Diel investments in metabolite production and consumption in a model microbial system

Organic carbon transfer between surface ocean photosynthetic and heterotrophic microbes is a central but poorly understood process in the global carbon cycle. In a model community in which diatom extracellular release of organic molecules sustained growth of a co-cultured bacterium, we determined quantitative changes in the diatom endometabolome and the bacterial uptake transcriptome over two diel cycles. Of the nuclear magnetic resonance (NMR) peaks in the diatom endometabolites, 38% had diel patterns with noon or mid-afternoon maxima; the remaining either increased (36%) or decreased (26%) through time. Of the genes in the bacterial uptake transcriptome, 94% had a diel pattern with a noon maximum; the remaining decreased over time (6%). Eight diatom endometabolites identified with high confidence were matched to the bacterial genes mediating their utilization. Modeling of these coupled inventories with only diffusion-based phytoplankton extracellular release could not reproduce all the patterns. Addition of active release mechanisms for physiological balance and bacterial recognition significantly improved model performance. Estimates of phytoplankton extracellular release range from only a few percent to nearly half of annual net primary production. Improved understanding of the factors that influence metabolite release and consumption by surface ocean microbes will better constrain this globally significant carbon flux.

Automated summary

Organic carbon transfer between surface ocean photosynthetic and heterotrophic microbes is a complex process influenced by diurnal cycles, as shown in a model community study revealing changes in diatom endometabolome and bacterial uptake transcriptome. Understanding the factors influencing metabolite release and consumption by surface ocean microbes is crucial for better constraining this globally significant carbon flux. Improved model performance was observed when active release mechanisms were incorporated, suggesting the importance of physiological balance and bacterial recognition in this process.