Complex marine microbial communities partition metabolism of scarce resources over the diel cycle

• Published in: Nature ecology & evolution Vol. 6; no. 2; pp. 218 - 229
• Main Authors: Muratore, Daniel, Boysen, Angela K., Harke, Matthew J., Becker, Kevin W., Casey, John R., Coesel, Sacha N., Mende, Daniel R., Wilson, Samuel T., Aylward, Frank O., Eppley, John M., Vislova, Alice, Peng, Shengyun, Rodriguez-Gonzalez, Rogelio A., Beckett, Stephen J., Virginia Armbrust, E., DeLong, Edward F., Karl, David M., White, Angelicque E., Zehr, Jonathan P., Van Mooy, Benjamin A. S., Dyhrman, Sonya T., Ingalls, Anitra E., Weitz, Joshua S.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.02.2022; Nature Publishing Group
• Subjects: 38/91; 631/158/2446/2447; 631/158/855; 82/58; Assimilation; Bacteria; Biological and Physical Anthropology; Biomedical and Life Sciences; Carbon; Carbon fixation; Coexistence; Competition; Cyanobacteria; Cyanobacteria - genetics; Ecology; Eukaryotes; Evolutionary Biology; Genes; Heterotrophic bacteria; Life Sciences; Lipid metabolism; Lipids; Macromolecules; Metabolic pathways; Metabolism; Metabolites; Microbial activity; Microbiota; Microorganisms; Niche overlap; Niches; Nitrogen; Nitrogen - metabolism; Nutrients; Paleontology; Partitioning; Photosynthesis; Plankton; Plankton - genetics; Resource partitioning; Seawater; Transcription; Zoology
• ISSN: 2397-334X; 2397-334X
• DOI: 10.1038/s41559-021-01606-w

Complex assemblages of microbes in the surface ocean are responsible for approximately half of global carbon fixation. The persistence of high taxonomic diversity despite competition for a small suite of relatively homogeneously distributed nutrients, that is, ‘the paradox of the plankton’, represents a long-standing challenge for ecological theory. Here we find evidence consistent with temporal niche partitioning of nitrogen assimilation processes over a diel cycle in the North Pacific Subtropical Gyre. We jointly analysed transcript abundances, lipids and metabolites and discovered that a small number of diel archetypes can explain pervasive periodic dynamics. Metabolic pathway analysis of identified diel signals revealed asynchronous timing in the transcription of nitrogen uptake and assimilation genes among different microbial groups—cyanobacteria, heterotrophic bacteria and eukaryotes. This temporal niche partitioning of nitrogen uptake emerged despite synchronous transcription of photosynthesis and central carbon metabolism genes and associated macromolecular abundances. Temporal niche partitioning may be a mechanism by which microorganisms in the open ocean mitigate competition for scarce resources, supporting community coexistence. By integrating time series analyses of transcripts, lipids and metabolites, the authors show that microorganisms in the open ocean partition scarce resources temporally, with different microbial groups expressing nitrogen uptake and assimilation processes at different points throughout the diel cycle.