Recognition cascade and metabolite transfer in a marine bacteria-phytoplankton model system

Bryndan P. Durham, Stephen P. Dearth, Shalabh Sharma, Shady Amin, Christa B. Smith, Shawn R. Campagna, E. Virginia Armbrust, Mary Ann Moran

    Research output: Contribution to journalArticle

    Abstract

    The trophic linkage between marine bacteria and phytoplankton in the surface ocean is a key step in the global carbon cycle, with almost half of marine primary production transformed by heterotrophic bacterioplankton within hours to weeks of fixation. Early studies conceptualized this link as the passive addition and removal of organic compounds from a shared seawater reservoir. Here, we analysed transcript and intracellular metabolite patterns in a two-member model system and found that the presence of a heterotrophic bacterium induced a potential recognition cascade in a marine phytoplankton species that parallels better-understood vascular plant response systems. Bacterium Ruegeria pomeroyi DSS-3 triggered differential expression of >80 genes in diatom Thalassiosira pseudonana CCMP1335 that are homologs to those used by plants to recognize external stimuli, including proteins putatively involved in leucine-rich repeat recognition activity, second messenger production and protein kinase cascades. Co-cultured diatoms also downregulated lipid biosynthesis genes and upregulated chitin metabolism genes. From differential expression of bacterial transporter systems, we hypothesize that nine diatom metabolites supported the majority of bacterial growth, among them sulfonates, sugar derivatives and organic nitrogen compounds. Similar recognition responses and metabolic linkages as observed in this model system may influence carbon transformations by ocean plankton.

    Original languageEnglish (US)
    Pages (from-to)3500-3513
    Number of pages14
    JournalEnvironmental Microbiology
    Volume19
    Issue number9
    DOIs
    StatePublished - Sep 1 2017

    Fingerprint

    Diatoms
    Phytoplankton
    Bacillariophyceae
    metabolite
    diatom
    phytoplankton
    metabolites
    Bacteria
    Oceans and Seas
    bacterium
    linkage (genetics)
    gene
    bacteria
    Ruegeria
    organic nitrogen compounds
    oceans
    organic nitrogen compound
    Plankton
    Genes
    Nitrogen Compounds

    ASJC Scopus subject areas

    • Microbiology
    • Ecology, Evolution, Behavior and Systematics

    Cite this

    Durham, B. P., Dearth, S. P., Sharma, S., Amin, S., Smith, C. B., Campagna, S. R., ... Moran, M. A. (2017). Recognition cascade and metabolite transfer in a marine bacteria-phytoplankton model system. Environmental Microbiology, 19(9), 3500-3513. https://doi.org/10.1111/1462-2920.13834

    Recognition cascade and metabolite transfer in a marine bacteria-phytoplankton model system. / Durham, Bryndan P.; Dearth, Stephen P.; Sharma, Shalabh; Amin, Shady; Smith, Christa B.; Campagna, Shawn R.; Armbrust, E. Virginia; Moran, Mary Ann.

    In: Environmental Microbiology, Vol. 19, No. 9, 01.09.2017, p. 3500-3513.

    Research output: Contribution to journalArticle

    Durham, BP, Dearth, SP, Sharma, S, Amin, S, Smith, CB, Campagna, SR, Armbrust, EV & Moran, MA 2017, 'Recognition cascade and metabolite transfer in a marine bacteria-phytoplankton model system', Environmental Microbiology, vol. 19, no. 9, pp. 3500-3513. https://doi.org/10.1111/1462-2920.13834
    Durham, Bryndan P. ; Dearth, Stephen P. ; Sharma, Shalabh ; Amin, Shady ; Smith, Christa B. ; Campagna, Shawn R. ; Armbrust, E. Virginia ; Moran, Mary Ann. / Recognition cascade and metabolite transfer in a marine bacteria-phytoplankton model system. In: Environmental Microbiology. 2017 ; Vol. 19, No. 9. pp. 3500-3513.
    @article{41f89063a6b244e082a5457a9104acfe,
    title = "Recognition cascade and metabolite transfer in a marine bacteria-phytoplankton model system",
    abstract = "The trophic linkage between marine bacteria and phytoplankton in the surface ocean is a key step in the global carbon cycle, with almost half of marine primary production transformed by heterotrophic bacterioplankton within hours to weeks of fixation. Early studies conceptualized this link as the passive addition and removal of organic compounds from a shared seawater reservoir. Here, we analysed transcript and intracellular metabolite patterns in a two-member model system and found that the presence of a heterotrophic bacterium induced a potential recognition cascade in a marine phytoplankton species that parallels better-understood vascular plant response systems. Bacterium Ruegeria pomeroyi DSS-3 triggered differential expression of >80 genes in diatom Thalassiosira pseudonana CCMP1335 that are homologs to those used by plants to recognize external stimuli, including proteins putatively involved in leucine-rich repeat recognition activity, second messenger production and protein kinase cascades. Co-cultured diatoms also downregulated lipid biosynthesis genes and upregulated chitin metabolism genes. From differential expression of bacterial transporter systems, we hypothesize that nine diatom metabolites supported the majority of bacterial growth, among them sulfonates, sugar derivatives and organic nitrogen compounds. Similar recognition responses and metabolic linkages as observed in this model system may influence carbon transformations by ocean plankton.",
    author = "Durham, {Bryndan P.} and Dearth, {Stephen P.} and Shalabh Sharma and Shady Amin and Smith, {Christa B.} and Campagna, {Shawn R.} and Armbrust, {E. Virginia} and Moran, {Mary Ann}",
    year = "2017",
    month = "9",
    day = "1",
    doi = "10.1111/1462-2920.13834",
    language = "English (US)",
    volume = "19",
    pages = "3500--3513",
    journal = "Environmental Microbiology",
    issn = "1462-2912",
    publisher = "Wiley-Blackwell",
    number = "9",

