Skip to main content
SpringerLink
Log in

Toward a photosynthetic microbial platform for terpenoid engineering

  • Review
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Plant terpenoids are among the most diverse group of naturally-occurring organic compounds known, and several are used in contemporary consumer products. Terpene synthase enzymes catalyze complex rearrangements of carbon skeleton precursors to yield thousands of unique chemical structures that range in size from the simplest five carbon isoprene unit to the long polymers of rubber. Such chemical diversity has established plant terpenoids as valuable commodity chemicals with applications in the pharmaceutical, neutraceutical, cosmetic, and food industries. More recently, terpenoids have received attention as a renewable alternative to petroleum-derived fuels and as the building blocks of synthetic biopolymers. However, the current plant- and petrochemical-based supplies of commodity terpenoids have major limitations. Photosynthetic microorganisms provide an opportunity to generate terpenoids in a renewable manner, employing a single consolidated host organism that is able to use solar energy, H2O and CO2 as the primary inputs for terpenoid biosynthesis. Advances in synthetic biology have seen important breakthroughs in microbial terpenoid engineering, traditionally via fermentative pathways in yeast and Escherichia coli. This review draws on the knowledge obtained from heterotrophic microbial engineering to propose strategies for the development of microbial photosynthetic platforms for industrial terpenoid production. The importance of utilizing the wealth of genetic information provided by nature to unravel the regulatory mechanisms of terpenoid biosynthesis is highlighted.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

DMAPP:

Dimethylallyl pyrophosphate

DXP:

1-Deoxy-d-xylulose 5-phosphate

DXR:

1-Deoxy-d-xylulose 5-phosphate reductase

DXS:

1-Deoxy-d-xylulose 5-phosphate synthase

FPP:

Farnesyl pyrophosphate

GAP:

Glyceraldehyde 3-phosphate

GGPP:

Geranylgeranyl pyrophosphate

GPP:

Geranyl pyrophosphate

IDI:

Isopentenyl diphosphate isomerase

IPP:

Isopentenyl pyrophosphate

LIMS:

Limonene synthase

MEP:

Methyl-d-erythritol 4-phosphate

MVA:

Mevalonate

PTM:

Post translational modification

TPS:

Terpene synthase

SQS:

Squalene synthase

References

  • Agranoff BW, Eggerer H, Henning U, Lynen F (1959) Isopentenyl pyrophosphate isomerase. J Am Chem Soc 81:1254–1255

    CAS  Google Scholar 

  • Agranoff BW, Eggerer H, Henning U, Lynen F (1960) Biosynthesis of terpenes. VII. Isopentenyl pyrophosphate isomerase. J Biol Chem 235:326–332

    CAS  PubMed  Google Scholar 

  • Ajikumar PK, Tyo K, Carlsen S, Mucha O, Phon TH, Stephanopoulos G (2008) Terpenoids: opportunities for biosynthesis of natural product drugs using engineered microorganisms. Mol Pharm 5:167–190

    CAS  PubMed  Google Scholar 

  • Ajikumar PK, Xiao WH, Tyo KEJ, Wang Y, Simeon F, Leonard E, Mucha O, Phon TH, Pfeifer B, Stephanopoulos G (2010) Isoprenoid pathway optimization for taxol precursor overproduction in Escherichia coli. Science 330:70–74

    PubMed Central  CAS  PubMed  Google Scholar 

  • Albertsen L, Chen Y, Bach LS, Rattleff S, Maury J, Brix S, Nielsen J, Mortensen UH (2011) Diversion of flux toward sesquiterpene production in Saccharomyces cerevisiae by fusion of host and heterologous enzymes. Appl Environ Microbiol 77:1033–1040

    PubMed Central  CAS  PubMed  Google Scholar 

  • Albrecht M, Misawa N, Sandmann G (1999) Metabolic engineering of the terpenoid biosynthetic pathway of Escherichia coli for production of the carotenoids beta-carotene and zeaxanthin. Biotechnol Lett 21:791–795

    CAS  Google Scholar 

  • Alonso WR, Rajaonarivony JIM, Gershenzon J, Croteau R (1992) Purification of 4S-limonene synthase, a monoterpene cyclase from the glandular trichomes of peppermint (Mentha x piperita) and spearmint (Mentha spicata). J Biol Chem 267:7582–7587

    CAS  PubMed  Google Scholar 

  • Alonso-Gutierrez J, Chan R, Batth TS, Adams PD, Keasling JD, Petzold CJ, Lee TS (2013) Metabolic engineering of Escherichia coli for limonene and perillyl alcohol production. Metab Eng 19:33–41

    CAS  PubMed  Google Scholar 

  • Balmer Y, Koller A, del Val G, Manieri W, Schurmann P, Buchanan BB (2003) Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proc Natl Acad Sci USA 100:370–375

    PubMed Central  CAS  PubMed  Google Scholar 

  • Behnke K, Ehlting B, Teuber M, Bauerfeind M, Louis S, Hasch R, Polle A, Bohlmann J, Schnitzler JP (2007) Transgenic, non-isoprene emitting poplars don’t like it hot. Plant J 51:485–499

    CAS  PubMed  Google Scholar 

  • Bentley FK, Melis A (2012) Diffusion-based process for carbon dioxide uptake and isoprene emission in gaseous/aqueous two-phase photobioreactors by photosynthetic microorganisms. Biotechnol Bioeng 109:100–109

