Abstract

ABSTRACTHarnessing the metabolic potential of photosynthetic microbes for next-generation biotechnology objectives requires detailed scientific understanding of the physiological constraints and regulatory controls affecting carbon partitioning between biomass, metabolite storage pools, and bioproduct synthesis. We dissected the cellular mechanisms underlying the remarkable physiological robustness of the euryhaline unicellular cyanobacterium Synechococcus sp. strain PCC 7002 (Synechococcus 7002) and identify key mechanisms that allow cyanobacteria to achieve unprecedented photoautotrophic productivities (~2.5-h doubling time). Ultrafast growth of Synechococcus 7002 was supported by high rates of photosynthetic electron transfer and linked to significantly elevated transcription of precursor biosynthesis and protein translation machinery. Notably, no growth or photosynthesis inhibition signatures were observed under any of the tested experimental conditions. Finally, the ultrafast growth in Synechococcus 7002 was also linked to a 300% expansion of average cell volume. We hypothesize that this cellular adaptation is required at high irradiances to support higher cell division rates and reduce deleterious effects, corresponding to high light, through increased carbon and reductant sequestration.

Highlights

  • Harnessing the metabolic potential of photosynthetic microbes for next-generation biotechnology objectives requires detailed scientific understanding of the physiological constraints and regulatory controls affecting carbon partitioning between biomass, metabolite storage pools, and bioproduct synthesis

  • Thin cultures of Synechococcus 7002 and Cyanothece 51142 were grown under turbidostat control to maintain nutrient-replete steady states operating at the maximum specific growth rate obtainable for a given environmental condition [27, 28]

  • The mechanisms by which Synechococcus 7002 mitigates the negative effects of high irradiance that typically inhibit the growth and photosynthesis processes of unicellular cyanobacteria are likely to have broader implications for understanding the metabolic and regulatory underpinnings of photosynthetic growth [2, 3]

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Summary

Introduction

Harnessing the metabolic potential of photosynthetic microbes for next-generation biotechnology objectives requires detailed scientific understanding of the physiological constraints and regulatory controls affecting carbon partitioning between biomass, metabolite storage pools, and bioproduct synthesis. Strain PCC 7002 (Synechococcus 7002) and identify key mechanisms that allow cyanobacteria to achieve unprecedented photoautotrophic productivities (~2.5-h doubling time). The ultrafast growth in Synechococcus 7002 was linked to a 300% expansion of average cell volume We hypothesize that this cellular adaptation is required at high irradiances to support higher cell division rates and reduce deleterious effects, corresponding to high light, through increased carbon and reductant sequestration. We interrogate the molecular mechanisms that operate at a systems level to allow cyanobacteria to achieve ultrafast growth This was done by considering growth and photosynthetic kinetics with global transcription patterns. Through integration of state-of-the-art cultivation with photophysiological kinetic analyses and transcriptomic measurements, this genome study provides a new level of insight into the mechanisms guiding the energy and resource partitioning in cyanobacteria and sheds light on the phenomenon of ultrafast photoautotrophic growth

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