The synthetic biology toolkit for photosynthetic ... · 111 commercial significance. In 1999, the...

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Short title: Synthetic biology in photosynthetic microorganisms 1

The synthetic biology toolkit for photosynthetic microorganisms 2

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Konstantinos Vavitsas1,2,5, Pierre Crozet3, Marcos Hamborg Vinde1,2, Fiona Davies4, Stéphane D. 4

Lemaire3, Claudia E. Vickers1,2* 5

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1 Australian Institute for Bioengineering and Nanotechnology, The University of Queensland, St 7

Lucia, Queensland 4072 8

2 CSIRO Synthetic Biology Future Science Platform, CSIRO Land & Water, GPO Box 2583, Brisbane, 9

Qld, 4001 10

3 Institut de Biologie Physico-Chimique, UMR 8226, CNRS, Sorbonne Université, Paris, France 11

4 Department of Chemistry, Colorado School of Mines, Golden, CO 80401, USA 12

5current address: Department of Biology, National and Kapodistrian University of Athens, 13

Panepistimioupolis, Athens 15784, Greece 14

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*Corresponding Author: [email protected] / [email protected] 16

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One-sentence summary: Photosynthetic microorganisms offer novel characteristics as synthetic 18

biology chassis, and the toolbox of componentry and techniques for cyanobacteria and algae is 19

rapidly increasing. 20

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Author contributions: All authors contributed to the writing of the paper 22

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Abstract 24

Cyanobacteria and algae are photosynthetic microorganisms that are emerging as attractive hosts 25

for synthetic biology applications, ranging from metabolic engineering for the production of 26

industrial biochemicals to microbial energy storage. Photosynthetic microbes have a unique 27

combination of characteristics that drives their consideration for synthetic biology, including 28

relatively simple physiology, fast photosynthetic growth, an availability of model systems, and useful 29

subcellular structures. However, their development as synthetic biology hosts/chassis has been 30

relatively slow compared to that of model heterotrophs. Here we review current synthetic biology 31

tools and applications in photosynthetic microbes and identify opportunities and challenges moving 32

into the future. We focus on cyanobacteria as model photosynthetic prokaryotes, specifically the 33

freshwater unicellular species Synechocystis sp. PCC 6803 and Synechococcus elongatus PCC 7942, 34

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the marine unicellular species Synechococcus sp. PCC 7002, and the nitrogen fixing filamentous 35

species Nostoc sp. PCC 7120. Moreover, we present algae as model photosynthetic eukaryotes, 36

specifically the unicellular green alga Chlamydomonas reinhardtii and the diatom Phaeodactylum 37

tricornutum. Finally, we include an examination of some emerging systems. For each organism, the 38

toolbox of genetic parts, high-throughput assembly systems, and other methods that are key 39

components to facilitate synthetic biology are described. Challenges and future directions for 40

synthetic biology and its applications in photosynthetic microorganisms are also discussed. 41



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Photosynthetic micro-organisms: attractive targets for synthetic biology 42

The appearance of microorganisms capable of oxygenic photosynthesis was a turning point in the 43

history of life: they shaped evolution by oxygenating the oceans and the atmosphere (Catling et al., 44

2005; Buick, 2008). A few billion years after the first cyanobacterial-like microbe started splitting 45

water into oxygen and hydrogen, photosynthetic microbes were found in almost every terrestrial 46

ecosystem, from hot springs to arctic ice. Moreover, a cyanobacterium was the likely ancestor of 47

chloroplasts (Jensen and Leister, 2014), an endosymbiosis which was deemed crucial for the 48

colonization of land by plants (Cavalier-Smith, 2010). 49

Photosynthetic microorganisms—specifically, cyanobacteria and algae—offer novel characteristics 50

as synthetic biology hosts. Their unique combination of characteristics, including relatively fast 51

photosynthetic growth, availability of redox power, a plethora of internal membranes, and 52

subcellular microcompartments, opens up a completely new palette of synthetic biology strategies 53

that is not possible in other well-studied heterotrophic host organisms. The photosynthetic 54

machinery is full of interesting targets for synthetic biology strategies (Leister, 2019), such as 55

enhancing photosynthesis for increased biomass production and yield (Zhu et al., 2010), direct 56

coupling of metabolic pathways to photosynthetic reducing power (Mellor et al., 2017), and creation 57

of bio-nano hybrids where photosynthetic modules are used as a source of electrons for non-58

biological processes by linking them to abiotic catalysts or electrode nanomaterials (Saar et al., 2018) 59

or by derivatization of photosynthetic electrons by redox mediators (Longatte et al., 2015; Fu et al., 60

