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Importance of mobile genetic element immunity in numerically abundant Trichodesmium clades
The colony-forming cyanobacteria Trichodesmium spp. are considered one of the most important nitrogen-fixing genera in the warm, low nutrient ocean. Despite this central biogeochemical role, many questions about their evolution, physiology, and trophic interactions remain unanswered. To address thes...
Autores principales: | , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9950141/ https://www.ncbi.nlm.nih.gov/pubmed/36823453 http://dx.doi.org/10.1038/s43705-023-00214-y |
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author | Webb, Eric A. Held, Noelle A. Zhao, Yiming Graham, Elaina D. Conover, Asa E. Semones, Jake Lee, Michael D. Feng, Yuanyuan Fu, Fei-xue Saito, Mak A. Hutchins, David A. |
author_facet | Webb, Eric A. Held, Noelle A. Zhao, Yiming Graham, Elaina D. Conover, Asa E. Semones, Jake Lee, Michael D. Feng, Yuanyuan Fu, Fei-xue Saito, Mak A. Hutchins, David A. |
author_sort | Webb, Eric A. |
collection | PubMed |
description | The colony-forming cyanobacteria Trichodesmium spp. are considered one of the most important nitrogen-fixing genera in the warm, low nutrient ocean. Despite this central biogeochemical role, many questions about their evolution, physiology, and trophic interactions remain unanswered. To address these questions, we describe Trichodesmium pangenomic potential via significantly improved genomic assemblies from two isolates and 15 new >50% complete Trichodesmium metagenome-assembled genomes from hand-picked, Trichodesmium colonies spanning the Atlantic Ocean. Phylogenomics identified ~four N(2) fixing clades of Trichodesmium across the transect, with T. thiebautii dominating the colony-specific reads. Pangenomic analyses showed that all T. thiebautii MAGs are enriched in COG defense mechanisms and encode a vertically inherited Type III-B Clustered Regularly Interspaced Short Palindromic Repeats and associated protein-based immunity system (CRISPR-Cas). Surprisingly, this CRISPR-Cas system was absent in all T. erythraeum genomes, vertically inherited by T. thiebautii, and correlated with increased signatures of horizontal gene transfer. Additionally, the system was expressed in metaproteomic and transcriptomic datasets and CRISPR spacer sequences with 100% identical hits to field-assembled, putative phage genome fragments were identified. While the currently CO(2)-limited T. erythraeum is expected to be a ‘winner’ of anthropogenic climate change, their genomic dearth of known phage resistance mechanisms, compared to T. thiebautii, could put this outcome in question. Thus, the clear demarcation of T. thiebautii maintaining CRISPR-Cas systems, while T. erythraeum does not, identifies Trichodesmium as an ecologically important CRISPR-Cas model system, and highlights the need for more research on phage-Trichodesmium interactions. |
format | Online Article Text |
id | pubmed-9950141 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-99501412023-02-25 Importance of mobile genetic element immunity in numerically abundant Trichodesmium clades Webb, Eric A. Held, Noelle A. Zhao, Yiming Graham, Elaina D. Conover, Asa E. Semones, Jake Lee, Michael D. Feng, Yuanyuan Fu, Fei-xue Saito, Mak A. Hutchins, David A. ISME Commun Article The colony-forming cyanobacteria Trichodesmium spp. are considered one of the most important nitrogen-fixing genera in the warm, low nutrient ocean. Despite this central biogeochemical role, many questions about their evolution, physiology, and trophic interactions remain unanswered. To address these questions, we describe Trichodesmium pangenomic potential via significantly improved genomic assemblies from two isolates and 15 new >50% complete Trichodesmium metagenome-assembled genomes from hand-picked, Trichodesmium colonies spanning the Atlantic Ocean. Phylogenomics identified ~four N(2) fixing clades of Trichodesmium across the transect, with T. thiebautii dominating the colony-specific reads. Pangenomic analyses showed that all T. thiebautii MAGs are enriched in COG defense mechanisms and encode a vertically inherited Type III-B Clustered Regularly Interspaced Short Palindromic Repeats and associated protein-based immunity system (CRISPR-Cas). Surprisingly, this CRISPR-Cas system was absent in all T. erythraeum genomes, vertically inherited by T. thiebautii, and correlated with increased signatures of horizontal gene transfer. Additionally, the system was expressed in metaproteomic and transcriptomic datasets and CRISPR spacer sequences with 100% identical hits to field-assembled, putative phage genome fragments were identified. While the currently CO(2)-limited T. erythraeum is expected to be a ‘winner’ of anthropogenic climate change, their genomic dearth of known phage resistance mechanisms, compared to T. thiebautii, could put this outcome in question. Thus, the clear demarcation of T. thiebautii maintaining CRISPR-Cas systems, while T. erythraeum does not, identifies Trichodesmium as an ecologically important CRISPR-Cas model system, and highlights the need for more research on phage-Trichodesmium interactions. Nature Publishing Group UK 2023-02-23 /pmc/articles/PMC9950141/ /pubmed/36823453 http://dx.doi.org/10.1038/s43705-023-00214-y Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Article Webb, Eric A. Held, Noelle A. Zhao, Yiming Graham, Elaina D. Conover, Asa E. Semones, Jake Lee, Michael D. Feng, Yuanyuan Fu, Fei-xue Saito, Mak A. Hutchins, David A. Importance of mobile genetic element immunity in numerically abundant Trichodesmium clades |
title | Importance of mobile genetic element immunity in numerically abundant Trichodesmium clades |
title_full | Importance of mobile genetic element immunity in numerically abundant Trichodesmium clades |
title_fullStr | Importance of mobile genetic element immunity in numerically abundant Trichodesmium clades |
title_full_unstemmed | Importance of mobile genetic element immunity in numerically abundant Trichodesmium clades |
title_short | Importance of mobile genetic element immunity in numerically abundant Trichodesmium clades |
title_sort | importance of mobile genetic element immunity in numerically abundant trichodesmium clades |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9950141/ https://www.ncbi.nlm.nih.gov/pubmed/36823453 http://dx.doi.org/10.1038/s43705-023-00214-y |
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