoS ONE, Vol. 7, Issue 2 https://doi.org/10.1371/journal.pone.0031528	journal	February 2012
Bacterial Communities in Women with Bacterial Vaginosis: High Resolution Phylogenetic Analyses Reveal Relationships of Microbiota to Clinical Criteria Srinivasan, Sujatha; Hoffman, Noah G.; Morgan, Martin T. PLoS ONE, Vol. 7, Issue 6 https://doi.org/10.1371/journal.pone.0037818	journal	June 2012
Free Glycogen in Vaginal Fluids Is Associated with Lactobacillus Colonization and Low Vaginal pH Mirmonsef, Paria; Hotton, Anna L.; Gilbert, Douglas PLoS ONE, Vol. 9, Issue 7 https://doi.org/10.1371/journal.pone.0102467	journal	July 2014
Lactic acid-containing products for bacterial vaginosis and their impact on the vaginal microbiota: A systematic review Plummer, Erica L.; Bradshaw, Catriona S.; Doyle, Michelle PLOS ONE, Vol. 16, Issue 2 https://doi.org/10.1371/journal.pone.0246953	journal	February 2021
Reduction of Trimethylamine Oxide to Trimethylamine by Mobiluncus Strains Isolated from Patients with Bacterial Vaginosis Cruden, Diana L.; Galask, R. P. Microbial Ecology in Health and Disease, Vol. 1, Issue 2 https://doi.org/10.3109/08910608809140187	journal	January 1988
Gardnerella vaginalis Enhances Atopobium vaginae Viability in an in vitro Model Castro, Joana; Rosca, Aliona S.; Cools, Piet Frontiers in Cellular and Infection Microbiology, Vol. 10 https://doi.org/10.3389/fcimb.2020.00083	journal	March 2020
The role of polyamine metabolism in remodeling immune responses and blocking therapy within the tumor immune microenvironment Lian, Jiachun; Liang, Yanfang; Zhang, Hailiang Frontiers in Immunology, Vol. 13 https://doi.org/10.3389/fimmu.2022.912279	journal	September 2022
Bacterial Vaginosis Biofilms: Challenges to Current Therapies and Emerging Solutions Machado, Daniela; Castro, Joana; Palmeira-de-Oliveira, Ana Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01528	journal	January 2016
Vaginal biogenic amines: biomarkers of bacterial vaginosis or precursors to vaginal dysbiosis? Nelson, Tiffanie M.; Borgogna, Joanna-Lynn C.; Brotman, Rebecca M. Frontiers in Physiology, Vol. 6 https://doi.org/10.3389/fphys.2015.00253	journal	September 2015
Transglutaminase 3: The Involvement in Epithelial Differentiation and Cancer Chermnykh, Elina S.; Alpeeva, Elena V.; Vorotelyak, Ekaterina A. Cells, Vol. 9, Issue 9 https://doi.org/10.3390/cells9091996	journal	August 2020
Crystal Structure of Escherichia coli Agmatinase: Catalytic Mechanism and Residues Relevant for Substrate Specificity Maturana, Pablo; Orellana, María S.; Herrera, Sixto M. International Journal of Molecular Sciences, Vol. 22, Issue 9 https://doi.org/10.3390/ijms22094769	journal	April 2021
Sodium Hypophosphite Inhibition of the Growth of Selected Gram Negative Foodborne Pathogenic and Spoilage Bacteria Rhodehamel, E. Jeffery; Pierson, Merle D. Journal of Food Protection, Vol. 53, Issue 1 https://doi.org/10.4315/0362-028x-53.1.56	journal	January 1990

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