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Quantifying the effects of light intensity on bioproduction and maintenance energy during photosynthetic growth of Rhodobacter sphaeroides

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Abstract

Obtaining a better understanding of the physiology and bioenergetics of photosynthetic microbes is an important step toward optimizing these systems for light energy capture or production of valuable commodities. In this work, we analyzed the effect of light intensity on bioproduction, biomass formation, and maintenance energy during photoheterotrophic growth of Rhodobacter sphaeroides. Using data obtained from steady-state bioreactors operated at varying dilution rates and light intensities, we found that irradiance had a significant impact on biomass yield and composition, with significant changes in photopigment, phospholipid, and biopolymer storage contents. We also observed a linear relationship between incident light intensity and H2 production rate between 3 and 10 W m−2, with saturation observed at 100 W m−2. The light conversion efficiency to H2 was also higher at lower light intensities. Photosynthetic maintenance energy requirements were also significantly affected by light intensity, with links to differences in biomass composition and the need to maintain redox homeostasis. Inclusion of the measured condition-dependent biomass and maintenance energy parameters and the measured photon uptake rate into a genome-scale metabolic model for R. sphaeroides (iRsp1140) significantly improved its predictive performance. We discuss how our analyses provide new insights into the light-dependent changes in bioenergetic requirements and physiology during photosynthetic growth of R. sphaeroides and potentially other photosynthetic organisms.

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References

  • Aagaard J, Sistrom WR (1972) Control of synthesis of reaction centre bacteriochlorophyll in photosynthetic bacteria. Photochem Photobiol 15(2):209–225

    Article  CAS  PubMed  Google Scholar 

  • Aiking H, Sojka G (1979) Response of Rhodopseudomonas capsulata to illumination and growth rate in a light-limited continuous culture. J Bacteriol 139(2):530–536

    CAS  PubMed Central  PubMed  Google Scholar 

  • Allen JF (2003) Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci 8(1):15–19

    Article  CAS  PubMed  Google Scholar 

  • Atsumi S, Higashide W, Liao JC (2009) Direct photosynthetic recycling of carbon dioxide to isobutyraldehyde. Nat Biotechnol 27(12):1177–1180

    Article  CAS  PubMed  Google Scholar 

  • Biel AJ (1986) Control of bacteriochlorophyll accumulation by light in Rhodobacter capsulatus. J Bacteriol 168(2):655–659

    CAS  PubMed Central  PubMed  Google Scholar 

  • Campbell TB, Lueking DR (1983) Light-mediated regulation of phospholipid synthesis in Rhodopseudomonas sphaeroides. J Bacteriol 155(2):806–816

    CAS  PubMed Central  PubMed  Google Scholar 

  • Carapezza G, Umeton R, Costanza J, Angione C, Stracquadanio G, Papini A, Lio P, Nicosia G (2013) Efficient behavior of photosynthetic organelles via Pareto optimality, identifiability, and sensitivity analysis. ACS Synth Biol 2(5):274–288

    Article  CAS  PubMed  Google Scholar 

  • Chory J, Kaplan S (1983) Light-dependent regulation of the synthesis of soluble and intracytoplasmic membrane proteins of Rhodopseudomonas sphaeroides. J Bacteriol 153(1):465–474

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cohen-Bazire G, Sistrom WR, Stanier RY (1957) Kinetic studies of pigment synthesis by non-sulfur purple bacteria. J Cell Physiol 49(1):25–68

    Article  CAS  PubMed  Google Scholar 

  • Connor MR, Atsumi S (2010) Synthetic biology guides biofuel production. J Biomed Biotechnol. doi:10.1155/2010/541698

    PubMed Central  PubMed  Google Scholar 

  • Dal’Molin CG, Quek LE, Palfreyman RW, Nielsen LK (2011) AlgaGEM—a genome-scale metabolic reconstruction of algae based on the Chlamydomonas reinhardtii genome. BMC Genom 12(suppl 4):S5

    Article  Google Scholar 

  • Geisser S (1975) The predictive sample reuse method with applications. J Am Stat Assoc 70(350):320–328

    Article  Google Scholar 

  • Golecki JR, Schumacher A, Drews G (1980) The differentiation of the photosynthetic apparatus and the intracytoplasmic membrane in cells of Rhodopseudomonas capsulata upon variation of light intensity. Eur J Cell Biol 23(1):1–5

    CAS  PubMed  Google Scholar 

  • Gronenberg LS, Marcheschi RJ, Liao JC (2013) Next generation biofuel engineering in prokaryotes. Curr Opin Chem Biol 17(3):462–471

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hartree EF (1972) Determination of protein: a modification of the Lowry method that gives a linear photometric response. Anal Biochem 48(2):422–427

    Article  CAS  PubMed  Google Scholar 

  • Imam S, Yilmaz S, Sohmen U, Gorzalski AS, Reed JL, Noguera DR, Donohue TJ (2011) iRsp1095: a genome-scale reconstruction of the Rhodobacter sphaeroides metabolic network. BMC Syst Biol 5:116

