Analysis of 1321 Eubacterium rectale genomes from metagenomes uncovers complex phylogeographic population structure and subspecies functional adaptations

Nicolai Karcher; Edoardo Pasolli; Francesco Asnicar; Kun D. Huang; Adrian Tett; Serena Manara; Federica Armanini; Debbie Bain; Sylvia H. Duncan; Petra Louis; Moreno Zolfo; Paolo Manghi; Mireia Valles-Colomer; Roberta Raffaetà; Omar Rota-Stabelli; Maria Carmen Collado; Georg Zeller; Daniel Falush; Frank Maixner; Alan W. Walker; Curtis Huttenhower; Nicola Segata

doi:10.1186/s13059-020-02042-y

Analysis of 1321 Eubacterium rectale genomes from metagenomes uncovers complex phylogeographic population structure and subspecies functional adaptations

Nicolai Karcher, Edoardo Pasolli, Francesco Asnicar, Kun D. Huang, Adrian Tett, Serena Manara, Federica Armanini, Debbie Bain, Sylvia H. Duncan, Petra Louis, Moreno Zolfo, Paolo Manghi, Mireia Valles-Colomer, Roberta Raffaetà, Omar Rota-Stabelli, Maria Carmen Collado, Georg Zeller, Daniel Falush, Frank Maixner, Alan W. WalkerCurtis Huttenhower, Nicola Segata^* (Corresponding Author)

^*Corresponding author for this work

The Rowett Institute of Nutrition and Health

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

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Abstract

Background
Eubacterium rectale is one of the most prevalent human gut bacteria, but its diversity and population genetics are not well understood because large-scale whole-genome investigations of this microbe have not been carried out.

Results
Here, we leverage metagenomic assembly followed by a reference-based binning strategy to screen over 6500 gut metagenomes spanning geography and lifestyle and reconstruct over 1300 E. rectale high-quality genomes from metagenomes. We extend previous results of biogeographic stratification, identifying a new subspecies predominantly found in African individuals and showing that closely related non-human primates do not harbor E. rectale. Comparison of pairwise genetic and geographic distances between subspecies suggests that isolation by distance and co-dispersal with human populations might have contributed to shaping the contemporary population structure of E. rectale. We confirm that a relatively recently diverged E. rectale subspecies specific to Europe consistently lacks motility operons and that it is immotile in vitro, probably due to ancestral genetic loss. The same subspecies exhibits expansion of its carbohydrate metabolism gene repertoire including the acquisition of a genomic island strongly enriched in glycosyltransferase genes involved in exopolysaccharide synthesis.

Conclusions
Our study provides new insights into the population structure and ecology of E. rectale and shows that shotgun metagenomes can enable population genomics studies of microbiota members at a resolution and scale previously attainable only by extensive isolate sequencing.

Original language	English
Article number	138
Number of pages	27
Journal	Genome Biology
Volume	21
DOIs	https://doi.org/10.1186/s13059-020-02042-y
Publication status	Published - 8 Jun 2020

Bibliographical note

Funding
This work was supported by NIH NHGRI grant R01HG005220, NIDDK grant R24DK110499, NIDDK grant U54DE023798, and CMIT grant 6935956 to C.H., and by the European Research Council (ERC-STG project MetaPG-716575), MIUR “Futuro in Ricerca” RBFR13EWWI_001, the European Union (H2020-SFS-2018-1 project MASTER-818368 and H2020-SC1-BHC project ONCOBIOME-825410), and the National Cancer Institute of the National Institutes of Health (1U01CA230551) to N.S. Further support was provided by the Programma Ricerca Budget prestazioni Eurac 2017 of the Province of Bolzano, Italy to F.M., and by the EU-H2020 (DiMeTrack-707345) to E.P. and N.S. D.B., S.H.D., P.L., A.W.W. and The Rowett Institute received core funding support from the Scottish Government Rural and Environmental Sciences and Analytical Services (SG-RESAS).