    }

    TY - JOUR

    T1 - Recognition cascade and metabolite transfer in a marine bacteria-phytoplankton model system

    AU - Durham, Bryndan P.

    AU - Dearth, Stephen P.

    AU - Sharma, Shalabh

    AU - Amin, Shady

    AU - Smith, Christa B.

    AU - Campagna, Shawn R.

    AU - Armbrust, E. Virginia

    AU - Moran, Mary Ann

    PY - 2017/9/1

    Y1 - 2017/9/1

    N2 - The trophic linkage between marine bacteria and phytoplankton in the surface ocean is a key step in the global carbon cycle, with almost half of marine primary production transformed by heterotrophic bacterioplankton within hours to weeks of fixation. Early studies conceptualized this link as the passive addition and removal of organic compounds from a shared seawater reservoir. Here, we analysed transcript and intracellular metabolite patterns in a two-member model system and found that the presence of a heterotrophic bacterium induced a potential recognition cascade in a marine phytoplankton species that parallels better-understood vascular plant response systems. Bacterium Ruegeria pomeroyi DSS-3 triggered differential expression of >80 genes in diatom Thalassiosira pseudonana CCMP1335 that are homologs to those used by plants to recognize external stimuli, including proteins putatively involved in leucine-rich repeat recognition activity, second messenger production and protein kinase cascades. Co-cultured diatoms also downregulated lipid biosynthesis genes and upregulated chitin metabolism genes. From differential expression of bacterial transporter systems, we hypothesize that nine diatom metabolites supported the majority of bacterial growth, among them sulfonates, sugar derivatives and organic nitrogen compounds. Similar recognition responses and metabolic linkages as observed in this model system may influence carbon transformations by ocean plankton.

    AB - The trophic linkage between marine bacteria and phytoplankton in the surface ocean is a key step in the global carbon cycle, with almost half of marine primary production transformed by heterotrophic bacterioplankton within hours to weeks of fixation. Early studies conceptualized this link as the passive addition and removal of organic compounds from a shared seawater reservoir. Here, we analysed transcript and intracellular metabolite patterns in a two-member model system and found that the presence of a heterotrophic bacterium induced a potential recognition cascade in a marine phytoplankton species that parallels better-understood vascular plant response systems. Bacterium Ruegeria pomeroyi DSS-3 triggered differential expression of >80 genes in diatom Thalassiosira pseudonana CCMP1335 that are homologs to those used by plants to recognize external stimuli, including proteins putatively involved in leucine-rich repeat recognition activity, second messenger production and protein kinase cascades. Co-cultured diatoms also downregulated lipid biosynthesis genes and upregulated chitin metabolism genes. From differential expression of bacterial transporter systems, we hypothesize that nine diatom metabolites supported the majority of bacterial growth, among them sulfonates, sugar derivatives and organic nitrogen compounds. Similar recognition responses and metabolic linkages as observed in this model system may influence carbon transformations by ocean plankton.

    UR - http://www.scopus.com/inward/record.url?scp=85029353945&partnerID=8YFLogxK

    UR - http://www.scopus.com/inward/citedby.url?scp=85029353945&partnerID=8YFLogxK

    U2 - 10.1111/1462-2920.13834

    DO - 10.1111/1462-2920.13834

    M3 - Article

    VL - 19

    SP - 3500

    EP - 3513

    JO - Environmental Microbiology

    JF - Environmental Microbiology

    SN - 1462-2912

    IS - 9

    ER -