Survival strategies and metabolic interactions between Ruminococcus gauvreauii and Ruminococcoides bili, isolated from human bile

Natalia Molinero; Elena Conti; Alan Walker; Abelardo Margolles; Sylvia Duncan; Susana  Delgado

doi:10.1128/spectrum.02776-21

Survival strategies and metabolic interactions between Ruminococcus gauvreauii and Ruminococcoides bili, isolated from human bile

Natalia Molinero ^* (Corresponding Author), Elena Conti, Alan Walker, Abelardo Margolles, Sylvia Duncan, Susana Delgado

^*Corresponding author for this work

The Rowett Institute of Nutrition and Health

Research output: Contribution to journal › Article › peer-review

7 Citations (Scopus)

Abstract

Little is known about the bacteria that reside in the human gallbladder and the mechanisms that allow them to survive within this harsh environment. Here we describe interactions between two strains from a human bile sample, one Ruminococcus gauvreauii (IPLA60001), belonging to the Lachnospiraceae family, and the other, designated as Ruminococcoides bili (IPLA60002T; DSM 110008) most closely related to Ruminococcus bromii within the family Ruminococcaceae. We provide evidence for bile salt resistance and sporulation for these new strains. Both differed markedly in their carbohydrate metabolism. The R. bili strain mainly metabolized resistant starches to form formate, lactate and acetate. R. gauvreauii mainly metabolized sugar alcohols, including inositol and also utilized formate to generate acetate employing the Wood Ljungdahl pathway. Amino acid and vitamin biosynthesis genomic profiles also differed markedly between the two isolates, likely contributing to their synergistic interactions, as revealed by transcriptomic analysis of cocultures. Transcriptome analysis also revealed that R. gauvreauii IPLA60001 is able to grow using the end-products of starch metabolism formed by the R. bili strain such as formate, and potentially other compounds (such as ethanolamine and inositol) possibly provided by the autolytic behavior of R. bili.

Original language	English
Article number	e0277621
Number of pages	14
Journal	Microbiology spectrum
Volume	10
Issue number	4
Early online date	11 Jul 2022
DOIs	https://doi.org/10.1128/spectrum.02776-21
Publication status	Published - Aug 2022

Bibliographical note

This work was funded by MINECO (Spanish Ministry of Economy and Competitiveness) under grant number AGL2013-44761-P, supported by FEDER (The European Regional Development Funds). N.M. was the recipient of an FPI Predoctoral Grant (BES-2014-068736) from MINECO. A.M. thanks the support of CSIC (PIE-201970E019 grant). N.M., A.M., and S.D. from the MicroHealth group would like to thank the grant of the “Plan for Research, Development and Innovation of the Principado de Asturias 2018–2020” (ref. IDI/2018/000236) co-financed by FEDER funds. S.H.D. and A.W.W. acknowledge core funding support for the Rowett Institute from the Scottish Government Rural and Environmental Sciences and Analytical Services (RESAS) as well as the support for E.C. from the Tenovus Charitable trust (Scotland). Donna Henderson from Rowett Institute (University of Aberdeen) is also acknowledged for carrying out the gas chromatography analysis.

Data Availability Statement

The whole-genome shotgun projects were deposited in the Sequence Read Archive (SRA) database of the NCBI under the accessions number SRR10273262 and SRR9209608. RNA-seq data were deposited in NCBI's Gene Expression Omnibus (42) and are accessible through GEO Series accession number GSE140753.

Keywords

syntrophy
survival
cross-feeding
co-cultures
ruminocci
bile resistance
SCFAs
stress conditions

Access to Document

10.1128/spectrum.02776-21Licence: CC BY

Molinero_etal_MbS_Survival_Strategies_and_VOR
© 2022 Molinero et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.
Final published version, 1.78 MBLicence: CC BY

Cite this

@article{8cd901a6755b4129bc391e1eddff4138,

title = "Survival strategies and metabolic interactions between Ruminococcus gauvreauii and Ruminococcoides bili, isolated from human bile",

abstract = "Little is known about the bacteria that reside in the human gallbladder and the mechanisms that allow them to survive within this harsh environment. Here we describe interactions between two strains from a human bile sample, one Ruminococcus gauvreauii (IPLA60001), belonging to the Lachnospiraceae family, and the other, designated as Ruminococcoides bili (IPLA60002T; DSM 110008) most closely related to Ruminococcus bromii within the family Ruminococcaceae. We provide evidence for bile salt resistance and sporulation for these new strains. Both differed markedly in their carbohydrate metabolism. The R. bili strain mainly metabolized resistant starches to form formate, lactate and acetate. R. gauvreauii mainly metabolized sugar alcohols, including inositol and also utilized formate to generate acetate employing the Wood Ljungdahl pathway. Amino acid and vitamin biosynthesis genomic profiles also differed markedly between the two isolates, likely contributing to their synergistic interactions, as revealed by transcriptomic analysis of cocultures. Transcriptome analysis also revealed that R. gauvreauii IPLA60001 is able to grow using the end-products of starch metabolism formed by the R. bili strain such as formate, and potentially other compounds (such as ethanolamine and inositol) possibly provided by the autolytic behavior of R. bili.",

keywords = "syntrophy, survival, cross-feeding, co-cultures, ruminocci, bile resistance, SCFAs, stress conditions",

author = "Natalia Molinero and Elena Conti and Alan Walker and Abelardo Margolles and Sylvia Duncan and Susana Delgado",