    CAS  PubMed  Google Scholar 

  • Bentley FK, García-Cerdán JG, Chen H-C (2013) Paradigm of monoterpene (β-phellandrene) hydrocarbons production via photosynthesis in cyanobacteria. BioEnergy Res 6:917–929

    CAS  Google Scholar 

  • Bentley FK, Zurbriggen A, Melis A (2014) Heterologous expression of the mevalonic acid pathway in cyanobacteria enhances endogenous carbon partitioning to isoprene. Mol Plant 7:71–86

    CAS  PubMed  Google Scholar 

  • Bohlmann J, Keeling CI (2008) Terpenoid biomaterials. Plant J 54:656–669

    CAS  PubMed  Google Scholar 

  • Breitmaier E (2006) Terpenes: flavors, fragrances, pharmaca, pheromones. Wiley-VCH, Weinheim

    Google Scholar 

  • Byrne CM, Allen SD, Lobkovsky EB, Coates GW (2004) Alternating copolymerization of limonene oxide and carbon dioxide. J Am Chem Soc 126:11404–11405

    CAS  PubMed  Google Scholar 

  • Carretero-Paulet L, Lipska A, Perez-Gil J, Sangari FJ, Albert VA, Rodriguez-Concepcion M (2013) Evolutionary diversification and characterization of the eubacterial gene family encoding DXR type II, an alternative isoprenoid biosynthetic enzyme. BMC Evol Biol 13:180–197

    PubMed Central  PubMed  Google Scholar 

  • Carrieri D, Paddock T, Maness PC, Seibert M, Yu JP (2012) Photo-catalytic conversion of carbon dioxide to organic acids by a recombinant cyanobacterium incapable of glycogen storage. Energy Environ Sci 5:9457–9461

    CAS  Google Scholar 

  • Carter OA, Peters RJ, Croteau R (2003) Monoterpene biosynthesis pathway construction in Escherichia coli. Phytochemistry 64:425–433

    CAS  PubMed  Google Scholar 

  • Chen F, Tholl D, Bohlmann J, Pichersky E (2011) The family of terpene synthases in plants: a mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant 66:212–229

    CAS  Google Scholar 

  • Colby SM, Alonso WR, Katahira EJ, McGarvey DJ, Croteau R (1993) 4S-limonene synthase from the oil glands of spearmint (Mentha spicata). cDNA isolation, characterization, and bacterial expression of the catalytically active monoterpene cyclase. J Biol Chem 268:23016–23024

    CAS  PubMed  Google Scholar 

  • Conrado RJ, Wu GC, Boock JT, Xu HS, Chen SY, Lebar T, Turnsek J, Tomsic N, Avbelj M, Gaber R, Koprivnjak T, Mori J, Glavnik V, Vovk I, Bencina M, Hodnik V, Anderluh G, Dueber JE, Jerala R, DeLisa MP (2012) DNA-guided assembly of biosynthetic pathways promotes improved catalytic efficiency. Nucleic Acids Res 40:1879–1889

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cordoba E, Porta H, Arroyo A, Roman CS, Medina L, Rodriguez-Concepcion M, Leon P (2011) Functional characterization of the three genes encoding 1-deoxy-D-xylulose 5-phosphate synthase in maize. J Exp Bot 62:2023–2038

    CAS  PubMed  Google Scholar 

  • Doshi R, Nguyen T, Chang G (2013) Transporter-mediated biofuel secretion. Proc Nat Acad Sci USA 110:7642–7647

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ducat DC, Avelar-Rivas JA, Way JC, Silver PA (2012) Rerouting carbon flux to enhance photosynthetic productivity. Appl Environ Microbiol 78:2660–2668

    PubMed Central  CAS  PubMed  Google Scholar 

  • Dueber JE, Wu GC, Malmirchegini GR, Moon TS, Petzold CJ, Ullal AV, Prather KLJ, Keasling JD (2009) Synthetic protein scaffolds provide modular control over metabolic flux. Nat Biotechnol 27:753–759

    CAS  PubMed  Google Scholar 

  • Dunlop MJ, Dossani ZY, Szmidt HL, Chu HC, Lee TS, Keasling JD, Hadi MZ, Mukhopadhyay A (2011) Engineering microbial biofuel tolerance and export using efflux pumps. Mol Syst Biol 7:487–493

    PubMed Central  PubMed  Google Scholar 

  • Eaton-Rye JJ (2011) Construction of gene interruptions and gene deletions in the cyanobacterium Synechocystis sp. strain PCC 6803. Methods Mol Biol 684:295–312

    CAS  PubMed  Google Scholar 

  • Erb TJ, Evans BS, Cho K, Warlick BP, Sriram J, Wood BM, Imker HJ, Sweedler JV, Tabita FR, Gerlt JA (2012) A RubisCO-like protein links SAM metabolism with isoprenoid biosynthesis. Nat Chem Biol 8:926–932

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ershov YV, Gantt RR, Cunningham FX, Gantt E (2002) Isoprenoid biosynthesis in Synechocystis sp strain PCC6803 is stimulated by compounds of the pentose phosphate cycle but not by pyruvate or deoxyxylulose-5-phosphate. J Bacteriol 184:5045–5051

    PubMed Central  CAS  PubMed  Google Scholar 

  • Farmer WR, Liao JC (2000) Improving lycopene production in Escherichia coli by engineering metabolic control. Nat Biotechnol 18:533–537

    CAS  PubMed  Google Scholar 

  • Farmer WR, Liao JC (2001) Precursor balancing for metabolic engineering of lycopene production in Escherichia coli. Biotechnol Prog 17:57–61

    CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence-limits on phylogenies—an approach using the bootstrap. Evolution 39:783–791

    Google Scholar 

  • Firdaus M, de Espinosa LM, Meier MAR (2011) Terpene-based renewable monomers and polymers via thiol-ene additions. Macromolecules 44:7253–7262

    CAS  Google Scholar 

  • Frenz L, Ubersax J (2012) Methods and compositions for detecting microbial production of water-immiscible compounds. Patent WO2012158466 A1

  • Frigaard NU, Sakuragi Y, Bryant DA (2004) Gene inactivation in the cyanobacterium Synechococcus sp. PCC 7002 and the green sulfur bacterium Chlorobium tepidum using in vitro-made DNA constructs and natural transformation. Methods Mol Biol 274:325–340

    CAS  PubMed  Google Scholar 

  • Gabrielsen M, Rohdich F, Eisenreich W, Grawert T, Hecht S, Bacher A, Hunter WN (2004) Biosynthesis of isoprenoids—a bifunctional IspDF enzyme from Campylobacter jejuni. Eur J Biochem 271:3028–3035

    CAS  PubMed  Google Scholar 

  • Geer LY, Domrachev M, Lipman DJ, Bryant SH (2002) CDART: protein homology by domain architecture. Genome Res 12:1619–1623

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ghirardo A, Gutknecht J, Zimmer I, Bruggemann N, Schnitzler JP (2011) Biogenic volatile organic compound and respiratory CO2 emissions after 13C-Labeling: online tracing of C translocation dynamics in poplar plants. PLoS ONE 6:e17393

    PubMed Central  CAS  PubMed  Google Scholar 

  • Go YM, Jones DP (2013) The redox proteome. J Biol Chem 288:26512–26520

    PubMed Central  CAS  PubMed  Google Scholar 

  • Grundel M, Scheunemann R, Lockau W, Zilliges Y (2012) Impaired glycogen synthesis causes metabolic overflow reactions and affects stress responses in the cyanobacterium Synechocystis sp PCC 6803. Microbiol SGM 158:3032–3043

    Google Scholar 

  • Guenther A, Karl T, Harley P, Wiedinmyer C, Palmer PI, Geron C (2006) Estimates of global terrestrial isoprene emissions using MEGAN (model of emissions of gases and aerosols from nature). Atmos Chem Phys 6:3181–3210

    CAS  Google Scholar 

  • Guenther AB, Jiang X, Heald CL, Sakulyanontvittaya T, Duhl T, Emmons LK, Wang X (2012) The model of emissions of gases and aerosols from nature version 2.1 (MEGAN2.1): an extended and updated framework for modeling biogenic emissions. Geosci Model Dev 5:1471–1492

    Google Scholar 

  • Hale I, O’Neill PM, Berry NG, Odom A, Sharma R (2012) The MEP pathway and the development of inhibitors as potential anti-infective agents. Medchemcomm 3:418–433

    CAS  Google Scholar 

  • Harker M, Bramley PM (1999) Expression of prokaryotic 1-deoxy-D-xylulose-5-phosphatases in Escherichia coli increases carotenoid and ubiquinone biosynthesis. FEBS Lett 448:115–119

    CAS  PubMed  Google Scholar 

  • Hedl M, Sutherlin A, Wilding EI, Mazzulla M, McDevitt D, Lane P, Burgner JW, Lehnbeuter KR, Stauffacher CV, Gwynn MN, Rodwell VW (2002) Enterococcus faecalis acetoacetyl-coenzyme A thiolase/3-hydroxy-3-methylglutaryl-coenzyme A reductase, a dual-function protein of isopentenyl diphosphate biosynthesis. J Bacteriol 184:2116–2122

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hellier P, Al-Haj L, Talibi M, Purton S, Ladommatos N (2013) Combustion and emissions characterization of terpenes with a view to their biological production in cyanobacteria. Fuel 111:670–688

    CAS  Google Scholar 

  • Hemmerlin A (2013) Post-translational events and modifications regulating plant enzymes involved in isoprenoid precursor biosynthesis. Plant Sci 203:41–54

    PubMed  Google Scholar 

  • Hemmerlin A, Harwood JL, Bach TJ (2012) A raison d’etre for two distinct pathways in the early steps of plant isoprenoid biosynthesis? Prog Lipid Res 51:95–148

    CAS  PubMed  Google Scholar 

  • Hezari M, Lewis NG, Croteau R (1995) Purification and characterization of taxa-4(5),11(12)-diene synthase from Pacific yew (Taxus brevifolia) that catalyzes the first committed step of taxol biosynthesis. Arch Biochem Biophys 322:437–444

    CAS  PubMed  Google Scholar 

  • Hickman JW, Kotovic KM, Miller C, Warrener P, Kaiser B, Jurista T, Budde M, Cross F, Roberts JM, Carleton M (2013) Glycogen synthesis is a required component of the nitrogen stress response in Synechococcus elongatus PCC 7942. Algal Res 2:98–106

    Google Scholar 

  • Huang HH, Lindblad P (2013) Wide-dynamic-range promoters engineered for cyanobacteria. J Biol Eng 7:10–21

    PubMed Central  CAS  PubMed  Google Scholar 

  • Huang QL, Roessner CA, Croteau R, Scott AI (2001) Engineering Escherichia coli for the synthesis of taxadiene, a key intermediate in the biosynthesis of taxol. Bioorg Med Chem 9:2237–2242