Availability of data and materials
All datasets used in this study are publicly available and matched with their respective PMID (Additional file 5). The high-quality E. rectale MAGs in fasta format and a metadata file are available at http://segatalab.cibio.unitn.it/data/Erectale_Karcher_et_al.html and in the following Zenodo repository: https://doi.org/10.5281/zenodo.3763191 [80]. The two new isolate genomes L2–21 and T3BWe13 have been uploaded to NCBI and can be found in RefSeq under the accession numbers GCF_008122485.1 [81] and GCF_008123415.1 [82], respectively.

Keywords

BUTYRATE-PRODUCING BACTERIA
GUT MICROBIOME
ALIGNMENT
TRANSMISSION
CSRA
TOOL

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10.1186/s13059-020-02042-yLicence: CC BY

Karcher_et_al_GenBio_AnalysisOf1321Eubacterium_VoR
© The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
Final published version, 3.7 MBLicence: CC BY

Cite this

Karcher, N., Pasolli, E., Asnicar, F., Huang, K. D., Tett, A., Manara, S., Armanini, F., Bain, D., Duncan, S. H., Louis, P., Zolfo, M., Manghi, P., Valles-Colomer, M., Raffaetà, R., Rota-Stabelli, O., Collado, M. C., Zeller, G., Falush, D., Maixner, F., ... Segata, N. (2020). Analysis of 1321 Eubacterium rectale genomes from metagenomes uncovers complex phylogeographic population structure and subspecies functional adaptations. Genome Biology, 21, Article 138. https://doi.org/10.1186/s13059-020-02042-y

Karcher, N, Pasolli, E, Asnicar, F, Huang, KD, Tett, A, Manara, S, Armanini, F, Bain, D, Duncan, SH , Louis, P, Zolfo, M, Manghi, P, Valles-Colomer, M, Raffaetà, R, Rota-Stabelli, O, Collado, MC, Zeller, G, Falush, D, Maixner, F, Walker, AW, Huttenhower, C & Segata, N 2020, 'Analysis of 1321 Eubacterium rectale genomes from metagenomes uncovers complex phylogeographic population structure and subspecies functional adaptations', Genome Biology, vol. 21, 138. https://doi.org/10.1186/s13059-020-02042-y

@article{665d56e3355f44fe9981519e0cee3fb1,

title = "Analysis of 1321 Eubacterium rectale genomes from metagenomes uncovers complex phylogeographic population structure and subspecies functional adaptations",

abstract = "BackgroundEubacterium rectale is one of the most prevalent human gut bacteria, but its diversity and population genetics are not well understood because large-scale whole-genome investigations of this microbe have not been carried out.ResultsHere, we leverage metagenomic assembly followed by a reference-based binning strategy to screen over 6500 gut metagenomes spanning geography and lifestyle and reconstruct over 1300 E. rectale high-quality genomes from metagenomes. We extend previous results of biogeographic stratification, identifying a new subspecies predominantly found in African individuals and showing that closely related non-human primates do not harbor E. rectale. Comparison of pairwise genetic and geographic distances between subspecies suggests that isolation by distance and co-dispersal with human populations might have contributed to shaping the contemporary population structure of E. rectale. We confirm that a relatively recently diverged E. rectale subspecies specific to Europe consistently lacks motility operons and that it is immotile in vitro, probably due to ancestral genetic loss. The same subspecies exhibits expansion of its carbohydrate metabolism gene repertoire including the acquisition of a genomic island strongly enriched in glycosyltransferase genes involved in exopolysaccharide synthesis.ConclusionsOur study provides new insights into the population structure and ecology of E. rectale and shows that shotgun metagenomes can enable population genomics studies of microbiota members at a resolution and scale previously attainable only by extensive isolate sequencing.",

