Synechococcus nitrogen gene loss in iron-limited ocean regions

Synechococcus are the most abundant cyanobacteria in high latitude regions and are responsible for an estimated 17% of annual marine net primary productivity. Despite their biogeochemical importance, Synechococcus populations have been unevenly sampled across the ocean, with most studies focused on...

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Published in:ISME Communications
Main Authors: Sharpe, Garrett, Zhao, Liang, Meyer, Meredith G., Gong, Weida, Burns, Shannon M., Tagliabue, Allesandro, Buck, Kristen N., Santoro, Alyson E., Graff, Jason R., Marchetti, Adrian, Gifford, Scott
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Language:English
Published: Nature Publishing Group UK 2023
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Online Access:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10545762/
http://www.ncbi.nlm.nih.gov/pubmed/37783796
https://doi.org/10.1038/s43705-023-00314-9
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spelling ftpubmed:oai:pubmedcentral.nih.gov:10545762 2023-11-05T03:45:18+01:00 Synechococcus nitrogen gene loss in iron-limited ocean regions Sharpe, Garrett Zhao, Liang Meyer, Meredith G. Gong, Weida Burns, Shannon M. Tagliabue, Allesandro Buck, Kristen N. Santoro, Alyson E. Graff, Jason R. Marchetti, Adrian Gifford, Scott 2023-10-02 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10545762/ http://www.ncbi.nlm.nih.gov/pubmed/37783796 https://doi.org/10.1038/s43705-023-00314-9 en eng Nature Publishing Group UK http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10545762/ http://www.ncbi.nlm.nih.gov/pubmed/37783796 http://dx.doi.org/10.1038/s43705-023-00314-9 © ISME Publications B.V 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . ISME Commun Article Text 2023 ftpubmed https://doi.org/10.1038/s43705-023-00314-9 2023-10-08T01:02:55Z Synechococcus are the most abundant cyanobacteria in high latitude regions and are responsible for an estimated 17% of annual marine net primary productivity. Despite their biogeochemical importance, Synechococcus populations have been unevenly sampled across the ocean, with most studies focused on low-latitude strains. In particular, the near absence of Synechococcus genomes from high-latitude, High Nutrient Low Chlorophyll (HNLC) regions leaves a gap in our knowledge of picocyanobacterial adaptations to iron limitation and their influence on carbon, nitrogen, and iron cycles. We examined Synechococcus populations from the subarctic North Pacific, a well-characterized HNLC region, with quantitative metagenomics. Assembly with short and long reads produced two near complete Synechococcus metagenome-assembled genomes (MAGs). Quantitative metagenome-derived abundances of these populations matched well with flow cytometry counts, and the Synechococcus MAGs were estimated to comprise >99% of the Synechococcus at Station P. Whereas the Station P Synechococcus MAGs contained multiple genes for adaptation to iron limitation, both genomes lacked genes for uptake and assimilation of nitrate and nitrite, suggesting a dependence on ammonium, urea, and other forms of recycled nitrogen leading to reduced iron requirements. A global analysis of Synechococcus nitrate reductase abundance in the TARA Oceans dataset found nitrate assimilation genes are also lower in other HNLC regions. We propose that nitrate and nitrite assimilation gene loss in Synechococcus may represent an adaptation to severe iron limitation in high-latitude regions where ammonium availability is higher. Our findings have implications for models that quantify the contribution of cyanobacteria to primary production and subsequent carbon export. Text Subarctic PubMed Central (PMC) ISME Communications 3 1
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Article
spellingShingle Article
Sharpe, Garrett
Zhao, Liang
Meyer, Meredith G.
Gong, Weida
Burns, Shannon M.
Tagliabue, Allesandro
Buck, Kristen N.
Santoro, Alyson E.
Graff, Jason R.
Marchetti, Adrian
Gifford, Scott
Synechococcus nitrogen gene loss in iron-limited ocean regions
topic_facet Article
description Synechococcus are the most abundant cyanobacteria in high latitude regions and are responsible for an estimated 17% of annual marine net primary productivity. Despite their biogeochemical importance, Synechococcus populations have been unevenly sampled across the ocean, with most studies focused on low-latitude strains. In particular, the near absence of Synechococcus genomes from high-latitude, High Nutrient Low Chlorophyll (HNLC) regions leaves a gap in our knowledge of picocyanobacterial adaptations to iron limitation and their influence on carbon, nitrogen, and iron cycles. We examined Synechococcus populations from the subarctic North Pacific, a well-characterized HNLC region, with quantitative metagenomics. Assembly with short and long reads produced two near complete Synechococcus metagenome-assembled genomes (MAGs). Quantitative metagenome-derived abundances of these populations matched well with flow cytometry counts, and the Synechococcus MAGs were estimated to comprise >99% of the Synechococcus at Station P. Whereas the Station P Synechococcus MAGs contained multiple genes for adaptation to iron limitation, both genomes lacked genes for uptake and assimilation of nitrate and nitrite, suggesting a dependence on ammonium, urea, and other forms of recycled nitrogen leading to reduced iron requirements. A global analysis of Synechococcus nitrate reductase abundance in the TARA Oceans dataset found nitrate assimilation genes are also lower in other HNLC regions. We propose that nitrate and nitrite assimilation gene loss in Synechococcus may represent an adaptation to severe iron limitation in high-latitude regions where ammonium availability is higher. Our findings have implications for models that quantify the contribution of cyanobacteria to primary production and subsequent carbon export.
format Text
author Sharpe, Garrett
Zhao, Liang
Meyer, Meredith G.
Gong, Weida
Burns, Shannon M.
Tagliabue, Allesandro
Buck, Kristen N.
Santoro, Alyson E.
Graff, Jason R.
Marchetti, Adrian
Gifford, Scott
author_facet Sharpe, Garrett
Zhao, Liang
Meyer, Meredith G.
Gong, Weida
Burns, Shannon M.
Tagliabue, Allesandro
Buck, Kristen N.
Santoro, Alyson E.
Graff, Jason R.
Marchetti, Adrian
Gifford, Scott
author_sort Sharpe, Garrett
title Synechococcus nitrogen gene loss in iron-limited ocean regions
title_short Synechococcus nitrogen gene loss in iron-limited ocean regions
title_full Synechococcus nitrogen gene loss in iron-limited ocean regions
title_fullStr Synechococcus nitrogen gene loss in iron-limited ocean regions
title_full_unstemmed Synechococcus nitrogen gene loss in iron-limited ocean regions
title_sort synechococcus nitrogen gene loss in iron-limited ocean regions
publisher Nature Publishing Group UK
publishDate 2023
url http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10545762/
http://www.ncbi.nlm.nih.gov/pubmed/37783796
https://doi.org/10.1038/s43705-023-00314-9
genre Subarctic
genre_facet Subarctic
op_source ISME Commun
op_relation http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10545762/
http://www.ncbi.nlm.nih.gov/pubmed/37783796
http://dx.doi.org/10.1038/s43705-023-00314-9
op_rights © ISME Publications B.V 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
op_doi https://doi.org/10.1038/s43705-023-00314-9
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