Adaptive Evolution of Phosphorus Metabolism in Prochlorococcus

John R Casey, Adil Mardinoglu, Jens Nielsen, David M. Karl

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Abstract

Inorganic phosphorus is scarce in the eastern Mediterranean Sea, where the high-light-adapted ecotype HLI of the marine picocyanobacterium Prochlorococcus marinus thrives. Physiological and regulatory control of phosphorus acquisition and partitioning has been observed in HLI both in culture and in the field; however, the optimization of phosphorus metabolism and associated gains for its phosphorus-limited-growth (PLG) phenotype have not been studied. Here, we reconstructed a genome-scale metabolic network of the HLI axenic strain MED4 (iJC568), consisting of 568 metabolic genes in relation to 794 reactions involving 680 metabolites distributed in 6 subcellular locations. iJC568 was used to quantify metabolic fluxes under PLG conditions, and we observed a close correspondence between experimental and computed fluxes. We found that MED4 has minimized its dependence on intracellular phosphate, not only through drastic depletion of phosphorus-containing biomass components but also through network-wide reductions in phosphate-reaction participation and the loss of a key enzyme, succinate dehydrogenase. These alterations occur despite the stringency of having relatively few pathway redundancies and an extremely high proportion of essential metabolic genes (47%; defined as the percentage of lethal in silico gene knockouts). These strategies are examples of nutrient-controlled adaptive evolution and confer a dramatic growth rate advantage to MED4 in phosphorus-limited regions. 
Original languageEnglish
Article numbere00065-16
JournalmSystems
Volume1
Issue number6
Number of pages15
ISSN2379-5077
DOIs
Publication statusPublished - 2016

Bibliographical note

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

Keywords

  • Prochlorococcus
  • Evolution of metabolic networks
  • Flux balance analysis
  • Metabolic modeling
  • Phosphorus metabolism
  • Succinate dehydrogenase

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