2017). Although in principle such applications can be hosted in plants, photosynthetic 61

microorganisms offer distinct advantages: the combination of photosynthesis with simple unicellular 62

organization, facile genetic manipulation strategies, quick growth in liquid cultures, relative ease of 63

scale-up, and, if grown in contained facilities, potentially fewer regulatory challenges. 64

However, synthetic biology applications in photosynthetic microbes lags behind when compared to 65

model heterotrophs (e.g., Escherichia coli and yeast). One reason is the lack of synthetic biology 66

tools and enabling technologies, which are crucial to achieve their full potential. Fortunately, in 67

recent years, significant advances have rendered synthetic biology applications in algae and 68

cyanobacteria using classical design-build-test cycles more feasible (Figure 1). In its most advanced 69

form, synthetic biology relies on standardization of genetic parts and high-throughput assembly and 70

transformation, the latter of which is far more achievable in photosynthetic microbes than in higher 71

photosynthetic organisms. This perspective provides an overview of recent developments in these 72

areas and identifies some of the challenges facing synthetic biology applications in photosynthetic 73

microbes. 74



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Synthetic biology in cyanobacteria 76

Cyanobacteria are photoautotrophic prokaryotes with fossil records dating back 3.5 billion years, 77

making them the oldest known microbes (Giordano et al., 2005). The cyanobacterial clade is quite 78

diverse; despite the apparent morphological and physiological similarity between different species, 79

extant cyanobacteria may have branched evolutionarily from their last common ancestor more than 80

a billion years ago (Tomitani et al., 2006). Now, in the era of synthetic biology, cyanobacteria have 81

been identified as excellent chassis for microbial cell factories due to their fast growth, small 82

genome size, genetic amenability, and natural transformability. The recently identified 83

Synechococcus elongatus UTEX 2973 strain has one of the fastest growth rates reported for any 84

photosynthetic microbe (Yu et al., 2015; Ungerer et al., 2018); high rates of photosynthesis to 85

produce photosynthates and biomass are required to support this growth. Cyanobacteria are also 86

known for their metabolic flexibility (Xiong et al., 2017), meaning they can thrive in conditions where 87

dramatic fluctuations in nutrient availability, salinity, pH, irradiance, temperature and moisture 88

occur. Thus, cyanobacteria can rapidly acclimate to environmental fluctuations, which is an 89

important characteristic of a robust industrial strain. They can also grow at environmental extremes. 90

For example, Athrospira sp. (‘Spirulina’) are grown successfully in large-scale open ponds at high pH 91

and salt concentrations, conditions that resist invasion from predating and contaminating species 92

(Jiménez et al., 2003). 93

Cyanobacteria have carbon fixation and photosynthesis characteristics that may lead to unique 94

synthetic biology applications. Firstly, carbon fixation takes place in dedicated organelles called 95

carboxysomes. Carboxysomes can be manipulated to host heterologous enzymes, thus generating 96

artificial metabolic microcompartments with a variety of uses (Gonzalez-Esquer et al., 2016). 97

Secondly, photosynthesis does not take place in specialized photosynthetic organelles. This means 98

that their photosynthetic membranes and photosystems therein are more accessible to 99

heterologous proteins. This has enabled the direct linkage of photosynthesis with heterologous 100

metabolic reactions (direct light-driven synthesis) by expression of electron-consuming enzymes 101

(cytochromes P450) in the thylakoid membranes (Berepiki et al., 2016; Wlodarczyk et al., 2016; 102

Mellor et al., 2017). A drawback of the extensive membrane system in cyanobacteria is that our 103

understanding of metabolic regulation through their intermingling respiratory and photosynthetic 104

electron transport chains is incomplete. 105

The most commonly utilized cyanobacteria for basic and applied research are the freshwater 106

unicellular species Synechocystis sp. PCC 6803 and Synechococcus elongatus PCC 7942, the marine 107



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unicellular species Synechococcus sp. PCC 7002, and the nitrogen-fixing filamentous species Nostoc 108

sp. PCC 7120. Synthetic biology applications in cyanobacteria have principally been directed towards 109

metabolic engineering to redistribute photosynthetically fixed carbon towards chemicals of 110

commercial significance. In 1999, the first synthetic metabolic pathway was constructed in 111

Synechococcus elongatus PCC 7942 by introducing Zymomonas mobilis pyruvate decarboxylase (pdc) 112

and alcohol dehydrogenase II (adh) genes to allow ethanol production in this species (Deng and 113

