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Disentangling the impact of environmental and phylogenetic constraints on prokaryotic within-species diversity

Microbial organisms inhabit virtually all environments and encompass a vast biological diversity. The pangenome concept aims to facilitate an understanding of diversity within defined phylogenetic groups. Hence, pangenomes are increasingly used to characterize the strain diversity of prokaryotic spe...

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Autores principales: Maistrenko, Oleksandr M., Mende, Daniel R., Luetge, Mechthild, Hildebrand, Falk, Schmidt, Thomas S. B., Li, Simone S., Rodrigues, João F. Matias, von Mering, Christian, Pedro Coelho, Luis, Huerta-Cepas, Jaime, Sunagawa, Shinichi, Bork, Peer
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7174425/
https://www.ncbi.nlm.nih.gov/pubmed/32047279
http://dx.doi.org/10.1038/s41396-020-0600-z
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author Maistrenko, Oleksandr M.
Mende, Daniel R.
Luetge, Mechthild
Hildebrand, Falk
Schmidt, Thomas S. B.
Li, Simone S.
Rodrigues, João F. Matias
von Mering, Christian
Pedro Coelho, Luis
Huerta-Cepas, Jaime
Sunagawa, Shinichi
Bork, Peer
author_facet Maistrenko, Oleksandr M.
Mende, Daniel R.
Luetge, Mechthild
Hildebrand, Falk
Schmidt, Thomas S. B.
Li, Simone S.
Rodrigues, João F. Matias
von Mering, Christian
Pedro Coelho, Luis
Huerta-Cepas, Jaime
Sunagawa, Shinichi
Bork, Peer
author_sort Maistrenko, Oleksandr M.
collection PubMed
description Microbial organisms inhabit virtually all environments and encompass a vast biological diversity. The pangenome concept aims to facilitate an understanding of diversity within defined phylogenetic groups. Hence, pangenomes are increasingly used to characterize the strain diversity of prokaryotic species. To understand the interdependence of pangenome features (such as the number of core and accessory genes) and to study the impact of environmental and phylogenetic constraints on the evolution of conspecific strains, we computed pangenomes for 155 phylogenetically diverse species (from ten phyla) using 7,000 high-quality genomes to each of which the respective habitats were assigned. Species habitat ubiquity was associated with several pangenome features. In particular, core-genome size was more important for ubiquity than accessory genome size. In general, environmental preferences had a stronger impact on pangenome evolution than phylogenetic inertia. Environmental preferences explained up to 49% of the variance for pangenome features, compared with 18% by phylogenetic inertia. This observation was robust when the dataset was extended to 10,100 species (59 phyla). The importance of environmental preferences was further accentuated by convergent evolution of pangenome features in a given habitat type across different phylogenetic clades. For example, the soil environment promotes expansion of pangenome size, while host-associated habitats lead to its reduction. Taken together, we explored the global principles of pangenome evolution, quantified the influence of habitat, and phylogenetic inertia on the evolution of pangenomes and identified criteria governing species ubiquity and habitat specificity.
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spelling pubmed-71744252020-04-27 Disentangling the impact of environmental and phylogenetic constraints on prokaryotic within-species diversity Maistrenko, Oleksandr M. Mende, Daniel R. Luetge, Mechthild Hildebrand, Falk Schmidt, Thomas S. B. Li, Simone S. Rodrigues, João F. Matias von Mering, Christian Pedro Coelho, Luis Huerta-Cepas, Jaime Sunagawa, Shinichi Bork, Peer ISME J Article Microbial organisms inhabit virtually all environments and encompass a vast biological diversity. The pangenome concept aims to facilitate an understanding of diversity within defined phylogenetic groups. Hence, pangenomes are increasingly used to characterize the strain diversity of prokaryotic species. To understand the interdependence of pangenome features (such as the number of core and accessory genes) and to study the impact of environmental and phylogenetic constraints on the evolution of conspecific strains, we computed pangenomes for 155 phylogenetically diverse species (from ten phyla) using 7,000 high-quality genomes to each of which the respective habitats were assigned. Species habitat ubiquity was associated with several pangenome features. In particular, core-genome size was more important for ubiquity than accessory genome size. In general, environmental preferences had a stronger impact on pangenome evolution than phylogenetic inertia. Environmental preferences explained up to 49% of the variance for pangenome features, compared with 18% by phylogenetic inertia. This observation was robust when the dataset was extended to 10,100 species (59 phyla). The importance of environmental preferences was further accentuated by convergent evolution of pangenome features in a given habitat type across different phylogenetic clades. For example, the soil environment promotes expansion of pangenome size, while host-associated habitats lead to its reduction. Taken together, we explored the global principles of pangenome evolution, quantified the influence of habitat, and phylogenetic inertia on the evolution of pangenomes and identified criteria governing species ubiquity and habitat specificity. Nature Publishing Group UK 2020-02-11 2020-05 /pmc/articles/PMC7174425/ /pubmed/32047279 http://dx.doi.org/10.1038/s41396-020-0600-z Text en © 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Maistrenko, Oleksandr M.
Mende, Daniel R.
Luetge, Mechthild
Hildebrand, Falk
Schmidt, Thomas S. B.
Li, Simone S.
Rodrigues, João F. Matias
von Mering, Christian
Pedro Coelho, Luis
Huerta-Cepas, Jaime
Sunagawa, Shinichi
Bork, Peer
Disentangling the impact of environmental and phylogenetic constraints on prokaryotic within-species diversity
title Disentangling the impact of environmental and phylogenetic constraints on prokaryotic within-species diversity
title_full Disentangling the impact of environmental and phylogenetic constraints on prokaryotic within-species diversity
title_fullStr Disentangling the impact of environmental and phylogenetic constraints on prokaryotic within-species diversity
title_full_unstemmed Disentangling the impact of environmental and phylogenetic constraints on prokaryotic within-species diversity
title_short Disentangling the impact of environmental and phylogenetic constraints on prokaryotic within-species diversity
title_sort disentangling the impact of environmental and phylogenetic constraints on prokaryotic within-species diversity
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7174425/
https://www.ncbi.nlm.nih.gov/pubmed/32047279
http://dx.doi.org/10.1038/s41396-020-0600-z
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