    CAS  PubMed  Google Scholar 

  • Huang HH, Camsund D, Lindblad P, Heidorn T (2010) Design and characterization of molecular tools for a synthetic biology approach towards developing cyanobacterial biotechnology. Nucleic Acids Res 38:2577–2593

    PubMed Central  CAS  PubMed  Google Scholar 

  • Huang SQ, Chen L, Te RG, Qiao JJ, Wang JX, Zhang WW (2013) Complementary iTRAQ proteomics and RNA-seq transcriptomics reveal multiple levels of regulation in response to nitrogen starvation in Synechocystis sp PCC 6803. Mol BioSyst 9:2565–2574

    CAS  PubMed  Google Scholar 

  • Hyatt DC, Youn BY, Zhao YX, Santhamma B, Coates RM, Croteau RB, Kang CH (2007) Structure of limonene synthase, a simple model for terpenoid cyclase catalysis. Proc Natl Acad Sci USA 104:5360–5365

    PubMed Central  CAS  PubMed  Google Scholar 

  • Immethun CM, Hoynes-O’Connor AG, Balassy A, Moon TS (2013) Microbial production of isoprenoids enabled by synthetic biology. Front Microbiol 4:75

    PubMed Central  PubMed  Google Scholar 

  • Jinkerson RE, Radakovits R, Posewitz MC (2013) Genomic insights from the oleaginous model alga Nannochloropsis gaditana. Bioengineered 4:37–43

    PubMed Central  PubMed  Google Scholar 

  • Kajiwara S, Fraser PD, Kondo K, Misawa N (1997) Expression of an exogenous isopentenyl diphosphate isomerase gene enhances isoprenoid biosynthesis in Escherichia coli. Biochem J 324:421–426

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kamatou GPP, Vermaak I, Viljoen AM, Lawrence BM (2013) Menthol: a simple monoterpene with remarkable biological properties. Phytochemistry 96:15–25

    CAS  PubMed  Google Scholar 

  • Kaneda K, Kuzuyama T, Takagi M, Hayakawa Y, Seto H (2001) An unusual isopentenyl diphosphate isomerase found in the mevalonate pathway gene cluster from Streptomyces sp strain CL190. Proc Nat Acad Sci USA 98:932–937

    PubMed Central  CAS  PubMed  Google Scholar 

  • Keasling JD (2012) Synthetic biology and the development of tools for metabolic engineering. Metab Eng 14:189–195

    CAS  PubMed  Google Scholar 

  • Kesselmeier J, Staudt M (1999) Biogenic volatile organic compounds (VOC): an overview on emission, physiology and ecology. J Atmos Chem 33:23–88

    CAS  Google Scholar 

  • Kirby J, Keasling JD (2009) Biosynthesis of plant isoprenoids: perspectives for microbial engineering. Annu Rev Plant Biol 60:335–355

    CAS  PubMed  Google Scholar 

  • Kobayashi S, Lu C, Hoye TR, Hillmyer MA (2009) Controlled polymerization of a cyclic diene prepared from the ring-closing metathesis of a naturally occurring monoterpene. J Am Chem Soc 131:7960–7961

    CAS  PubMed  Google Scholar 

  • Koksal M, Zimmer I, Schnitzler JP, Christianson DW (2010) Structure of isoprene synthase illuminates the chemical mechanism of teragram atmospheric carbon emission. J Mol Biol 402:363–373

    PubMed Central  PubMed  Google Scholar 

  • Kung Y, Runguphan W, Keasling JD (2012) From fields to fuels: recent advances in the microbial production of biofuels. ACS Synth Biol 1:498–513

    CAS  PubMed  Google Scholar 

  • Lanekoff I, Geydebrekht O, Pinchuk GE, Konopka AE, Laskin J (2013) Spatially resolved analysis of glycolipids and metabolites in living Synechococcus sp PCC 7002 using nanospray desorption electrospray ionization. Analyst 138:1971–1978

    CAS  PubMed  Google Scholar 

  • Lange BM, Rujan T, Martin W, Croteau R (2000) Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. Proc Nat Acad Sci USA 97:13172–13177

    PubMed Central  CAS  PubMed  Google Scholar 

  • Langenheim JH (1994) Higher plant terpenoids: a phytocentric overview of their ecological roles. J Chem Ecol 20:1223–1280

    CAS  PubMed  Google Scholar 

  • Laupitz R, Hecht S, Amslinger S, Zepeck F, Kaiser J, Richter G, Schramek N, Steinbacher S, Huber R, Arigoni D, Bacher A, Eisenreich W, Rohdich F (2004) Biochemical characterization of Bacillus subtilis type II isopentenyl diphosphate isomerase, and phylogenetic distribution of isoprenoid biosynthesis pathways. Eur J Biochem 271:2658–2669

    CAS  PubMed  Google Scholar 

  • Legere E, Mantecon E, Moll B, Unamunzaga C, Woods RP (2008) Closed photobioreactor system for production of ethanol. Patent WO2008055190 A3

  • Lemaire SD, Guillon B, Le Marechal P, Keryer E, Miginiac-Maslow M, Decottignies P (2004) New thioredoxin targets in the unicellular photosynthetic eukaryote Chlamydomonas reinhardtii. Proc Nat Acad Sci USA 101:7475–7480

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lherbet C, Pojer F, Richard SB, Noel JP, Poulter CD (2006) Absence of substrate channeling between active sites in the Agrobacterium tumefaciens IspDF and IspE enzymes of the methyl erythritol phosphate pathway. Biochemistry 45:3548–3553

