Physiology and evolution of nitrate acquisition in Prochlorococcus
Prochlorococcus is the numerically dominant phototroph in the oligotrophic subtropical ocean and carries out a significant fraction of marine primary productivity. Although field studies have provided evidence for nitrate uptake by Prochlorococcus, little is known about this trait because axenic cul...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | en_US |
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Nature Publishing Group
2015
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| Online Access: | http://hdl.handle.net/1721.1/97195 https://orcid.org/0000-0003-2795-2418 https://orcid.org/0000-0002-6944-5177 https://orcid.org/0000-0002-2638-823X |
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| author | Kent, Alyssa G. Roache-Johnson, Kathryn H. Ackerman, Marcia Moore, Lisa R. Sher, Daniel Thompson, Luke R. Campbell, Lisa Martiny, Adam C. Berube, Paul M. Biller, Steven Meisel, Joshua Daniel Chisholm, Sallie (Penny) Thompson, Jessica Weidemier Roggensack, Sara |
| author2 | Massachusetts Institute of Technology. Department of Biology |
| author_facet | Massachusetts Institute of Technology. Department of Biology Kent, Alyssa G. Roache-Johnson, Kathryn H. Ackerman, Marcia Moore, Lisa R. Sher, Daniel Thompson, Luke R. Campbell, Lisa Martiny, Adam C. Berube, Paul M. Biller, Steven Meisel, Joshua Daniel Chisholm, Sallie (Penny) Thompson, Jessica Weidemier Roggensack, Sara |
| author_sort | Kent, Alyssa G. |
| collection | MIT |
| description | Prochlorococcus is the numerically dominant phototroph in the oligotrophic subtropical ocean and carries out a significant fraction of marine primary productivity. Although field studies have provided evidence for nitrate uptake by Prochlorococcus, little is known about this trait because axenic cultures capable of growth on nitrate have not been available. Additionally, all previously sequenced genomes lacked the genes necessary for nitrate assimilation. Here we introduce three Prochlorococcus strains capable of growth on nitrate and analyze their physiology and genome architecture. We show that the growth of high-light (HL) adapted strains on nitrate is ~17% slower than their growth on ammonium. By analyzing 41 Prochlorococcus genomes, we find that genes for nitrate assimilation have been gained multiple times during the evolution of this group, and can be found in at least three lineages. In low-light adapted strains, nitrate assimilation genes are located in the same genomic context as in marine Synechococcus. These genes are located elsewhere in HL adapted strains and may often exist as a stable genetic acquisition as suggested by the striking degree of similarity in the order, phylogeny and location of these genes in one HL adapted strain and a consensus assembly of environmental Prochlorococcus metagenome sequences. In another HL adapted strain, nitrate utilization genes may have been independently acquired as indicated by adjacent phage mobility elements; these genes are also duplicated with each copy detected in separate genomic islands. These results provide direct evidence for nitrate utilization by Prochlorococcus and illuminate the complex evolutionary history of this trait. |
| first_indexed | 2024-09-23T10:54:52Z |
| format | Article |
| id | mit-1721.1/97195 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T10:54:52Z |
| publishDate | 2015 |
| publisher | Nature Publishing Group |
| record_format | dspace |
| spelling | mit-1721.1/971952022-09-27T15:54:34Z Physiology and evolution of nitrate acquisition in Prochlorococcus Kent, Alyssa G. Roache-Johnson, Kathryn H. Ackerman, Marcia Moore, Lisa R. Sher, Daniel Thompson, Luke R. Campbell, Lisa Martiny, Adam C. Berube, Paul M. Biller, Steven Meisel, Joshua Daniel Chisholm, Sallie (Penny) Thompson, Jessica Weidemier Roggensack, Sara Massachusetts Institute of Technology. Department of Biology Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Chisholm, Sallie (Penny) Berube, Paul M. Biller, Steven Berta-Thompson, Jessie W. Roggensack, Sara E. Meisel, Joshua Daniel Chisholm, Sallie (Penny) Prochlorococcus is the numerically dominant phototroph in the oligotrophic subtropical ocean and carries out a significant fraction of marine primary productivity. Although field studies have provided evidence for nitrate uptake by Prochlorococcus, little is known about this trait because axenic cultures capable of growth on nitrate have not been available. Additionally, all previously sequenced genomes lacked the genes necessary for nitrate assimilation. Here we introduce three Prochlorococcus strains capable of growth on nitrate and analyze their physiology and genome architecture. We show that the growth of high-light (HL) adapted strains on nitrate is ~17% slower than their growth on ammonium. By analyzing 41 Prochlorococcus genomes, we find that genes for nitrate assimilation have been gained multiple times during the evolution of this group, and can be found in at least three lineages. In low-light adapted strains, nitrate assimilation genes are located in the same genomic context as in marine Synechococcus. These genes are located elsewhere in HL adapted strains and may often exist as a stable genetic acquisition as suggested by the striking degree of similarity in the order, phylogeny and location of these genes in one HL adapted strain and a consensus assembly of environmental Prochlorococcus metagenome sequences. In another HL adapted strain, nitrate utilization genes may have been independently acquired as indicated by adjacent phage mobility elements; these genes are also duplicated with each copy detected in separate genomic islands. These results provide direct evidence for nitrate utilization by Prochlorococcus and illuminate the complex evolutionary history of this trait. Gordon and Betty Moore Foundation (Grant GBMF495) National Science Foundation (U.S.) (Grant OCE-1153588) National Science Foundation (U.S.) (Grant DBI-0424599) 2015-06-05T16:53:19Z 2015-06-05T16:53:19Z 2014-10 2014-09 Article http://purl.org/eprint/type/JournalArticle 1751-7362 1751-7370 http://hdl.handle.net/1721.1/97195 Berube, Paul M, Steven J Biller, Alyssa G Kent, Jessie W Berta-Thompson, Sara E Roggensack, Kathryn H Roache-Johnson, Marcia Ackerman, et al. “Physiology and Evolution of Nitrate Acquisition in Prochlorococcus.” ISME J 9, no. 5 (October 28, 2014): 1195–1207. https://orcid.org/0000-0003-2795-2418 https://orcid.org/0000-0002-6944-5177 https://orcid.org/0000-0002-2638-823X en_US http://dx.doi.org/10.1038/ismej.2014.211 The ISME Journal Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf Nature Publishing Group Anne Graham |
| spellingShingle | Kent, Alyssa G. Roache-Johnson, Kathryn H. Ackerman, Marcia Moore, Lisa R. Sher, Daniel Thompson, Luke R. Campbell, Lisa Martiny, Adam C. Berube, Paul M. Biller, Steven Meisel, Joshua Daniel Chisholm, Sallie (Penny) Thompson, Jessica Weidemier Roggensack, Sara Physiology and evolution of nitrate acquisition in Prochlorococcus |
| title | Physiology and evolution of nitrate acquisition in Prochlorococcus |
| title_full | Physiology and evolution of nitrate acquisition in Prochlorococcus |
| title_fullStr | Physiology and evolution of nitrate acquisition in Prochlorococcus |
| title_full_unstemmed | Physiology and evolution of nitrate acquisition in Prochlorococcus |
| title_short | Physiology and evolution of nitrate acquisition in Prochlorococcus |
| title_sort | physiology and evolution of nitrate acquisition in prochlorococcus |
| url | http://hdl.handle.net/1721.1/97195 https://orcid.org/0000-0003-2795-2418 https://orcid.org/0000-0002-6944-5177 https://orcid.org/0000-0002-2638-823X |
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