TY - JOUR
T1 - Nuclear magnetic resonance metabolomics of symbioses between bacterial vaginosis associated bacteria
AU - Horrocks, Victoria
AU - Hind, Charlotte K.
AU - Wand, Matthew E.
AU - Fady, Paul-Enguerrand
AU - Chan, Joel
AU - Hopkins, Jade
AU - Houston, Georgina
AU - Tribe, Rachel
AU - Sutton, John
AU - Mason, James
N1 - Funding Information:
NMR experiments described in this paper were carried out using the facilities of the Centre for Biomolecular Spectroscopy, King’s College London, using instruments acquired with a Multiuser Equipment Grant from the Wellcome Trust and an Infrastructure Grant from the British Heart Foundation. V.H. was supported by a King’s College London iCASE award, affiliated with the London Interdisciplinary Doctoral Program (LIDo), and Public Health England. Funding for the INSGHT cohort providing swabs was provided from Tommy’s Charity (no. 1060508); NIHR Biomedical Research Centre (BRC) based at Guy’s and St. Thomas’ National Health Service Foundation Trust, and the Rosetrees Trust (charity no. 298582) (M303-CD1). P.F. was supported by a BBSRC LIDo iCASE studentship with Public Health England 2081638.
Funding Information:
NMR experiments described in this paper were carried out using the facilities of the Centre for Biomolecular Spectroscopy, King’s College London, using instruments acquired with a Multiuser Equipment Grant from the Wellcome Trust and an Infrastructure Grant from the British Heart Foundation. V.H. was supported by a King’s College London iCASE award, affiliated with the London Interdisciplinary Doctoral Program (LIDo), and Public Health England. Funding for the INSGHT cohort providing swabs was provided from Tommy’s Charity (no. 1060508); NIHR Biomedical Research Centre (BRC) based at Guy’s and St. Thomas’ National Health Service Foundation Trust, and the Rosetrees Trust (charity no. 298582) (M303-CD1). P.F. was supported by a BBSRC LIDo iCASE studentship with Public Health England 2081638. This research was funded/supported by the National Institute for Health Research (NIHR) Biomedical Research Centre based at Guy’s and St Thomas’ NHS Foundation Trust and King’s College London and/or the NIHR Clinical Research Facility. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR, or the Department of Health and Social Care. We thank Andrew Atkinson, Adrien Le Guennec, and James Jarvis for assistance with liquid-state NMR experiments performed at KCL. We thank Collette Allen at SDH for providing patient swabs. V.H., C.K.H., R.M.T., J.M.S., and A.J.M. designed the study. V.H. and A.J.M. wrote the main manuscript text and prepared all figures apart from Fig. 7, which was prepared by V.H. and P.-E.F. Assisted by P.-E.F., J.C., J.H., and G.H., V.H. conducted all bacterial culture and NMR metabolomics experiments and, together with A.J.M., analyzed the data. M.E.W. carried out the analysis of whole-genome sequence data. V.A. and C.K.H. obtained isolates from swabs supplied by R.M.T. All authors approved the manuscript.
Publisher Copyright:
© 2022 Horrocks et al.
PY - 2022/6/29
Y1 - 2022/6/29
N2 - Bacterial vaginosis (BV) is a dysbiosis of the vaginal microbiome, characterized by low levels of lactobacilli and overgrowth of a diverse group of bacteria, associated with higher risk of a variety of infections, surgical complications, cancer, and preterm birth (PTB). Despite the lack of a consistently applicable etiology, Prevotella spp. are often associated with both BV and PTB, and Pr. bivia has known symbiotic relationships with both Peptostreptococcus anaerobius and Gardnerella vaginalis. Higher risk of PTB can also be predicted by a composite of metabolites linked to bacterial metabolism, but their specific bacterial source remains poorly understood. Here, we characterize diversity of metabolic strategies among BV-associated bacteria and lactobacilli and the symbiotic metabolic relationships between Pr. bivia and its partners and show how these influence the availability of metabolites associated with BV/PTB and/or pro- or anti-inflammatory immune responses. We confirm a commensal relationship between Pe. anaerobius and Pr. bivia, refining its mechanism, which sustains a substantial increase in acetate production. In contrast, the relationship between Pr. bivia and G. vaginalis strains, with sequence variant G2, is mutualistic, with outcome dependent on the metabolic strategy of the G. vaginalis strain. Taken together, our data show how knowledge of inter- and intraspecies metabolic diversity and the effects of symbiosis may refine our understanding of the mechanism and approach to risk prediction in BV and/or PTB.
AB - Bacterial vaginosis (BV) is a dysbiosis of the vaginal microbiome, characterized by low levels of lactobacilli and overgrowth of a diverse group of bacteria, associated with higher risk of a variety of infections, surgical complications, cancer, and preterm birth (PTB). Despite the lack of a consistently applicable etiology, Prevotella spp. are often associated with both BV and PTB, and Pr. bivia has known symbiotic relationships with both Peptostreptococcus anaerobius and Gardnerella vaginalis. Higher risk of PTB can also be predicted by a composite of metabolites linked to bacterial metabolism, but their specific bacterial source remains poorly understood. Here, we characterize diversity of metabolic strategies among BV-associated bacteria and lactobacilli and the symbiotic metabolic relationships between Pr. bivia and its partners and show how these influence the availability of metabolites associated with BV/PTB and/or pro- or anti-inflammatory immune responses. We confirm a commensal relationship between Pe. anaerobius and Pr. bivia, refining its mechanism, which sustains a substantial increase in acetate production. In contrast, the relationship between Pr. bivia and G. vaginalis strains, with sequence variant G2, is mutualistic, with outcome dependent on the metabolic strategy of the G. vaginalis strain. Taken together, our data show how knowledge of inter- and intraspecies metabolic diversity and the effects of symbiosis may refine our understanding of the mechanism and approach to risk prediction in BV and/or PTB.
UR - http://www.scopus.com/inward/record.url?scp=85133214566&partnerID=8YFLogxK
U2 - https://doi.org/10.1128/msphere.00166-22
DO - https://doi.org/10.1128/msphere.00166-22
M3 - Article
VL - 7
SP - e0016622
JO - mSphere
JF - mSphere
IS - 3
ER -