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lichtenthaler HK (1999) The 1-deoxy-D-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 50:47–65

    CAS  PubMed  Google Scholar 

  • Lindberg P, Park S, Melis A (2010) Engineering a platform for photosynthetic isoprene production in cyanobacteria, using Synechocystis as the model organism. Metab Eng 12:70–79

    CAS  PubMed  Google Scholar 

  • Lombard J, Moreira D (2011) Origins and early evolution of the mevalonate pathway of isoprenoid biosynthesis in the three domains of life. Mol Biol Evol 28:87–99

    CAS  PubMed  Google Scholar 

  • Lucker J, El Tamer MK, Schwab W, Verstappen FWA, van der Plas LHW, Bouwmeester HJ, Verhoeven HA (2002) Monoterpene biosynthesis in lemon (Citrus limon)—cDNA isolation and functional analysis of four monoterpene synthases. Eur J Biochem 269:3160–3171

    CAS  PubMed  Google Scholar 

  • Ludwig M, Bryant DA (2012) Acclimation of the global transcriptome of the cyanobacterium Synechococcus sp. strain PCC 7002 to nutrient limitations and different nitrogen sources. Front Microbiol 3:145

    PubMed Central  CAS  PubMed  Google Scholar 

  • Macek B, Gnad F, Soufi B, Kumar C, Olsen JV, Mijakovic I, Mann M (2008) Phosphoproteome analysis of E. coli reveals evolutionary conservation of bacterial Ser/Thr/Tyr phosphorylation. Mol Cell Proteomics 7:299–307

    CAS  PubMed  Google Scholar 

  • Martin VJJ, Pitera DJ, Withers ST, Newman JD, Keasling JD (2003) Engineering a mevalonate pathway in Escherichia coli for production of terpenoids. Nat Biotechnol 21:796–802

    CAS  PubMed  Google Scholar 

  • Matsushima D, Jenke-Kodama H, Sato Y, Fukunaga Y, Sumimoto K, Kuzuyama T, Matsunaga S, Okada S (2012) The single cellular green microalga Botryococcus braunii, race B possesses three distinct 1-deoxy-D-xylulose 5-phosphate synthases. Plant Sci 185:309–320

    PubMed  Google Scholar 

  • McGarvey DJ, Croteau R (1995) Terpenoid metabolism. Plant Cell 7:1015–1026

    PubMed Central  CAS  PubMed  Google Scholar 

  • Melis A (2013) Carbon partitioning in photosynthesis. Curr Opin Chem Biol 17:453–456

    CAS  PubMed  Google Scholar 

  • Metzger P, Berkaloff C, Casadevall E, Couté A (1985) Alkadiene-producing and botryococcene-producing races of wild strains of Botryococcus braunii. Phytochemistry 24:2305–2312

    CAS  Google Scholar 

  • Mgalobilishvili MP, Khetsuriani ND, Kalandadze AN, Sanadze GA (1978) Localization of isoprene biosynthesis in poplar leaf chloroplasts. Fiziol Rast 25:1055–1061

    Google Scholar 

  • Misawa N, Nakagawa M, Kobayashi K, Yamano S, Izawa Y, Nakamura K, Harashima K (1990) Elucidation of the Erwinia uredovora carotenoid biosynthetic pathway by functional analysis of gene products expressed in Escherichia coli. J Bacteriol 172:6704–6712

    PubMed Central  CAS  PubMed  Google Scholar 

  • Miura Y, Kondo K, Saito T, Shimada H, Fraser PD, Misawa N (1998) Production of the carotenoid lycopene, beta-carotene, and astaxanthin in the food yeast Candida utilis. Appl Environ Microbiol 64:1226–1229

    PubMed Central  CAS  PubMed  Google Scholar 

  • Miziorko HM (2011) Enzymes of the mevalonate pathway of isoprenoid biosynthesis. Arch Biochem Biophys 505:131–143

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mohamed A, Eriksson J, Osiewacz HD, Jansson C (1993) Differential expression of the psbA genes in the cyanobacterium Synechocystis 6803. Mol Gen Genet 238:161–168

    CAS  PubMed  Google Scholar 

  • Morrone D, Lowry L, Determan MK, Hershey DM, Xu MM, Peters RJ (2010) Increasing diterpene yield with a modular metabolic engineering system in E. coli: comparison of MEV and MEP isoprenoid precursor pathway engineering. Appl Microbiol Biotechnol 85:1893–1906

    PubMed Central  CAS  PubMed  Google Scholar 

  • Okada K, Hase T (2005) Cyanobacterial non-mevalonate pathway—(E)-4-hydroxy-3-methylbut-2-enyl diphosphate synthase interacts with ferredoxin in Thermosynechococcus elongatus BP-1. J Biol Chem 280:20672–20679

    CAS  PubMed  Google Scholar 

  • Okada S, Murakami M, Yamaguchi K (1995) Hydrocarbon composition of newly isolated strains of the green microalga Botryococcus braunii. J Appl Phycol 7:555–559

    CAS  Google Scholar 

  • Peralta-Yahya PP, Ouellet M, Chan R, Mukhopadhyay A, Keasling JD, Lee TS (2011) Identification and microbial production of a terpene-based advanced biofuel. Nat Commun 2:483

    PubMed Central  PubMed  Google Scholar 

  • Perez-Gil J, Bergua M, Boronat A, Imperial S (2010) Cloning and functional characterization of an enzyme from Helicobacter pylori that catalyzes two steps of the methylerythritol phosphate pathway for isoprenoid biosynthesis. Biochim Biophys Acta 1800:919–928