keywords = "BUTYRATE-PRODUCING BACTERIA, GUT MICROBIOME, ALIGNMENT, TRANSMISSION, CSRA, TOOL",

author = "Nicolai Karcher and Edoardo Pasolli and Francesco Asnicar and Huang, {Kun D.} and Adrian Tett and Serena Manara and Federica Armanini and Debbie Bain and Duncan, {Sylvia H.} and Petra Louis and Moreno Zolfo and Paolo Manghi and Mireia Valles-Colomer and Roberta Raffaet{\`a} and Omar Rota-Stabelli and Collado, {Maria Carmen} and Georg Zeller and Daniel Falush and Frank Maixner and Walker, {Alan W.} and Curtis Huttenhower and Nicola Segata",

note = "Funding This work was supported by NIH NHGRI grant R01HG005220, NIDDK grant R24DK110499, NIDDK grant U54DE023798, and CMIT grant 6935956 to C.H., and by the European Research Council (ERC-STG project MetaPG-716575), MIUR “Futuro in Ricerca” RBFR13EWWI_001, the European Union (H2020-SFS-2018-1 project MASTER-818368 and H2020-SC1-BHC project ONCOBIOME-825410), and the National Cancer Institute of the National Institutes of Health (1U01CA230551) to N.S. Further support was provided by the Programma Ricerca Budget prestazioni Eurac 2017 of the Province of Bolzano, Italy to F.M., and by the EU-H2020 (DiMeTrack-707345) to E.P. and N.S. D.B., S.H.D., P.L., A.W.W. and The Rowett Institute received core funding support from the Scottish Government Rural and Environmental Sciences and Analytical Services (SG-RESAS). Availability of data and materials All datasets used in this study are publicly available and matched with their respective PMID (Additional file 5). The high-quality E. rectale MAGs in fasta format and a metadata file are available at http://segatalab.cibio.unitn.it/data/Erectale_Karcher_et_al.html and in the following Zenodo repository: https://doi.org/10.5281/zenodo.3763191 [80]. The two new isolate genomes L2–21 and T3BWe13 have been uploaded to NCBI and can be found in RefSeq under the accession numbers GCF_008122485.1 [81] and GCF_008123415.1 [82], respectively.",

year = "2020",

month = jun,

day = "8",

doi = "10.1186/s13059-020-02042-y",

language = "English",

volume = "21",

journal = "Genome Biology",

issn = "1474-760X",

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TY - JOUR

T1 - Analysis of 1321 Eubacterium rectale genomes from metagenomes uncovers complex phylogeographic population structure and subspecies functional adaptations

AU - Karcher, Nicolai

AU - Pasolli, Edoardo

AU - Asnicar, Francesco

AU - Huang, Kun D.

AU - Tett, Adrian

AU - Manara, Serena

AU - Armanini, Federica

AU - Bain, Debbie

AU - Duncan, Sylvia H.

AU - Louis, Petra

AU - Zolfo, Moreno

AU - Manghi, Paolo

AU - Valles-Colomer, Mireia

AU - Raffaetà, Roberta

AU - Rota-Stabelli, Omar

AU - Collado, Maria Carmen

AU - Zeller, Georg

AU - Falush, Daniel

AU - Maixner, Frank

AU - Walker, Alan W.

AU - Huttenhower, Curtis

AU - Segata, Nicola

N1 - Funding This work was supported by NIH NHGRI grant R01HG005220, NIDDK grant R24DK110499, NIDDK grant U54DE023798, and CMIT grant 6935956 to C.H., and by the European Research Council (ERC-STG project MetaPG-716575), MIUR “Futuro in Ricerca” RBFR13EWWI_001, the European Union (H2020-SFS-2018-1 project MASTER-818368 and H2020-SC1-BHC project ONCOBIOME-825410), and the National Cancer Institute of the National Institutes of Health (1U01CA230551) to N.S. Further support was provided by the Programma Ricerca Budget prestazioni Eurac 2017 of the Province of Bolzano, Italy to F.M., and by the EU-H2020 (DiMeTrack-707345) to E.P. and N.S. D.B., S.H.D., P.L., A.W.W. and The Rowett Institute received core funding support from the Scottish Government Rural and Environmental Sciences and Analytical Services (SG-RESAS). Availability of data and materials All datasets used in this study are publicly available and matched with their respective PMID (Additional file 5). The high-quality E. rectale MAGs in fasta format and a metadata file are available at http://segatalab.cibio.unitn.it/data/Erectale_Karcher_et_al.html and in the following Zenodo repository: https://doi.org/10.5281/zenodo.3763191 [80]. The two new isolate genomes L2–21 and T3BWe13 have been uploaded to NCBI and can be found in RefSeq under the accession numbers GCF_008122485.1 [81] and GCF_008123415.1 [82], respectively.

