January 28, 2022
Journal Article

Basin-scale biogeography of marine phytoplankton reflects cellular-scale optimization of metabolism and physiology


Extensive microdiversity within the cyanobacterial genus Prochlorococcus, the most abundant photosynthetic organism on earth, has been observed at scales from a single droplet of seawater to ocean basins. Large-scale patterns of ecotypes are apparent and relate to environmental gradients. To interpret the structuring role of variations in genetic potential, as well as metabolic and physiological acclimation, we developed a mechanistic constraint-based modeling framework which incorporates the full suite of genes, proteins, metabolic reactions, pigments, and biochemical compositions of 69 sequenced isolates spanning the Prochlorococcus pangenome. Each in silico strain acclimates to its local environment by maximizing growth rate through adjustment of its metabolic pathways and fluxes, as well as allocation to membrane transporters, pigments, and macromolecules. Optimizing each strain to the local, observed physical and chemical environment along a transect in the Atlantic Ocean, we predicted strain-specific, basin-scale patterns of growth rate, metabolic configuration, and physiological state. Predicted growth rates co-varied with observed ecotype abundances, affirming their significance as a measure of fitness and inferring a non-linear density dependence of mortality. At the ecotype level, patterns of fitness with depth and latitude could be directly traced to adaptations to light, nutrients and temperature. At the strain level, even close phylogenetic relatives varied in their fitness, defining subtle niche sub-spaces directly attributable to differences in their encoded metabolic potential. Physiological and metabolic flexibility and acclimation significantly enhanced fitness and broadened niche-width around the adapted, strain-specific optimal environment. Our study demonstrates the potential to interpret and relate global-scale ecosystem organization in terms of cellular and genome-scale processes.

Published: January 28, 2022


Casey J.R., R.M. Boiteau, M.K. Engqvist, Z. Finkel, G. Li, J. Liefer, and C.L. Mueller, et al. 2022. Basin-scale biogeography of marine phytoplankton reflects cellular-scale optimization of metabolism and physiology. Science Advances 8, no. 3:Art. No. eabl4930. PNNL-SA-169821. doi:10.1126/sciadv.abl4930