    CAS  PubMed  Google Scholar 

  • Phillips MA, Walter MH, Ralph SG, Dabrowska P, Luck K, Uros EM, Boland W, Strack D, Rodriguez-Concepcion M, Bohlmann J, Gershenzon J (2007) Functional identification and differential expression of 1-deoxy-D-xylulose 5-phosphate synthase in induced terpenoid resin formation of Norway spruce (Picea abies). Plant Mol Biol 65:243–257

    CAS  PubMed  Google Scholar 

  • Poliquin K, Ershov YV, Cunningham FX, Woreta TT, Gantt RR, Gantt E (2004) Inactivation of sll1556 in Synechocystis strain PCC 6803 impairs isoprenoid biosynthesis from pentose phosphate cycle substrates in vitro. J Bacteriol 186:4685–4693

    PubMed Central  CAS  PubMed  Google Scholar 

  • Puan KJ, Wang H, Dairi T, Kuzuyama T, Morita CT (2005) fldA is an essential gene required in the 2-C-methyl-D-erythritol 4-phosphate pathway for isoprenoid biosynthesis. FEBS Lett 579:3802–3806

    CAS  PubMed  Google Scholar 

  • Pulido P, Toledo-Ortiz G, Phillips MA, Wright LP, Rodríguez-Concepción M (2013) Arabidopsis J-protein J20 delivers the first enzyme of the plastidial isoprenoid pathway to protein quality control. Plant Cell 25:4183–4194

    PubMed Central  CAS  PubMed  Google Scholar 

  • Puskas JE, Gautriaud E, Deffieux A, Kennedy JP (2006) Natural rubber biosynthesis—a living carbocationic polymerization? Prog Polym Sci 31:533–548

    CAS  Google Scholar 

  • Radakovits R, Jinkerson RE, Fuerstenberg SI, Tae H, Settlage RE, Boore JL, Posewitz MC (2012) Draft genome sequence and genetic transformation of the oleaginous alga Nannochloropis gaditana. Nat Commun 3:686

    PubMed Central  PubMed  Google Scholar 

  • Rajaonarivony JIM, Gershenzon J, Croteau R (1992) Characterization and mechanism of (4S)-limonene synthase, a monoterpene cyclase from the glandular trichomes of peppermint (Mentha × piperita). Arch Biochem Biophys 296:49–57

    CAS  PubMed  Google Scholar 

  • Reiland S, Messerli G, Baerenfaller K, Gerrits B, Endler A, Grossmann J, Gruissem W, Baginsky S (2009) Large-scale Arabidopsis phosphoproteome profiling reveals novel chloroplast kinase substrates and phosphorylation networks. Plant Physiol 150:889–903

    PubMed Central  CAS  PubMed  Google Scholar 

  • Reinsvold RE, Jinkerson RE, Radakovits R, Posewitz MC, Basu C (2011) The production of the sesquiterpene β-caryophyllene in a transgenic strain of the cyanobacterium Synechocystis. J Plant Physiol 168:848–852

    CAS  PubMed  Google Scholar 

  • Ro DK, Paradise EM, Ouellet M, Fisher KJ, Newman KL, Ndungu JM, Ho KA, Eachus RA, Ham TS, Kirby J, Chang MCY, Withers ST, Shiba Y, Sarpong R, Keasling JD (2006) Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 440:940–943

    CAS  PubMed  Google Scholar 

  • Rohmer M, Knani M, Simonin P, Sutter B, Sahm H (1993) Isoprenoid biosynthesis in bacteria: A novel pathway for the early steps leading to isopentenyl diphosphate. Biochem J 295:517–524

    PubMed Central  CAS  PubMed  Google Scholar 

  • Rohmer M, Seemann M, Horbach S, BringerMeyer S, Sahm H (1996) Glyceraldehyde 3-phosphate and pyruvate as precursors of isoprenic units in an alternative non-mevalonate pathway for terpenoid biosynthesis. J Am Chem Soc 118:2564–2566

    CAS  Google Scholar 

  • Ruzicka L (1953) The isoprene rule and the biogenesis of terpenic compounds. Experientia 9:357–367

    CAS  PubMed  Google Scholar 

  • Sadler NC, Melnicki MR, Serres MH, et al (2013) Live cell chemical profiling of temporal redox dynamics in a photoautotrophic cyanobacterium. ACS Chem Biol. doi:10.1021/cb400769v

  • Saitou N, Nei M (1987) The neighbor-joining method—a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Sanadze GA (1969) Light-dependent excretion of molecular isoprene. Prog Photosynth Res 2:701–707

    CAS  Google Scholar 

  • Sanadze GA, Dzhaiani GI, Tevzadze IM (1972) Incorporating into the isoprene molecule of carbon from 13CO2 assimilated during photosynthesis. Fisiol Rast 19:17–20

    Google Scholar 

  • Sangari FJ, Perez-Gil J, Carretero-Paulet L, Garcia-Lobo JM, Rodriguez-Concepcion M (2010) A new family of enzymes catalyzing the first committed step of the methylerythritol 4-phosphate (MEP) pathway for isoprenoid biosynthesis in bacteria. Proc Nat Acad Sci USA 107:14081–14086

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sasaki K, Ohara K, Yazaki K (2005) Gene expression and characterization of isoprene synthase from Populus alba. FEBS Lett 579:2514–2518