    Article  PubMed Central  PubMed  Google Scholar 

  • Imam S, Noguera DR, Donohue TJ (2013) Global insights into energetic and metabolic networks in Rhodobacter sphaeroides. BMC Syst Biol 7(1):89

    Article  PubMed Central  PubMed  Google Scholar 

  • Khatipov E, Miyake M, Miyake J, Asada Y (1998) Polyhydroxybutyrate accumulation and hydrogen evolution by Rhodobacter sphaeroides as a function of nitrogen availability. In: Zaborsky O, Benemann J, Matsunaga T, Miyake J, San Pietro A (eds) BioHydrogen. Springer, US, pp 157–161

  • Kien NB, Kong IS, Lee MG, Kim JK (2010) Coenzyme Q10 production in a 150-l reactor by a mutant strain of Rhodobacter sphaeroides. J Ind Microbiol Biotechnol 37(5):521–529

    Article  CAS  PubMed  Google Scholar 

  • Kiley PJ, Kaplan S (1988) Molecular genetics of photosynthetic membrane biosynthesis in Rhodobacter sphaeroides. Microbiol Rev 52(1):50–69

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kim E, Lee M, Kim M, Lee JK (2008) Molecular hydrogen production by nitrogenase of Rhodobacter sphaeroides and by Fe-only hydrogenase of Rhodospirillum rubrum. Int J Hydrog Energy 33(5):1516–1521

    Article  CAS  Google Scholar 

  • Kliphuis AM, Klok AJ, Martens DE, Lamers PP, Janssen M, Wijffels RH (2011) Metabolic modeling of Chlamydomonas reinhardtii: energy requirements for photoautotrophic growth and maintenance. J Appl Phycol 24(2):253–266

    Article  PubMed Central  PubMed  Google Scholar 

  • Koku H, Eroglu I, Gunduz U, Yucel M, Turker L (2002) Aspects of the metabolism of hydrogen production by Rhodobacter sphaeroides. Int J Hydrogen Energy 27(11–12):1315–1329

    Article  CAS  Google Scholar 

  • Kontur WS, Ziegelhoffer EC, Spero MA, Imam S, Noguera DR, Donohue TJ (2011) Pathways involved in reductant distribution during photobiological H2 production by Rhodobacter sphaeroides. Appl Environ Microbiol 77(20):7425–7429

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kontur WS, Schackwitz WS, Ivanova N, Martin J, Labutti K, Deshpande S, Tice HN, Pennacchio C, Sodergren E, Weinstock GM, Noguera DR, Donohue TJ (2012) Revised sequence and annotation of the Rhodobacter sphaeroides 2.4.1 genome. J Bacteriol 194(24):7016–7017

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lee S, Phalakornkule C, Domach MM, Grossmann IE (2000) Recursive MILP model for finding all the alternate optima in LP models for metabolic networks. Comput Chem Eng 24(2–7):711–716

    Article  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275

    CAS  PubMed  Google Scholar 

  • Mackenzie C, Eraso JM, Choudhary M, Roh JH, Zeng X, Bruscella P, Puskas A, Kaplan S (2007) Postgenomic adventures with Rhodobacter sphaeroides. Annu Rev Microbiol 61:283–307

    Article  CAS  PubMed  Google Scholar 

  • Mahadevan R, Schilling CH (2003) The effects of alternate optimal solutions in constraint-based genome-scale metabolic models. Metab Eng 5(4):264–276

    Article  CAS  PubMed  Google Scholar 

  • Masepohl B, Hallenbeck PC (2010) Nitrogen and molybdenum control of nitrogen fixation in the phototrophic bacterium Rhodobacter capsulatus. Adv Exp Med Biol 675:49–70

    Article  CAS  PubMed  Google Scholar 

  • Miyake J, Kawamur S (1987) Efficiency of light energy conversion to hydrogen by the photosynthetic bacterium Rhodobacter sphaeroides. Int J Hydrogen Energy 12(3):147–149

    Article  CAS  Google Scholar 

  • Montagud A, Navarro E, de Cordoba PF, Urchueguia JF, Patil KR (2010) Reconstruction and analysis of genome-scale metabolic model of a photosynthetic bacterium. BMC Syst Biol 4:156

    Article  PubMed Central  PubMed  Google Scholar 

  • Nogales J, Gudmundsson S, Knight EM, Palsson BO, Thiele I (2012) Detailing the optimality of photosynthesis in cyanobacteria through systems biology analysis. Proc Nat Acad Sci USA 109(7):2678–2683

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Oberhardt MA, Palsson BO, Papin JA (2009) Applications of genome-scale metabolic reconstructions. Mol Syst Biol 5:320

    Article  PubMed Central  PubMed  Google Scholar 

  • Oelze J (1988) Regulation of tetrapyrrole synthesis by light in chemostat cultures of Rhodobacter sphaeroides. J Bacteriol 170(10):4652–4657

