Adaptive Evolution of Phosphorus Metabolism in <italic toggle="yes">Prochlorococcus</italic>

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 cultur...

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Autores principales:	John R. Casey, Adil Mardinoglu, Jens Nielsen, David M. Karl
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Prochlorococcus evolution of metabolic networks flux balance analysis metabolic modeling phosphorus metabolism succinate dehydrogenase Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/9aa0b279328c4ad99998bc0c092901c2
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spelling	oai:doaj.org-article:9aa0b279328c4ad99998bc0c092901c22021-12-02T19:48:49ZAdaptive Evolution of Phosphorus Metabolism in <italic toggle="yes">Prochlorococcus</italic>10.1128/mSystems.00065-162379-5077https://doaj.org/article/9aa0b279328c4ad99998bc0c092901c22016-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00065-16https://doaj.org/toc/2379-5077ABSTRACT 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. IMPORTANCE Microbes are known to employ three basic strategies to compete for limiting elemental resources: (i) cell quotas may be adjusted by alterations to cell physiology or by substitution of a more plentiful resource, (ii) stressed cells may synthesize high-affinity transporters, and (iii) cells may access more costly sources from internal stores, by degradation, or by petitioning other microbes. In the case of phosphorus, a limiting resource in vast oceanic regions, the cosmopolitan cyanobacterium Prochlorococcus marinus thrives by adopting all three strategies and a fourth, previously unknown strategy. By generating a detailed model of its metabolism, we found that strain MED4 has evolved a way to reduce its dependence on phosphate by minimizing the number of enzymes involved in phosphate transformations, despite the stringency of nearly half of its metabolic genes being essential for survival. Relieving phosphorus limitation, both physiologically and throughout intermediate metabolism, substantially improves phosphorus-specific growth rates.John R. CaseyAdil MardinogluJens NielsenDavid M. KarlAmerican Society for MicrobiologyarticleProchlorococcusevolution of metabolic networksflux balance analysismetabolic modelingphosphorus metabolismsuccinate dehydrogenaseMicrobiologyQR1-502ENmSystems, Vol 1, Iss 6 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Prochlorococcus evolution of metabolic networks flux balance analysis metabolic modeling phosphorus metabolism succinate dehydrogenase Microbiology QR1-502
spellingShingle	Prochlorococcus evolution of metabolic networks flux balance analysis metabolic modeling phosphorus metabolism succinate dehydrogenase Microbiology QR1-502 John R. Casey Adil Mardinoglu Jens Nielsen David M. Karl Adaptive Evolution of Phosphorus Metabolism in <italic toggle="yes">Prochlorococcus</italic>
description	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. IMPORTANCE Microbes are known to employ three basic strategies to compete for limiting elemental resources: (i) cell quotas may be adjusted by alterations to cell physiology or by substitution of a more plentiful resource, (ii) stressed cells may synthesize high-affinity transporters, and (iii) cells may access more costly sources from internal stores, by degradation, or by petitioning other microbes. In the case of phosphorus, a limiting resource in vast oceanic regions, the cosmopolitan cyanobacterium Prochlorococcus marinus thrives by adopting all three strategies and a fourth, previously unknown strategy. By generating a detailed model of its metabolism, we found that strain MED4 has evolved a way to reduce its dependence on phosphate by minimizing the number of enzymes involved in phosphate transformations, despite the stringency of nearly half of its metabolic genes being essential for survival. Relieving phosphorus limitation, both physiologically and throughout intermediate metabolism, substantially improves phosphorus-specific growth rates.
format	article
author	John R. Casey Adil Mardinoglu Jens Nielsen David M. Karl
author_facet	John R. Casey Adil Mardinoglu Jens Nielsen David M. Karl
author_sort	John R. Casey
title	Adaptive Evolution of Phosphorus Metabolism in <italic toggle="yes">Prochlorococcus</italic>
title_short	Adaptive Evolution of Phosphorus Metabolism in <italic toggle="yes">Prochlorococcus</italic>
title_full	Adaptive Evolution of Phosphorus Metabolism in <italic toggle="yes">Prochlorococcus</italic>
title_fullStr	Adaptive Evolution of Phosphorus Metabolism in <italic toggle="yes">Prochlorococcus</italic>
title_full_unstemmed	Adaptive Evolution of Phosphorus Metabolism in <italic toggle="yes">Prochlorococcus</italic>
title_sort	adaptive evolution of phosphorus metabolism in <italic toggle="yes">prochlorococcus</italic>
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/9aa0b279328c4ad99998bc0c092901c2
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Adaptive Evolution of Phosphorus Metabolism in <italic toggle="yes">Prochlorococcus</italic>

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