Coleman, 1999). A wealth of subsequent literature describes synthetic biology applications in 114

cyanobacterial metabolic engineering (Nielsen et al., 2016; Matson and Atsumi, 2018; Sengupta et 115

al., 2018). Synthetic biology is also being used to deliver applications other than industrial 116

biochemical production in cyanobacteria. For example, it was recently shown that 3-D printed 117

cyanobacteria could generate and store electricity from light and subsequently power small devices 118

for a limited time (McCormick et al., 2015; Sawa et al., 2017). 119

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Genetic parts 121

Many cyanobacteria (including all of the model species) are naturally transformable and can 122

integrate transgenes into their chromosomes via homologous recombination. Whereas current 123

resources are not as extensive as in heterotrophic model microbes, numerous synthetic components 124

have been characterized for use in cyanobacteria. Vectors and genome editing tools are described in 125

subsequent sections. 126

Promoters and other control elements. Promoters are key synthetic biology components in 127

cyanobacteria (Camsund and Lindblad, 2014; Stensjö et al., 2018); a large selection is available, 128

including constitutive, inducible, and repressible promoters and riboswitches (Ma et al., 2014; 129

Ohbayashi et al., 2016; Videau et al., 2016; Qiao et al., 2017; Immethun and Moon, 2018; Wegelius 130

et al., 2018).A detailed description of the promoter landscape is provided in Box 1, and promoter 131

characteristics summarized in Table 1 for ease of reference. In addition, ribosome binding sites 132

(Englund et al., 2016; Thiel et al., 2018) and riboregulators, which are RNA sequences that respond 133

to signal nucleic acids to modify expression (Abe et al., 2014b), have been characterized. 134

Selectable Markers. Genetic engineering of cyanobacteria is facilitated by antibiotic resistance 135

cassettes. Thus far, resistance to spectinomycin, kanamycin, chloramphenicol, gentamycin, and 136

erythromycin has been used successfully (Eaton-Rye, 2010; Heidorn et al., 2011). Another selection 137

technique that has been applied results in unmarked mutants, and it is based in two consecutive 138

recombination events: the first introduces an antibiotic resistance marker and a sucrose-sensitivity 139

gene (selection on antibiotic), the second replaces the selection markers with the native sequence, 140



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maintaining the transgene (selection on sucrose) (Lea-Smith et al., 2016). This technique is 141

applicable only to cyanobacteria that can grow mixotrophically. For example, Synechocystis sp. PCC 142

6803 and Synechocystis sp. PCC 7002 are naturally mixotrophic, but Synechococcus elongatus UTEX 143

2973 and Synechococcus elongatus PCC 7942 are not. However, mixotrophy can also be engineered, 144

as has been demonstrated in Synechcystis elongatus PCC 7942 (Kanno and Atsumi, 2017). 145

Reporter Genes. Reporter genes are used to illustrate the behavior of genetic parts in a variety of 146

different contexts and are essential to characterize synthetic biology circuits. Bacterial luciferase and 147

fluorescent proteins are most commonly used [reviewed in (Heidorn et al., 2011; Berla et al., 2013)]. 148



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Promoters, characterized using reporter genes, are used for transcriptional regulation. Numerous 149

studies have identified and characterized promoters in cyanobacteria. Cyanobacteria have been 150

classically studied as model photosynthetic organisms and, as a result, several key parts of the 151

synthetic biology toolbox are sourced from photosynthesis genes. The light-inducible promoter 152

driving expression of the D1 subunit of Photosystem II (psbA2) is commonly used, due to strong 153

expression in the light and repression under limited UV (Máté et al., 1998). 154

Heterologous promoters, broadly LacI-repressible and metal-inducible promoters, have also been 155

characterized in cyanobacteria. LacI-inducible promoters, such as ptac and ptrc, are well characterized 156

in eubacteria. However, cyanobacteria have fundamental differences in their transcription 157

machinery (Stensjö et al., 2018); consequently, the same elements behave differently than in other 158

eubacteria [cyanobacteria are part of the eubacteria (Cavalier-Smith, 2010)]. The main distinction is 159

reduced efficiency of repression by LacI, rendering the construction of tightly-controlled on/off 160

transcriptional circuits practically impossible in cyanobacteria (Guerrero et al., 2012; Huang and 161

Lindblad, 2013; Oliver et al., 2013; Camsund and Lindblad, 2014). 162

Inducible promoters are widely used in synthetic biology for intermittent controlled expression. 163

