title: Unlocking the Constraints of Cyanobacterial Productivity: Acclimations Enabling Ultrafast Growth.
abstract: 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. 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.
  
  
  
  Efficient coupling between photosynthesis and productivity is central to the development of biotechnology based on solar energy. Therefore, understanding the factors constraining maximum rates of carbon processing is necessary to identify regulatory mechanisms and devise strategies to overcome productivity constraints. Here, 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. We have delineated putative biological principles that allow unicellular cyanobacteria to achieve ultrahigh growth rates through photophysiological acclimation and effective management of cellular resource under different growth regimes.
authors.affiliation: Chemical and Biological Signature Science, Pacific Northwest National Laboratory, Richland, Washington, USA Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA The Gene and Linda Voiland School of Chemical Engineering and Bioengineering, Washington State University, Pullman, Washington, USA Hans.Bernstein@pnnl.gov alex.beliaev@pnnl.gov.
authors.forename: Hans C
authors.initials: HC
authors.lastname: Bernstein
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA.
authors.forename: Ryan S
authors.initials: RS
authors.lastname: McClure
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA.
authors.forename: Eric A
authors.initials: EA
authors.lastname: Hill
authors.affiliation: Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, USA.
authors.forename: Lye Meng
authors.initials: LM
authors.lastname: Markillie
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA.
authors.forename: William B
authors.initials: WB
authors.lastname: Chrisler
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA.
authors.forename: Margie F
authors.initials: MF
authors.lastname: Romine
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA.
authors.forename: Jason E
authors.initials: JE
authors.lastname: McDermott
authors.affiliation: Department of Chemistry and Geochemistry, Colorado School of Mines, Golden, Colorado, USA.
authors.forename: Matthew C
authors.initials: MC
authors.lastname: Posewitz
authors.affiliation: Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, Pennsylvania, USA Department of Chemistry and Biochemistry, Montana State University, Bozeman, Montana, USA.
authors.forename: Donald A
authors.initials: DA
authors.lastname: Bryant
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA Department of Biological Sciences, Purdue University, West Lafayette, Indiana, USA.
authors.forename: Allan E
authors.initials: AE
authors.lastname: Konopka
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA.
authors.forename: James K
authors.initials: JK
authors.lastname: Fredrickson
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA Hans.Bernstein@pnnl.gov alex.beliaev@pnnl.gov.
authors.forename: Alexander S
authors.initials: AS
authors.lastname: Beliaev
mesh_terms: D000222:Adaptation, Physiological; D052818:Autotrophic Processes; D002244:Carbon / Q000378:metabolism; D008027:Light; D010084:Oxidation-Reduction; D010788:Photosynthesis; D046940:Synechococcus / Q000166:cytology / Q000254:growth & development / Q000378:metabolism / Q000502:physiology*
chemical_list: D002244:Carbon