Cryptic carbon and sulfur cycling between surface ocean plankton

Bryndan P. Durham, Shalabh Sharma, Haiwei Luo, Christa B. Smith, Shady Amin, Sara J. Bender, Stephen P. Dearth, Benjamin A.S. Van Mooy, Shawn R. Campagna, Elizabeth B. Kujawinski, E. Virginia Armbrust, Mary Ann Moran

    Research output: Contribution to journalArticle

    Abstract

    About half the carbon fixed by phytoplankton in the ocean is taken up and metabolized by marine bacteria, a transfer that is mediated through the seawater dissolved organic carbon (DOC) pool. The chemical complexity of marine DOC, along with a poor understanding of which compounds form the basis of trophic interactions between bacteria and phytoplankton, have impeded efforts to identify key currencies of this carbon cycle link. Here, we used transcriptional patterns in a bacterial-diatom model system based on vitamin B12 auxotrophy as a sensitive assay for metabolite exchange between marine plankton. The most highly up-regulated genes (up to 374-fold) by a marine Roseobacter clade bacterium when cocultured with the diatom Thalassiosira pseudonana were those encoding the transport and catabolism of 2,3- dihydroxypropane-1-sulfonate (DHPS). This compound has no currently recognized role in the marine microbial food web. As the genes for DHPS catabolism have limited distribution among bacterial taxa, T. pseudonana may use this sulfonate for targeted feeding of beneficial associates. Indeed, DHPS was both a major component of the T. pseudonana cytosol and an abundant microbial metabolite in a diatom bloom in the eastern North Pacific Ocean. Moreover, transcript analysis of the North Pacific samples provided evidence of DHPS catabolism by Roseobacter populations. Other such biogeochemically important metabolites may be common in the ocean but difficult to discriminate against the complex chemical background of seawater. Bacterial transformation of this diatom-derived sulfonate represents a previously unidentified and likely sizeable link in both the marine carbon and sulfur cycles.

    Original languageEnglish (US)
    Pages (from-to)453-457
    Number of pages5
    JournalProceedings of the National Academy of Sciences of the United States of America
    Volume112
    Issue number2
    DOIs
    StatePublished - Jan 13 2015

    Fingerprint

    Plankton
    Diatoms
    Sulfur
    Oceans and Seas
    Roseobacter
    Carbon
    Carbon Cycle
    Phytoplankton
    Seawater
    Bacteria
    Bacterial Transformation
    Pacific Ocean
    Food Chain
    Vitamin B 12
    Cytosol
    Genes
    Population

    Keywords

    • Bacteria
    • DHPS
    • Diatoms
    • Sulfonates
    • Vitamin B12

    ASJC Scopus subject areas

    • General

    Cite this

    Cryptic carbon and sulfur cycling between surface ocean plankton. / Durham, Bryndan P.; Sharma, Shalabh; Luo, Haiwei; Smith, Christa B.; Amin, Shady; Bender, Sara J.; Dearth, Stephen P.; Van Mooy, Benjamin A.S.; Campagna, Shawn R.; Kujawinski, Elizabeth B.; Armbrust, E. Virginia; Moran, Mary Ann.

    In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 112, No. 2, 13.01.2015, p. 453-457.

    Research output: Contribution to journalArticle

    Durham, BP, Sharma, S, Luo, H, Smith, CB, Amin, S, Bender, SJ, Dearth, SP, Van Mooy, BAS, Campagna, SR, Kujawinski, EB, Armbrust, EV & Moran, MA 2015, 'Cryptic carbon and sulfur cycling between surface ocean plankton', Proceedings of the National Academy of Sciences of the United States of America, vol. 112, no. 2, pp. 453-457. https://doi.org/10.1073/pnas.1413137112
    Durham, Bryndan P. ; Sharma, Shalabh ; Luo, Haiwei ; Smith, Christa B. ; Amin, Shady ; Bender, Sara J. ; Dearth, Stephen P. ; Van Mooy, Benjamin A.S. ; Campagna, Shawn R. ; Kujawinski, Elizabeth B. ; Armbrust, E. Virginia ; Moran, Mary Ann. / Cryptic carbon and sulfur cycling between surface ocean plankton. In: Proceedings of the National Academy of Sciences of the United States of America. 2015 ; Vol. 112, No. 2. pp. 453-457.
    @article{0c072dcabcde45bbbf3447b4b67391cc,
    title = "Cryptic carbon and sulfur cycling between surface ocean plankton",
    abstract = "About half the carbon fixed by phytoplankton in the ocean is taken up and metabolized by marine bacteria, a transfer that is mediated through the seawater dissolved organic carbon (DOC) pool. The chemical complexity of marine DOC, along with a poor understanding of which compounds form the basis of trophic interactions between bacteria and phytoplankton, have impeded efforts to identify key currencies of this carbon cycle link. Here, we used transcriptional patterns in a bacterial-diatom model system based on vitamin B12 auxotrophy as a sensitive assay for metabolite exchange between marine plankton. The most highly up-regulated genes (up to 374-fold) by a marine Roseobacter clade bacterium when cocultured with the diatom Thalassiosira pseudonana were those encoding the transport and catabolism of 2,3- dihydroxypropane-1-sulfonate (DHPS). This compound has no currently recognized role in the marine microbial food web. As the genes for DHPS catabolism have limited distribution among bacterial taxa, T. pseudonana may use this sulfonate for targeted feeding of beneficial associates. Indeed, DHPS was both a major component of the T. pseudonana cytosol and an abundant microbial metabolite in a diatom bloom in the eastern North Pacific Ocean. Moreover, transcript analysis of the North Pacific samples provided evidence of DHPS catabolism by Roseobacter populations. Other such biogeochemically important metabolites may be common in the ocean but difficult to discriminate against the complex chemical background of seawater. Bacterial transformation of this diatom-derived sulfonate represents a previously unidentified and likely sizeable link in both the marine carbon and sulfur cycles.",
    keywords = "Bacteria, DHPS, Diatoms, Sulfonates, Vitamin B12",
    author = "Durham, {Bryndan P.} and Shalabh Sharma and Haiwei Luo and Smith, {Christa B.} and Shady Amin and Bender, {Sara J.} and Dearth, {Stephen P.} and {Van Mooy}, {Benjamin A.S.} and Campagna, {Shawn R.} and Kujawinski, {Elizabeth B.} and Armbrust, {E. Virginia} and Moran, {Mary Ann}",
    year = "2015",
    month = "1",
    day = "13",
    doi = "10.1073/pnas.1413137112",
    language = "English (US)",
    volume = "112",
    pages = "453--457",
    journal = "Proceedings of the National Academy of Sciences of the United States of America",
    issn = "0027-8424",
    number = "2",

