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Chemical microenvironments and single-cell carbon and nitrogen uptake in field-collected colonies of Trichodesmium under different pCO₂.

ABSTRACT: Gradients of oxygen (O₂) and pH, as well as small-scale fluxes of carbon (C), nitrogen (N) and O₂ were investigated under different partial pressures of carbon dioxide (pCO₂) in field-collected colonies of the marine dinitrogen (N₂)-fixing cyanobacterium Trichodesmium. Microsensor measurements indicated that cells within colonies experienced large fluctuations in O₂, pH and CO₂ concentrations over a day-night cycle. O₂ concentrations varied with light intensity and time of day, yet colonies exposed to light were supersaturated with O₂ (up to ~200%) throughout the light period and anoxia was not detected. Alternating between light and dark conditions caused a variation in pH levels by on average 0.5 units (equivalent to 15?nmol?l^-1 proton concentration). Single-cell analyses of C and N assimilation using secondary ion mass spectrometry (SIMS; large geometry SIMS and nanoscale SIMS) revealed high variability in metabolic activity of single cells and trichomes of Trichodesmium, and indicated transfer of C and N to colony-associated non-photosynthetic bacteria. Neither O₂ fluxes nor C fixation by Trichodesmium were significantly influenced by short-term incubations under different pCO₂ levels, whereas N₂ fixation increased with increasing pCO₂. The large range of metabolic rates observed at the single-cell level may reflect a response by colony-forming microbial populations to highly variable microenvironments.

SUBMITTER: Eichner MJ

PROVIDER: S-EPMC5437350 | biostudies-literature | 2017 Jun

REPOSITORIES: biostudies-literature

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Chemical microenvironments and single-cell carbon and nitrogen uptake in field-collected colonies of Trichodesmium under different pCO2.

Eichner Meri J MJ Klawonn Isabell I Wilson Samuel T ST Littmann Sten S Whitehouse Martin J MJ Church Matthew J MJ Kuypers Marcel Mm MM Karl David M DM Ploug Helle H

The ISME journal 20170411 6

Gradients of oxygen (O2) and pH, as well as small-scale fluxes of carbon (C), nitrogen (N) and O2 were investigated under different partial pressures of carbon dioxide (pCO2) in field-collected colonies of the marine dinitrogen (N2)-fixing cyanobacterium Trichodesmium. Microsensor measurements indicated that cells within colonies experienced large fluctuations in O2, pH and CO2 concentrations over a day-night cycle. O2 ...[more]

PMID: 28398346

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Project description:Filamentous diazotrophic Cyanobacteria of the genus Trichodesmium, often found in colonial form, provide an important source of new nitrogen to tropical and subtropical marine ecosystems. Colonies are composed of several clades of Trichodesmium in association with a diverse community of bacterial and eukaryotic epibionts. We used high-throughput 16S rRNA and nifH gene sequencing, carbon (C) and dinitrogen (N2) fixation assays, and metagenomics to describe the diversity and functional potential of the microbiome associated with Trichodesmium colonies collected from the North Pacific Subtropical Gyre (NPSG). The 16S rRNA and nifH gene sequences from hand-picked colonies were predominantly (>99%) from Trichodesmium Clade I (i.e., T. thiebautii), which is phylogenetically and ecologically distinct from the Clade III IMS101 isolate used in most laboratory studies. The bacterial epibiont communities were dominated by Bacteroidetes, Alphaproteobacteria, and Gammaproteobacteria, including several taxa with a known preference for surface attachment, and were relatively depleted in the unicellular Cyanobacteria and small photoheterotrophic bacteria that dominate NPSG surface waters. Sequencing the nifH gene (encoding a subcomponent of the nitrogenase enzyme) identified non-Trichodesmium diazotrophs that clustered predominantly among the Cluster III nifH sequence-types that includes putative anaerobic diazotrophs. Trichodesmium colonies may represent an important habitat for these Cluster III diazotrophs, which were relatively rare in the surrounding seawater. Sequence analyses of nifH gene transcripts revealed several cyanobacterial groups, including heterocystous Richelia, associated with the colonies. Both the 16S rRNA and nifH datasets indicated strong differences between Trichodesmium epibionts and picoplankton in the surrounding seawater, and also between the epibionts inhabiting Trichodesmium puff and tuft colony morphologies. Metagenomic and 16S rRNA gene sequence analyses suggested that lineages typically associated with a copiotrophic lifestyle comprised a large fraction of colony-associated epibionts, in contrast to the streamlined genomes typical of bacterioplankton in these oligotrophic waters. Additionally, epibiont metagenomes were enriched in specific genes involved in phosphate and iron acquisition and denitrification pathways relative to surface seawater metagenomes. We propose that the unique microbial consortium inhabiting colonies has a significant impact on the biogeochemical functioning of Trichodesmium colonies in pelagic environments.

Dataset Information

Chemical microenvironments and single-cell carbon and nitrogen uptake in field-collected colonies of Trichodesmium under different pCO₂.

Publications

Chemical microenvironments and single-cell carbon and nitrogen uptake in field-collected colonies of Trichodesmium under different pCO<sub>2</sub>.

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