Marine DNA methylation patterns are associated with microbial community composition and inform virus-host dynamics
Abstract
Background: DNA methylation in prokaryotes is involved in many different cellular processes including cell cycle regulation and defense against viruses. To date, most prokaryotic methylation systems have been studied in culturable microorganisms, resulting in a limited understanding of DNA methylation from a microbial ecology perspective. Here, we analyze the distribution patterns of several microbial epigenetics marks in the ocean microbiome through genome-centric metagenomics across all domains of life. Results: We reconstructed 15,056 viral, 252 prokaryotic, 56 giant viral, and 6 eukaryotic metagenome-assembled genomes from northwest Pacific Ocean seawater samples using short- and long-read sequencing approaches. These metagenome-derived genomes mostly represented novel taxa, and recruited a majority of reads. Thanks to single-molecule real-time (SMRT) sequencing technology, base modification could also be detected for these genomes. This showed that DNA methylation can readily be detected across dominant oceanic bacterial, archaeal, and viral populations, and microbial epigenetic changes correlate with population differentiation. Furthermore, our genome-wide epigenetic analysis of Pelagibacter suggests that GANTC, a DNA methyltransferase target motif, is related to the cell cycle and is affected by environmental conditions. Yet, the presence of this motif also partitions the phylogeny of the Pelagibacter phages, possibly hinting at a competitive co-evolutionary history and multiple effectsmore »
- Authors:
-
- Chung-Ang Univ. (Korea, Republic of)
- USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Seoul National Univ. (Korea, Republic of)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Research Foundation of Korea (NRF)
- OSTI Identifier:
- 1902679
- Grant/Contract Number:
- AC02-05CH11231; NRF-2014R1A1A2A16055779; NRF-2017R1A2B4008968; NRF-2019R1A2C1090861
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Microbiome
- Additional Journal Information:
- Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 2049-2618
- Publisher:
- BioMed Central
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; ocean microbiome; DNA methylation; metagenome-assembled genome; host-phage; long-read sequencing
Citation Formats
Seong, Hoon Je, Roux, Simon, Hwang, Chung Yeon, and Sul, Woo Jun. Marine DNA methylation patterns are associated with microbial community composition and inform virus-host dynamics. United States: N. p., 2022.
Web. doi:10.1186/s40168-022-01340-w.
Seong, Hoon Je, Roux, Simon, Hwang, Chung Yeon, & Sul, Woo Jun. Marine DNA methylation patterns are associated with microbial community composition and inform virus-host dynamics. United States. https://doi.org/10.1186/s40168-022-01340-w
Seong, Hoon Je, Roux, Simon, Hwang, Chung Yeon, and Sul, Woo Jun. Wed .
"Marine DNA methylation patterns are associated with microbial community composition and inform virus-host dynamics". United States. https://doi.org/10.1186/s40168-022-01340-w. https://www.osti.gov/servlets/purl/1902679.
@article{osti_1902679,
title = {Marine DNA methylation patterns are associated with microbial community composition and inform virus-host dynamics},
author = {Seong, Hoon Je and Roux, Simon and Hwang, Chung Yeon and Sul, Woo Jun},
abstractNote = {Background: DNA methylation in prokaryotes is involved in many different cellular processes including cell cycle regulation and defense against viruses. To date, most prokaryotic methylation systems have been studied in culturable microorganisms, resulting in a limited understanding of DNA methylation from a microbial ecology perspective. Here, we analyze the distribution patterns of several microbial epigenetics marks in the ocean microbiome through genome-centric metagenomics across all domains of life. Results: We reconstructed 15,056 viral, 252 prokaryotic, 56 giant viral, and 6 eukaryotic metagenome-assembled genomes from northwest Pacific Ocean seawater samples using short- and long-read sequencing approaches. These metagenome-derived genomes mostly represented novel taxa, and recruited a majority of reads. Thanks to single-molecule real-time (SMRT) sequencing technology, base modification could also be detected for these genomes. This showed that DNA methylation can readily be detected across dominant oceanic bacterial, archaeal, and viral populations, and microbial epigenetic changes correlate with population differentiation. Furthermore, our genome-wide epigenetic analysis of Pelagibacter suggests that GANTC, a DNA methyltransferase target motif, is related to the cell cycle and is affected by environmental conditions. Yet, the presence of this motif also partitions the phylogeny of the Pelagibacter phages, possibly hinting at a competitive co-evolutionary history and multiple effects of a single methylation mark. Conclusions: Overall, this study elucidates that DNA methylation patterns are associated with ecological changes and virus-host dynamics in the ocean microbiome.},
doi = {10.1186/s40168-022-01340-w},
journal = {Microbiome},
number = 1,
volume = 10,
place = {United States},
year = {Wed Sep 28 00:00:00 EDT 2022},
month = {Wed Sep 28 00:00:00 EDT 2022}
}
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