Methylome evolution suggests lineage-dependent selection in the gastric pathogen Helicobacter pylori
Abstract The bacterial pathogen Helicobacter pylori, the leading cause of gastric cancer, is genetically highly diverse and harbours a large and variable portfolio of restriction-modification systems. Our understanding of the evolution and function of DNA methylation in bacteria is limited. Here, we...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-08-01
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| Series: | Communications Biology |
| Online Access: | https://doi.org/10.1038/s42003-023-05218-x |
| _version_ | 1797557193673801728 |
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| author | Florent Ailloud Wilhelm Gottschall Sebastian Suerbaum |
| author_facet | Florent Ailloud Wilhelm Gottschall Sebastian Suerbaum |
| author_sort | Florent Ailloud |
| collection | DOAJ |
| description | Abstract The bacterial pathogen Helicobacter pylori, the leading cause of gastric cancer, is genetically highly diverse and harbours a large and variable portfolio of restriction-modification systems. Our understanding of the evolution and function of DNA methylation in bacteria is limited. Here, we performed a comprehensive analysis of the methylome diversity in H. pylori, using a dataset of 541 genomes that included all known phylogeographic populations. The frequency of 96 methyltransferases and the abundance of their cognate recognition sequences were strongly influenced by phylogeographic structure and were inter-correlated, positively or negatively, for 20% of type II methyltransferases. Low density motifs were more likely to be affected by natural selection, as reflected by higher genomic instability and compositional bias. Importantly, direct correlation implied that methylation patterns can be actively enriched by positive selection and suggests that specific sites have important functions in methylation-dependent phenotypes. Finally, we identified lineage-specific selective pressures modulating the contraction and expansion of the motif ACGT, revealing that the genetic load of methylation could be dependent on local ecological factors. Taken together, natural selection may shape both the abundance and distribution of methyltransferases and their specific recognition sequences, likely permitting a fine-tuning of genome-encoded functions not achievable by genetic variation alone. |
| first_indexed | 2024-03-10T17:13:54Z |
| format | Article |
| id | doaj.art-2e86f9df8e554556bf5239307affc551 |
| institution | Directory Open Access Journal |
| issn | 2399-3642 |
| language | English |
| last_indexed | 2024-03-10T17:13:54Z |
| publishDate | 2023-08-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Communications Biology |
| spelling | doaj.art-2e86f9df8e554556bf5239307affc5512023-11-20T10:34:25ZengNature PortfolioCommunications Biology2399-36422023-08-016111310.1038/s42003-023-05218-xMethylome evolution suggests lineage-dependent selection in the gastric pathogen Helicobacter pyloriFlorent Ailloud0Wilhelm Gottschall1Sebastian Suerbaum2Medical Microbiology and Hospital Epidemiology, Max von Pettenkofer Institute, Faculty of Medicine, LMU MunichMedical Microbiology and Hospital Epidemiology, Max von Pettenkofer Institute, Faculty of Medicine, LMU MunichMedical Microbiology and Hospital Epidemiology, Max von Pettenkofer Institute, Faculty of Medicine, LMU MunichAbstract The bacterial pathogen Helicobacter pylori, the leading cause of gastric cancer, is genetically highly diverse and harbours a large and variable portfolio of restriction-modification systems. Our understanding of the evolution and function of DNA methylation in bacteria is limited. Here, we performed a comprehensive analysis of the methylome diversity in H. pylori, using a dataset of 541 genomes that included all known phylogeographic populations. The frequency of 96 methyltransferases and the abundance of their cognate recognition sequences were strongly influenced by phylogeographic structure and were inter-correlated, positively or negatively, for 20% of type II methyltransferases. Low density motifs were more likely to be affected by natural selection, as reflected by higher genomic instability and compositional bias. Importantly, direct correlation implied that methylation patterns can be actively enriched by positive selection and suggests that specific sites have important functions in methylation-dependent phenotypes. Finally, we identified lineage-specific selective pressures modulating the contraction and expansion of the motif ACGT, revealing that the genetic load of methylation could be dependent on local ecological factors. Taken together, natural selection may shape both the abundance and distribution of methyltransferases and their specific recognition sequences, likely permitting a fine-tuning of genome-encoded functions not achievable by genetic variation alone.https://doi.org/10.1038/s42003-023-05218-x |
| spellingShingle | Florent Ailloud Wilhelm Gottschall Sebastian Suerbaum Methylome evolution suggests lineage-dependent selection in the gastric pathogen Helicobacter pylori Communications Biology |
| title | Methylome evolution suggests lineage-dependent selection in the gastric pathogen Helicobacter pylori |
| title_full | Methylome evolution suggests lineage-dependent selection in the gastric pathogen Helicobacter pylori |
| title_fullStr | Methylome evolution suggests lineage-dependent selection in the gastric pathogen Helicobacter pylori |
| title_full_unstemmed | Methylome evolution suggests lineage-dependent selection in the gastric pathogen Helicobacter pylori |
| title_short | Methylome evolution suggests lineage-dependent selection in the gastric pathogen Helicobacter pylori |
| title_sort | methylome evolution suggests lineage dependent selection in the gastric pathogen helicobacter pylori |
| url | https://doi.org/10.1038/s42003-023-05218-x |
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