note = "This work was funded by MINECO (Spanish Ministry of Economy and Competitiveness) under grant number AGL2013-44761-P, supported by FEDER (The European Regional Development Funds). N.M. was the recipient of an FPI Predoctoral Grant (BES-2014-068736) from MINECO. A.M. thanks the support of CSIC (PIE-201970E019 grant). N.M., A.M., and S.D. from the MicroHealth group would like to thank the grant of the “Plan for Research, Development and Innovation of the Principado de Asturias 2018–2020” (ref. IDI/2018/000236) co-financed by FEDER funds. S.H.D. and A.W.W. acknowledge core funding support for the Rowett Institute from the Scottish Government Rural and Environmental Sciences and Analytical Services (RESAS) as well as the support for E.C. from the Tenovus Charitable trust (Scotland). Donna Henderson from Rowett Institute (University of Aberdeen) is also acknowledged for carrying out the gas chromatography analysis.",

year = "2022",

month = aug,

doi = "10.1128/spectrum.02776-21",

language = "English",

volume = "10",

journal = "Microbiology spectrum",

issn = "2165-0497",

publisher = "American Society for Microbiology",

number = "4",

}

TY - JOUR

T1 - Survival strategies and metabolic interactions between Ruminococcus gauvreauii and Ruminococcoides bili, isolated from human bile

AU - Molinero , Natalia

AU - Conti, Elena

AU - Walker, Alan

AU - Margolles, Abelardo

AU - Duncan, Sylvia

AU - Delgado , Susana

N1 - This work was funded by MINECO (Spanish Ministry of Economy and Competitiveness) under grant number AGL2013-44761-P, supported by FEDER (The European Regional Development Funds). N.M. was the recipient of an FPI Predoctoral Grant (BES-2014-068736) from MINECO. A.M. thanks the support of CSIC (PIE-201970E019 grant). N.M., A.M., and S.D. from the MicroHealth group would like to thank the grant of the “Plan for Research, Development and Innovation of the Principado de Asturias 2018–2020” (ref. IDI/2018/000236) co-financed by FEDER funds. S.H.D. and A.W.W. acknowledge core funding support for the Rowett Institute from the Scottish Government Rural and Environmental Sciences and Analytical Services (RESAS) as well as the support for E.C. from the Tenovus Charitable trust (Scotland). Donna Henderson from Rowett Institute (University of Aberdeen) is also acknowledged for carrying out the gas chromatography analysis.

PY - 2022/8

Y1 - 2022/8

N2 - Little is known about the bacteria that reside in the human gallbladder and the mechanisms that allow them to survive within this harsh environment. Here we describe interactions between two strains from a human bile sample, one Ruminococcus gauvreauii (IPLA60001), belonging to the Lachnospiraceae family, and the other, designated as Ruminococcoides bili (IPLA60002T; DSM 110008) most closely related to Ruminococcus bromii within the family Ruminococcaceae. We provide evidence for bile salt resistance and sporulation for these new strains. Both differed markedly in their carbohydrate metabolism. The R. bili strain mainly metabolized resistant starches to form formate, lactate and acetate. R. gauvreauii mainly metabolized sugar alcohols, including inositol and also utilized formate to generate acetate employing the Wood Ljungdahl pathway. Amino acid and vitamin biosynthesis genomic profiles also differed markedly between the two isolates, likely contributing to their synergistic interactions, as revealed by transcriptomic analysis of cocultures. Transcriptome analysis also revealed that R. gauvreauii IPLA60001 is able to grow using the end-products of starch metabolism formed by the R. bili strain such as formate, and potentially other compounds (such as ethanolamine and inositol) possibly provided by the autolytic behavior of R. bili.

AB - Little is known about the bacteria that reside in the human gallbladder and the mechanisms that allow them to survive within this harsh environment. Here we describe interactions between two strains from a human bile sample, one Ruminococcus gauvreauii (IPLA60001), belonging to the Lachnospiraceae family, and the other, designated as Ruminococcoides bili (IPLA60002T; DSM 110008) most closely related to Ruminococcus bromii within the family Ruminococcaceae. We provide evidence for bile salt resistance and sporulation for these new strains. Both differed markedly in their carbohydrate metabolism. The R. bili strain mainly metabolized resistant starches to form formate, lactate and acetate. R. gauvreauii mainly metabolized sugar alcohols, including inositol and also utilized formate to generate acetate employing the Wood Ljungdahl pathway. Amino acid and vitamin biosynthesis genomic profiles also differed markedly between the two isolates, likely contributing to their synergistic interactions, as revealed by transcriptomic analysis of cocultures. Transcriptome analysis also revealed that R. gauvreauii IPLA60001 is able to grow using the end-products of starch metabolism formed by the R. bili strain such as formate, and potentially other compounds (such as ethanolamine and inositol) possibly provided by the autolytic behavior of R. bili.

KW - syntrophy

KW - survival

KW - cross-feeding

KW - co-cultures

KW - ruminocci

KW - bile resistance

KW - SCFAs

KW - stress conditions

U2 - 10.1128/spectrum.02776-21

DO - 10.1128/spectrum.02776-21

M3 - Article

C2 - 35863028

SN - 2165-0497

VL - 10

JO - Microbiology spectrum

JF - Microbiology spectrum

IS - 4

M1 - e0277621

ER -

Survival strategies and metabolic interactions between Ruminococcus gauvreauii and Ruminococcoides bili, isolated from human bile

Abstract

Bibliographical note

Data Availability Statement

Keywords

Access to Document

Fingerprint

Cite this