Exploring short k-mer profiles in cells and mobile elements from Archaea highlights the major influence of both the ecological niche and evolutionary history
Abstract Background K-mer-based methods have greatly advanced in recent years, largely driven by the realization of their biological significance and by the advent of next-generation sequencing. Their speed and their independence from the annotation process are major advantages. Their utility in the...
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doaj-a7e90addb57b47a1992fd79eeb0adba82021-03-21T12:23:33ZengBMCBMC Genomics1471-21642021-03-0122112210.1186/s12864-021-07471-yExploring short k-mer profiles in cells and mobile elements from Archaea highlights the major influence of both the ecological niche and evolutionary historyAriane Bize0Cédric Midoux1Mahendra Mariadassou2Sophie Schbath3Patrick Forterre4Violette Da Cunha5Université Paris-Saclay, INRAE, PROSEUniversité Paris-Saclay, INRAE, PROSEUniversité Paris-Saclay, INRAE, MaIAGEUniversité Paris-Saclay, INRAE, MaIAGEInstitut Pasteur, Unité de Virologie des Archées, Département de MicrobiologieUniversité Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC)Abstract Background K-mer-based methods have greatly advanced in recent years, largely driven by the realization of their biological significance and by the advent of next-generation sequencing. Their speed and their independence from the annotation process are major advantages. Their utility in the study of the mobilome has recently emerged and they seem a priori adapted to the patchy gene distribution and the lack of universal marker genes of viruses and plasmids. To provide a framework for the interpretation of results from k-mer based methods applied to archaea or their mobilome, we analyzed the 5-mer DNA profiles of close to 600 archaeal cells, viruses and plasmids. Archaea is one of the three domains of life. Archaea seem enriched in extremophiles and are associated with a high diversity of viral and plasmid families, many of which are specific to this domain. We explored the dataset structure by multivariate and statistical analyses, seeking to identify the underlying factors. Results For cells, the 5-mer profiles were inconsistent with the phylogeny of archaea. At a finer taxonomic level, the influence of the taxonomy and the environmental constraints on 5-mer profiles was very strong. These two factors were interdependent to a significant extent, and the respective weights of their contributions varied according to the clade. A convergent adaptation was observed for the class Halobacteria, for which a strong 5-mer signature was identified. For mobile elements, coevolution with the host had a clear influence on their 5-mer profile. This enabled us to identify one previously known and one new case of recent host transfer based on the atypical composition of the mobile elements involved. Beyond the effect of coevolution, extrachromosomal elements strikingly retain the specific imprint of their own viral or plasmid taxonomic family in their 5-mer profile. Conclusion This specific imprint confirms that the evolution of extrachromosomal elements is driven by multiple parameters and is not restricted to host adaptation. In addition, we detected only recent host transfer events, suggesting the fast evolution of short k-mer profiles. This calls for caution when using k-mers for host prediction, metagenomic binning or phylogenetic reconstruction.https://doi.org/10.1186/s12864-021-07471-yExtrachromosomal elementVirusPlasmid5-merCodon compositionMultivariate analysis |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Ariane Bize Cédric Midoux Mahendra Mariadassou Sophie Schbath Patrick Forterre Violette Da Cunha |
spellingShingle |
Ariane Bize Cédric Midoux Mahendra Mariadassou Sophie Schbath Patrick Forterre Violette Da Cunha Exploring short k-mer profiles in cells and mobile elements from Archaea highlights the major influence of both the ecological niche and evolutionary history BMC Genomics Extrachromosomal element Virus Plasmid 5-mer Codon composition Multivariate analysis |
author_facet |
Ariane Bize Cédric Midoux Mahendra Mariadassou Sophie Schbath Patrick Forterre Violette Da Cunha |
author_sort |
Ariane Bize |
title |
Exploring short k-mer profiles in cells and mobile elements from Archaea highlights the major influence of both the ecological niche and evolutionary history |
title_short |
Exploring short k-mer profiles in cells and mobile elements from Archaea highlights the major influence of both the ecological niche and evolutionary history |
title_full |
Exploring short k-mer profiles in cells and mobile elements from Archaea highlights the major influence of both the ecological niche and evolutionary history |
title_fullStr |
Exploring short k-mer profiles in cells and mobile elements from Archaea highlights the major influence of both the ecological niche and evolutionary history |
title_full_unstemmed |
Exploring short k-mer profiles in cells and mobile elements from Archaea highlights the major influence of both the ecological niche and evolutionary history |
title_sort |
exploring short k-mer profiles in cells and mobile elements from archaea highlights the major influence of both the ecological niche and evolutionary history |
publisher |
BMC |
series |
BMC Genomics |
issn |
1471-2164 |
publishDate |
2021-03-01 |
description |
Abstract Background K-mer-based methods have greatly advanced in recent years, largely driven by the realization of their biological significance and by the advent of next-generation sequencing. Their speed and their independence from the annotation process are major advantages. Their utility in the study of the mobilome has recently emerged and they seem a priori adapted to the patchy gene distribution and the lack of universal marker genes of viruses and plasmids. To provide a framework for the interpretation of results from k-mer based methods applied to archaea or their mobilome, we analyzed the 5-mer DNA profiles of close to 600 archaeal cells, viruses and plasmids. Archaea is one of the three domains of life. Archaea seem enriched in extremophiles and are associated with a high diversity of viral and plasmid families, many of which are specific to this domain. We explored the dataset structure by multivariate and statistical analyses, seeking to identify the underlying factors. Results For cells, the 5-mer profiles were inconsistent with the phylogeny of archaea. At a finer taxonomic level, the influence of the taxonomy and the environmental constraints on 5-mer profiles was very strong. These two factors were interdependent to a significant extent, and the respective weights of their contributions varied according to the clade. A convergent adaptation was observed for the class Halobacteria, for which a strong 5-mer signature was identified. For mobile elements, coevolution with the host had a clear influence on their 5-mer profile. This enabled us to identify one previously known and one new case of recent host transfer based on the atypical composition of the mobile elements involved. Beyond the effect of coevolution, extrachromosomal elements strikingly retain the specific imprint of their own viral or plasmid taxonomic family in their 5-mer profile. Conclusion This specific imprint confirms that the evolution of extrachromosomal elements is driven by multiple parameters and is not restricted to host adaptation. In addition, we detected only recent host transfer events, suggesting the fast evolution of short k-mer profiles. This calls for caution when using k-mers for host prediction, metagenomic binning or phylogenetic reconstruction. |
topic |
Extrachromosomal element Virus Plasmid 5-mer Codon composition Multivariate analysis |
url |
https://doi.org/10.1186/s12864-021-07471-y |
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