    CAS  PubMed  Google Scholar 

  • Sasaki K, Saito T, Lamsa M, Oksman-Caldentey KM, Suzuki M, Ohyama K, Muranaka T, Ohara K, Yazaki K (2007) Plants utilize isoprene emission as a thermotolerance mechanism. Plant Cell Physiol 48:1254–1262

    CAS  PubMed  Google Scholar 

  • Sauret-Gueto S, Uros EM, Ibanez E, Boronat A, Rodriguez-Concepcion M (2006) A mutant pyruvate dehydrogenase E1 subunit allows survival of Escherichia coli strains defective in 1-deoxy-D-xylulose 5-phosphate synthase. FEBS Lett 580:736–740

    PubMed  Google Scholar 

  • Schnitzler JP, Zimmer I, Bachl A, Arend M, Fromm J, Fischbach RJ (2005) Biochemical properties of isoprene synthase in poplar (Populus × canescens). Planta 222:777–786

    CAS  PubMed  Google Scholar 

  • Schnitzler JP, Louis S, Behnke K, Loivamaki M (2010) Poplar volatiles—biosynthesis, regulation and (eco)physiology of isoprene and stress-induced isoprenoids. Plant Biol 12:302–316

    CAS  PubMed  Google Scholar 

  • Seemann M, Bui BTS, Wolff M, Miginlac-Maslow M, Rohmer M (2006) Isoprenoid biosynthesis in plant chloroplasts via the MEP pathway: direct thylakoid/ferredoxin-dependent photoreduction of GcpE/IspG. FEBS Lett 580:1547–1552

    CAS  PubMed  Google Scholar 

  • Sharkey TD, Singsaas EL (1995) Why plants emit isoprene. Nature 374:769

    CAS  Google Scholar 

  • Sharkey TD, Yeh SS (2001) Isoprene emission from plants. Annu Rev Plant Physiol Plant Mol Biol 52:407–436

    CAS  PubMed  Google Scholar 

  • Sharkey TD, Wiberley AE, Donohue AR (2008) Isoprene emission from plants: why and how. Ann Bot 101:5–18

    PubMed Central  CAS  PubMed  Google Scholar 

  • Shimada H, Kondo K, Fraser PD, Miura Y, Saito T, Misawa N (1998) Increased carotenoid production by the food yeast Candida utilis through metabolic engineering of the isoprenoid pathway. Appl Environ Microbiol 64:2676–2680

    PubMed Central  CAS  PubMed  Google Scholar 

  • Silver GM, Fall R (1995) Characterization of aspen isoprene synthase, an enzyme responsible for leaf isoprene emission to the atmosphere. J Biol Chem 270:13010–13016

    CAS  PubMed  Google Scholar 

  • Singsaas EL, Lerdau M, Winter K, Sharkey TD (1997) Isoprene increases thermotolerance of isoprene-emitting species. Plant Physiol 115:1413–1420

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    PubMed Central  CAS  PubMed  Google Scholar 

  • Testa CA, Lherbet C, Pojer F, Noel JP, Poulter CD (2006) Cloning and expression of IspDF from Mesorhizobium loti. Characterization of a bifunctional protein that catalyzes non-consecutive steps in the methylerythritol phosphate pathway. Biochim Biophys Acta 1764:85–96

    CAS  PubMed  Google Scholar 

  • Thulasiram HV, Erickson HK, Poulter CD (2007) Chimeras of two isoprenoid synthases catalyze all four coupling reactions in isoprenoid biosynthesis. Science 316:73–76

    CAS  PubMed  Google Scholar 

  • Tritsch D, Hemmerlin A, Bach TJ, Rohmer M (2010) Plant isoprenoid biosynthesis via the MEP pathway: in vivo IPP/DMAPP ratio produced by (E)-4-hydroxy-3-methylbut-2-enyl diphosphate reductase in tobacco BY-2 cell cultures. FEBS Lett 584:129–134

    CAS  PubMed  Google Scholar 

  • Tuskan GA, DiFazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604

    CAS  PubMed  Google Scholar 

  • Vadali RV, Fu YC, Bennett GN, San KY (2005) Enhanced lycopene productivity by manipulation of carbon flow to isopentenyl diphosphate in Escherichia coli. Biotechnol Prog 21:1558–1561

    CAS  PubMed  Google Scholar 

  • van Beillen JB, Poirier Y (2007) Gunyule and Russian dandelion as alternative sources of natural rubber. Crit Rev Biotechnol 27:217–231

    Google Scholar 

  • Wagschal K, Savage TJ, Croteau R (1991) Isotopically sensitive branching as a tool for evaluating multiple product formation by monoterpene cyclases. Tetrahedron 47:5933–5944

    CAS  Google Scholar 

  • Walter MH, Hans J, Strack D (2002) Two distantly related genes encoding 1-deoxy-D-xylulose 5-phosphate synthases: differential regulation in shoots and apocarotenoid-accumulating mycorrhizal roots. Plant J 31:243–254

    CAS  PubMed  Google Scholar 

  • Wang CW, Oh MK, Liao JC (1999) Engineered isoprenoid pathway enhances astaxanthin production in Escherichia coli. Biotechnol Bioeng 62:235–241

    CAS  PubMed  Google Scholar 

  • Wang C, Yoon SH, Jang HJ, Chung YR, Kim JY, Choi ES, Kim SW (2011) Metabolic engineering of Escherichia coli for alpha-farnesene production. Metab Eng 13:648–655