    CAS  PubMed Central  PubMed  Google Scholar 

  • Peralta-Yahya PP, Zhang F, del Cardayre SB, Keasling JD (2012) Microbial engineering for the production of advanced biofuels. Nature 488(7411):320–328

    Article  CAS  PubMed  Google Scholar 

  • Reed JL (2012) Shrinking the metabolic solution space using experimental datasets. PLoS Comput Biol 8(8):e1002662

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Reed JL, Palsson BO (2004) Genome-scale in silico models of E. coli have multiple equivalent phenotypic states: assessment of correlated reaction subsets that comprise network states. Genome Res 14(9):1797–1805

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rex R, Bill N, Schmidt-Hohagen K, Schomburg D (2013) Swimming in light: a large-scale computational analysis of the metabolism of Dinoroseobacter shibae. PLoS Comput Biol 9(10):e1003224

    Article  PubMed Central  PubMed  Google Scholar 

  • Rittmann B, McCarty PL (2001) Environmental biotechnology: principles and applications. McGraw-Hill Science Engineering, New York

    Google Scholar 

  • Rouser G, Fkeischer S, Yamamoto A (1970) Two dimensional then layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots. Lipids 5(5):494–496

    Article  CAS  PubMed  Google Scholar 

  • Russell JB, Cook GM (1995) Energetics of bacterial growth: balance of anabolic and catabolic reactions. Microbiol Rev 59(1):48–62

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sasikala K, Ramana VC, Rao RP, Kovacs KL (1993) Anoxygenic phototrophic bacteria: physiology and advances in hydrogen production technology. Adv Appl Microbiol 38:211–295

    Article  CAS  Google Scholar 

  • Schumacher A, Drews G (1979) Effects of light intensity on membrane differentiation in Rhodopseudomonas capsulata. Biochim Biophys Acta 547(3):417–428

    Article  CAS  PubMed  Google Scholar 

  • Sistrom WR (1960) A requirement for sodium in the growth of Rhodopseudomonas spheroides. J Gen Microbiol 22:778–785

    Article  CAS  PubMed  Google Scholar 

  • Stone M (1974) Cross-validatory choice and assessment of statistical predictions. J Royal Stat Soc 36(2):111–147

    Google Scholar 

  • Stouthamer AH, van Verseveld HW (1987) Microbial energetics should be considered in manipulating metabolism for biotechnological purposes. Trends Biotechnol 5(5):149–155

    Article  CAS  Google Scholar 

  • Tannler S, Decasper S, Sauer U (2008) Maintenance metabolism and carbon fluxes in Bacillus species. Microb Cell Fact 7:19

    Article  PubMed Central  PubMed  Google Scholar 

  • Thiele I, Palsson BO (2010) A protocol for generating a high-quality genome-scale metabolic reconstruction. Nat Protoc 5(1):93–121

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Varma A, Palsson BO (1994) Metabolic flux balancing: basic concepts, scientific and practical use. Nat Biotechnol 12:994–998

    Article  CAS  Google Scholar 

  • Vu TT, Stolyar SM, Pinchuk GE, Hill EA, Kucek LA, Brown RN, Lipton MS, Osterman A, Fredrickson JK, Konopka AE, Beliaev AS, Reed JL (2012) Genome-scale modeling of light-driven reductant partitioning and carbon fluxes in diazotrophic unicellular cyanobacterium Cyanothece sp. ATCC 51142. PLoS Comput Biol 8(4):e1002460

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wahlund TM, Conway T, Tabita FR (1996) Bioconversion of CO2 to ethanol and other compounds. American Chemical Society Division of Fuel Chemistry 3:1403–1405

    Google Scholar 

  • Yilmaz LS, Kontur WS, Sanders AP, Sohmen U, Donohue TJ, Noguera DR (2010) Electron partitioning during light- and nutrient-powered hydrogen production by Rhodobacter sphaeroides. Bioenerg Res 1:55–66

    Article  Google Scholar 

  • Zijffers JW, Schippers KJ, Zheng K, Janssen M, Tramper J, Wijffels RH (2010) Maximum photosynthetic yield of green microalgae in photobioreactors. Mar Biotechnol (NY) 12(6):708–718

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded in part by the Department of Energy, Office of Science, Great Lakes Bioenergy Research Center (DE-FC02-07ER64494), and the Genomics:GTL and SciDAC Programs (DE-FG02-04ER25627). SI was supported during part of this work by a William H. Peterson Predoctoral Fellowship from the University of Wisconsin-Madison Bacteriology Department.

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Correspondence to Daniel R. Noguera.

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Imam, S., Fitzgerald, C.M., Cook, E.M. et al. Quantifying the effects of light intensity on bioproduction and maintenance energy during photosynthetic growth of Rhodobacter sphaeroides . Photosynth Res 123, 167–182 (2015). https://doi.org/10.1007/s11120-014-0061-1

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