PY - 2020/6/8

Y1 - 2020/6/8

N2 - BackgroundEubacterium rectale is one of the most prevalent human gut bacteria, but its diversity and population genetics are not well understood because large-scale whole-genome investigations of this microbe have not been carried out.ResultsHere, we leverage metagenomic assembly followed by a reference-based binning strategy to screen over 6500 gut metagenomes spanning geography and lifestyle and reconstruct over 1300 E. rectale high-quality genomes from metagenomes. We extend previous results of biogeographic stratification, identifying a new subspecies predominantly found in African individuals and showing that closely related non-human primates do not harbor E. rectale. Comparison of pairwise genetic and geographic distances between subspecies suggests that isolation by distance and co-dispersal with human populations might have contributed to shaping the contemporary population structure of E. rectale. We confirm that a relatively recently diverged E. rectale subspecies specific to Europe consistently lacks motility operons and that it is immotile in vitro, probably due to ancestral genetic loss. The same subspecies exhibits expansion of its carbohydrate metabolism gene repertoire including the acquisition of a genomic island strongly enriched in glycosyltransferase genes involved in exopolysaccharide synthesis.ConclusionsOur study provides new insights into the population structure and ecology of E. rectale and shows that shotgun metagenomes can enable population genomics studies of microbiota members at a resolution and scale previously attainable only by extensive isolate sequencing.

AB - BackgroundEubacterium rectale is one of the most prevalent human gut bacteria, but its diversity and population genetics are not well understood because large-scale whole-genome investigations of this microbe have not been carried out.ResultsHere, we leverage metagenomic assembly followed by a reference-based binning strategy to screen over 6500 gut metagenomes spanning geography and lifestyle and reconstruct over 1300 E. rectale high-quality genomes from metagenomes. We extend previous results of biogeographic stratification, identifying a new subspecies predominantly found in African individuals and showing that closely related non-human primates do not harbor E. rectale. Comparison of pairwise genetic and geographic distances between subspecies suggests that isolation by distance and co-dispersal with human populations might have contributed to shaping the contemporary population structure of E. rectale. We confirm that a relatively recently diverged E. rectale subspecies specific to Europe consistently lacks motility operons and that it is immotile in vitro, probably due to ancestral genetic loss. The same subspecies exhibits expansion of its carbohydrate metabolism gene repertoire including the acquisition of a genomic island strongly enriched in glycosyltransferase genes involved in exopolysaccharide synthesis.ConclusionsOur study provides new insights into the population structure and ecology of E. rectale and shows that shotgun metagenomes can enable population genomics studies of microbiota members at a resolution and scale previously attainable only by extensive isolate sequencing.

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KW - GUT MICROBIOME

KW - ALIGNMENT

KW - TRANSMISSION

KW - CSRA

KW - TOOL

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Analysis of 1321 Eubacterium rectale genomes from metagenomes uncovers complex phylogeographic population structure and subspecies functional adaptations

Abstract

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Alan Walker

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Analysis of 1321 Eubacterium rectale genomes from metagenomes uncovers complex phylogeographic population structure and subspecies functional adaptations

Abstract

Bibliographical note

Keywords

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Fingerprint

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Alan Walker

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