Genetic diversity in cultured and wild marine cyanomyoviruses reveals phosphorus stress as a strong selective agent

Viruses that infect marine cyanobacteria–cyanophages–often carry genes with orthologs in their cyanobacterial hosts, and the frequency of these genes can vary with habitat. To explore habitat-influenced genomic diversity more deeply, we used the genomes of 28 cultured cyanomyoviruses as references t...

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Main Authors: Kelly, Libusha, Ding, Huiming, Huang, Katherine H., Chisholm, Sallie (Penny), Osburne, Marcia Susan
Other Authors: Massachusetts Institute of Technology. Department of Biology
Format: Article
Language:en_US
Published: Nature Publishing Group 2015
Online Access:http://hdl.handle.net/1721.1/92756
https://orcid.org/0000-0003-1072-6828
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author Kelly, Libusha
Ding, Huiming
Huang, Katherine H.
Chisholm, Sallie (Penny)
Osburne, Marcia Susan
author2 Massachusetts Institute of Technology. Department of Biology
author_facet Massachusetts Institute of Technology. Department of Biology
Kelly, Libusha
Ding, Huiming
Huang, Katherine H.
Chisholm, Sallie (Penny)
Osburne, Marcia Susan
author_sort Kelly, Libusha
collection MIT
description Viruses that infect marine cyanobacteria–cyanophages–often carry genes with orthologs in their cyanobacterial hosts, and the frequency of these genes can vary with habitat. To explore habitat-influenced genomic diversity more deeply, we used the genomes of 28 cultured cyanomyoviruses as references to identify phage genes in three ocean habitats. Only about 6–11% of genes were consistently observed in the wild, revealing high gene-content variability in these populations. Numerous shared phage/host genes differed in relative frequency between environments, including genes related to phosphorous acquisition, photorespiration, photosynthesis and the pentose phosphate pathway, possibly reflecting environmental selection for these genes in cyanomyovirus genomes. The strongest emergent signal was related to phosphorous availability; a higher fraction of genomes from relatively low-phosphorus environments–the Sargasso and Mediterranean Sea–contained host-like phosphorus assimilation genes compared with those from the N. Pacific Gyre. These genes are known to be upregulated when the host is phosphorous starved, a response mediated by pho box motifs in phage genomes that bind a host regulatory protein. Eleven cyanomyoviruses have predicted pho boxes upstream of the phosphate-acquisition genes pstS and phoA; eight of these have a conserved cyanophage-specific gene (PhCOG173) between the pho box and pstS. PhCOG173 is also found upstream of other shared phage/host genes, suggesting a unique regulatory role. Pho boxes are found upstream of high light-inducible (hli) genes in cyanomyoviruses, suggesting that this motif may have a broader role than regulating phosphorous-stress responses in infected hosts or that these hlis are involved in the phosphorous-stress response.
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spelling mit-1721.1/927562022-09-27T19:01:40Z Genetic diversity in cultured and wild marine cyanomyoviruses reveals phosphorus stress as a strong selective agent Kelly, Libusha Ding, Huiming Huang, Katherine H. Chisholm, Sallie (Penny) Osburne, Marcia Susan Massachusetts Institute of Technology. Department of Biology Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Chisholm, Sallie (Penny) Kelly, Libusha Ding, Huiming Huang, Katherine H. Osburne, Marcia Chisholm, Sallie (Penny) Viruses that infect marine cyanobacteria–cyanophages–often carry genes with orthologs in their cyanobacterial hosts, and the frequency of these genes can vary with habitat. To explore habitat-influenced genomic diversity more deeply, we used the genomes of 28 cultured cyanomyoviruses as references to identify phage genes in three ocean habitats. Only about 6–11% of genes were consistently observed in the wild, revealing high gene-content variability in these populations. Numerous shared phage/host genes differed in relative frequency between environments, including genes related to phosphorous acquisition, photorespiration, photosynthesis and the pentose phosphate pathway, possibly reflecting environmental selection for these genes in cyanomyovirus genomes. The strongest emergent signal was related to phosphorous availability; a higher fraction of genomes from relatively low-phosphorus environments–the Sargasso and Mediterranean Sea–contained host-like phosphorus assimilation genes compared with those from the N. Pacific Gyre. These genes are known to be upregulated when the host is phosphorous starved, a response mediated by pho box motifs in phage genomes that bind a host regulatory protein. Eleven cyanomyoviruses have predicted pho boxes upstream of the phosphate-acquisition genes pstS and phoA; eight of these have a conserved cyanophage-specific gene (PhCOG173) between the pho box and pstS. PhCOG173 is also found upstream of other shared phage/host genes, suggesting a unique regulatory role. Pho boxes are found upstream of high light-inducible (hli) genes in cyanomyoviruses, suggesting that this motif may have a broader role than regulating phosphorous-stress responses in infected hosts or that these hlis are involved in the phosphorous-stress response. National Science Foundation (U.S.). Biological Oceanography Section National Science Foundation (U.S.). Center for Microbial Oceanography Research and Education United States. Dept. of Energy. Genomic Science Program Gordon and Betty Moore Foundation 2015-01-09T15:12:46Z 2015-01-09T15:12:46Z 2013-05 2013-02 Article http://purl.org/eprint/type/JournalArticle 1751-7362 1751-7370 http://hdl.handle.net/1721.1/92756 Kelly, Libusha, Huiming Ding, Katherine H Huang, Marcia S Osburne, and Sallie W Chisholm. “Genetic Diversity in Cultured and Wild Marine Cyanomyoviruses Reveals Phosphorus Stress as a Strong Selective Agent.” ISME J 7, no. 9 (May 9, 2013): 1827–1841. https://orcid.org/0000-0003-1072-6828 en_US http://dx.doi.org/10.1038/ismej.2013.58 The ISME Journal Creative Commons Attribution-Noncommercial-Share Alike http://creativecommons.org/licenses/by-nc-sa/4.0/ application/pdf Nature Publishing Group Anne Graham
spellingShingle Kelly, Libusha
Ding, Huiming
Huang, Katherine H.
Chisholm, Sallie (Penny)
Osburne, Marcia Susan
Genetic diversity in cultured and wild marine cyanomyoviruses reveals phosphorus stress as a strong selective agent
title Genetic diversity in cultured and wild marine cyanomyoviruses reveals phosphorus stress as a strong selective agent
title_full Genetic diversity in cultured and wild marine cyanomyoviruses reveals phosphorus stress as a strong selective agent
title_fullStr Genetic diversity in cultured and wild marine cyanomyoviruses reveals phosphorus stress as a strong selective agent
title_full_unstemmed Genetic diversity in cultured and wild marine cyanomyoviruses reveals phosphorus stress as a strong selective agent
title_short Genetic diversity in cultured and wild marine cyanomyoviruses reveals phosphorus stress as a strong selective agent
title_sort genetic diversity in cultured and wild marine cyanomyoviruses reveals phosphorus stress as a strong selective agent
url http://hdl.handle.net/1721.1/92756
https://orcid.org/0000-0003-1072-6828
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