    }

    TY - JOUR

    T1 - Cryptic carbon and sulfur cycling between surface ocean plankton

    AU - Durham, Bryndan P.

    AU - Sharma, Shalabh

    AU - Luo, Haiwei

    AU - Smith, Christa B.

    AU - Amin, Shady

    AU - Bender, Sara J.

    AU - Dearth, Stephen P.

    AU - Van Mooy, Benjamin A.S.

    AU - Campagna, Shawn R.

    AU - Kujawinski, Elizabeth B.

    AU - Armbrust, E. Virginia

    AU - Moran, Mary Ann

    PY - 2015/1/13

    Y1 - 2015/1/13

    N2 - About half the carbon fixed by phytoplankton in the ocean is taken up and metabolized by marine bacteria, a transfer that is mediated through the seawater dissolved organic carbon (DOC) pool. The chemical complexity of marine DOC, along with a poor understanding of which compounds form the basis of trophic interactions between bacteria and phytoplankton, have impeded efforts to identify key currencies of this carbon cycle link. Here, we used transcriptional patterns in a bacterial-diatom model system based on vitamin B12 auxotrophy as a sensitive assay for metabolite exchange between marine plankton. The most highly up-regulated genes (up to 374-fold) by a marine Roseobacter clade bacterium when cocultured with the diatom Thalassiosira pseudonana were those encoding the transport and catabolism of 2,3- dihydroxypropane-1-sulfonate (DHPS). This compound has no currently recognized role in the marine microbial food web. As the genes for DHPS catabolism have limited distribution among bacterial taxa, T. pseudonana may use this sulfonate for targeted feeding of beneficial associates. Indeed, DHPS was both a major component of the T. pseudonana cytosol and an abundant microbial metabolite in a diatom bloom in the eastern North Pacific Ocean. Moreover, transcript analysis of the North Pacific samples provided evidence of DHPS catabolism by Roseobacter populations. Other such biogeochemically important metabolites may be common in the ocean but difficult to discriminate against the complex chemical background of seawater. Bacterial transformation of this diatom-derived sulfonate represents a previously unidentified and likely sizeable link in both the marine carbon and sulfur cycles.

    AB - About half the carbon fixed by phytoplankton in the ocean is taken up and metabolized by marine bacteria, a transfer that is mediated through the seawater dissolved organic carbon (DOC) pool. The chemical complexity of marine DOC, along with a poor understanding of which compounds form the basis of trophic interactions between bacteria and phytoplankton, have impeded efforts to identify key currencies of this carbon cycle link. Here, we used transcriptional patterns in a bacterial-diatom model system based on vitamin B12 auxotrophy as a sensitive assay for metabolite exchange between marine plankton. The most highly up-regulated genes (up to 374-fold) by a marine Roseobacter clade bacterium when cocultured with the diatom Thalassiosira pseudonana were those encoding the transport and catabolism of 2,3- dihydroxypropane-1-sulfonate (DHPS). This compound has no currently recognized role in the marine microbial food web. As the genes for DHPS catabolism have limited distribution among bacterial taxa, T. pseudonana may use this sulfonate for targeted feeding of beneficial associates. Indeed, DHPS was both a major component of the T. pseudonana cytosol and an abundant microbial metabolite in a diatom bloom in the eastern North Pacific Ocean. Moreover, transcript analysis of the North Pacific samples provided evidence of DHPS catabolism by Roseobacter populations. Other such biogeochemically important metabolites may be common in the ocean but difficult to discriminate against the complex chemical background of seawater. Bacterial transformation of this diatom-derived sulfonate represents a previously unidentified and likely sizeable link in both the marine carbon and sulfur cycles.

    KW - Bacteria

    KW - DHPS

    KW - Diatoms

    KW - Sulfonates

    KW - Vitamin B12

    UR - http://www.scopus.com/inward/record.url?scp=84920964214&partnerID=8YFLogxK

    UR - http://www.scopus.com/inward/citedby.url?scp=84920964214&partnerID=8YFLogxK

    U2 - 10.1073/pnas.1413137112

    DO - 10.1073/pnas.1413137112

    M3 - Article

    VL - 112

    SP - 453

    EP - 457

    JO - Proceedings of the National Academy of Sciences of the United States of America

    JF - Proceedings of the National Academy of Sciences of the United States of America

    SN - 0027-8424

    IS - 2

    ER -