    CAS  PubMed  Google Scholar 

  • Webb H, Lanfear R, Hamill J, Foley WJ, Kulheim C (2013) The yield of essential oils in Melaleuca alternifolia (Myrtaceae) is regulated through transcript abundance of genes in the MEP pathway. PLoS ONE 8:e60631

    PubMed Central  CAS  PubMed  Google Scholar 

  • Weise SE, Li ZR, Sutter AE, Corrion A, Banerjee A, Sharkey TD (2013) Measuring dimethylallyl diphosphate available for isoprene synthesis. Anal Biochem 435:27–34

    CAS  PubMed  Google Scholar 

  • Whited GM, Feher FJ, Benko DA, Cervin MA, Chotani GK, McAuliffe JC, LaDuca RJ, Ben-Shoshan EA, Sanford KJ (2010) Development of a gas-phase bioprocess for isoprene-monomer production using metabolic pathway engineering. Ind Biotechnol 6:152–163

    CAS  Google Scholar 

  • Wilbon PA, Chu FX, Tang CB (2013) Progress in renewable polymers from natural terpenes, terpenoids, and rosin. Macromol Rapid Commun 34:8–37

    CAS  PubMed  Google Scholar 

  • Williams DC, McGarvey DJ, Katahira EJ, Croteau R (1998) Truncation of limonene synthase preprotein provides a fully active ‘Pseudomature’ form of this monoterpene cyclase and reveals the function of the amino-terminal arginine pair. Biochemistry 37:12213–12220

    CAS  PubMed  Google Scholar 

  • Work VH, D’Adamo S, Radakovits R, Jinkerson RE, Posewitz MC (2012) Improving photosynthesis and metabolic networks for the competitive production of phototroph-derived biofuels. Curr Opin Biotechnol 23:290–297

    CAS  PubMed  Google Scholar 

  • Xu Y, Alvey RM, Byrne PO, Graham JE, Shen G, Bryant DA (2011) Expression of genes in cyanobacteria: adaptation of endogenous plasmids as platforms for high level gene expression in Synechococcus sp. PCC 7002. Methods Mol Biol 684:273–293

    CAS  PubMed  Google Scholar 

  • Yang JM, Nie QJ, Ren M, Feng HR, Jiang XL, Zheng YN, Liu M, Zhang HB, Xian M (2013a) Metabolic engineering of Escherichia coli for the biosynthesis of alpha-pinene. Biotechnol Biofuels 6:60

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yang MK, Qiao ZX, Zhang WY, Xiong Q, Zhang J, Li T, Ge F, Zhao JD (2013b) Global phosphoproteomic analysis reveals diverse functions of serine/threonine/tyrosine phosphorylation in the model cyanobacterium Synechococcus sp strain PCC 7002. J Proteome Res 12:1909–1923

    CAS  PubMed  Google Scholar 

  • Zhang C, Chen X, Zou R, Zhou K, Gregory Stephanopoulos1, Too H-P (2013) Combining genotype improvement and statistical media optimization for isoprenoid production in E. coli. PLoS One. doi:10.1371/journal.pone.0075164

  • Zhao LS, Chang WC, Xiao YL, Liu HW, Liu PH (2013) Methylerythritol phosphate pathway of isoprenoid biosynthesis. Annu Rev Biochem 82:497–530

    CAS  PubMed  Google Scholar 

  • Zhou K, Zou RY, Stephanopoulos G, Too HP (2012) Metabolite profiling identified methylerythritol cyclodiphosphate efflux as a limiting step in microbial isoprenoid production. PLoS ONE 7:e47513

    PubMed Central  CAS  PubMed  Google Scholar 

  • Zhou CF, Li ZR, Wiberley-Bradford AE, Weise SE, Sharkey TD (2013a) Isopentenyl diphosphate and dimethylallyl diphosphate/isopentenyl diphosphate ratio measured with recombinant isopentenyl diphosphate isomerase and isoprene synthase. Anal Biochem 440:130–136

    CAS  PubMed  Google Scholar 

  • Zhou Y, Nambou K, Wei L, Cao J, Imanaka T, Hua Q (2013b) Lycopene production in recombinant strains of Escherichia coli is improved by knockout of the central carbon metabolism gene coding for glucose-6-phosphate dehydrogenase. Biotechnol Lett 35:2137–2145

    CAS  PubMed  Google Scholar 

  • Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. Evolving Genes and Proteins Academic Press, New York

    Google Scholar 

  • Zurbriggen A, Kirst H, Melis A (2012) Isoprene production via the mevalonic acid pathway in Escherichia coli (bacteria). Bioenergy Res 5:814–828

    CAS  Google Scholar 

Download references

Acknowledgments

The authors gratefully acknowledge financial support from the U.S. Department of Energy, Office of Science, Basic Energy Sciences (Grant DE-FG02-12ER16339), and the Air Force Office of Scientific Research (Grant FA9550-11-1-0211).

Author information

Authors and Affiliations

  1. Department of Chemistry and Geochemistry, Colorado School of Mines, Golden, CO, 80401, USA

    Fiona K. Davies, Robert E. Jinkerson & Matthew C. Posewitz

Authors
  1. Fiona K. Davies
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert E. Jinkerson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Matthew C. Posewitz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fiona K. Davies.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Davies, F.K., Jinkerson, R.E. & Posewitz, M.C. Toward a photosynthetic microbial platform for terpenoid engineering. Photosynth Res 123, 265–284 (2015). https://doi.org/10.1007/s11120-014-9979-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-014-9979-6

Keywords

Search

Navigation