These include promoters activated by increased metal concentration, such as copper, iron, zinc, and 164

nickel, in the growth medium (Briggs et al., 1990; Peca et al., 2008). These promoters show good 165

induction ratios and are useful for experimentation, but are not suitable for large-scale applications 166

due to the cost and the toxicity of the metal ions. A rhamnose-inducible expression system has been 167

developed by Kelly et al. (2018), which combines strong expression and good induction, suitable for 168

synthetic biology applications. Several riboswitches also provide tightly regulated, highly tunable 169

expression systems in cyanobacteria (Ma et al., 2014; Ohbayashi et al., 2016; Immethun and Moon, 170

2018). 171

A very strong, constitutive, synthetic promoter (cpc560) was constructed by combining the high-172

level expression phycocyanin C promoter with 14 transcription factor recognition sequences (Zhou 173

et al., 2014). 174

For expression characteristics of promoters in specific species, see the following references: 175

Synechocystis sp. PCC 6803 (Huang et al., 2010; Huang and Lindblad, 2013; Englund et al., 176

2016; Liu and Pakrasi, 2018; Ferreira et al., 2018) 177

Synechococcus sp. PCC 7002 (Markley et al., 2015; Ruffing et al., 2016; Zess et al., 2016) 178

Synechococcus elongatus PCC 7942 (Ma et al., 2014; Qiao et al., 2017) 179

Synechococcus elongatus UTEX 2973 (Li et al., 2018) 180

Nostoc sp. PCC 712mix0 (Videau et al., 2016; Wegelius et al., 2018) 181

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Vectors and standardized assembly 183

The first shuttle vector that enabled assembly of genetic constructs and expression in several 184

cyanobacteria [using the then-popular BioBricks standard (Shetty et al., 2008)] was reported in 2010 185

(Huang et al., 2010). Standardized genetic assembly paved the way for large-scale development and 186

characterization of parts. The first broad-host cyanobacterial shuttle vector pPMQAK1 (Huang et al., 187

2010), as well as the pDF-trc vector (Guerrero et al., 2012), enabled more streamlined construct 188

generation and strain characterization using restriction-based and isothermal cloning techniques. 189

There are several advantages to using extrachromosomal (ectopic) self-replicating vectors: (1) more 190

efficient transformation using conjugation and electroporation (compared to homologous 191

recombination); (2) avoids the need for time-consuming segregation to achieve incorporation of the 192

transgenic sequence in all copies of the genome; and (3) increased orthogonality of the heterologous 193

sequences, meaning no insertion in genomic loci which may not be neutral. A hybrid strategy that 194

combines the advantages of using a shuttle vector and the stability of genomic insertion involves 195

using native cyanobacterial plasmids, either as insertion sites (Ng et al., 2015) or as true shuttle 196

vectors after isolation and modification (Jin et al., 2018). 197

BioBricks and isothermal assembly techniques are adequate for the generation of a limited number 198

of constructs. However, the automated generation of very large numbers of plasmids and the 199

subsequent streamlined strain generation and characterization requires an alternative approach for 200

genetic assembly. Golden Gate-based techniques, which rely on Type II restriction enzymes (Engler 201

et al., 2008), are more compatible with high-throughput applications. So far, there are two reported 202

Golden Gate toolboxes for cyanobacteria. The first is a streamlined approach for generating 203

constructs either for insertion in the genome or to be incorporated into self-replicating vectors 204

(Taton et al., 2014). This toolkit works in the frequently used model species as well as the Californian 205

species Leptolyngbya sp. BL0902, showing that tools can function across the cyanobacterial phylum. 206

A more recent Golden Gate kit is based on the modular cloning (MoClo; Weber et al., 2011) 207

assembly standard (Vasudevan et al., 2019). This kit contains more than 100 parts for transforming 208

four model cyanobacterial species, including a broad selection of native, heterologous, and synthetic 209

promoters, terminators, linkers, fluorescent makers, antibiotic resistance genes, and more. It also 210

uses the same assembly syntax as the plant and algal MoClo kits, thus making the exchange of parts 211

straightforward. To display the suitability of this kit for high-throughput applications and to 212

characterize promoter/terminator combinations, Vasudevan et al. (2019) used automated assembly 213

to generate more than two hundred constructs. 214



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Genome editing tools 215

A significant development was the implementation of CRISPR-mediated modification systems, 216

including transformation using CRISPR/Cas9 and Cpf1 (Li et al., 2016a; Ungerer and Pakrasi, 2016), 217

and CRISPRi, the latter of which has the potential to provide simultaneous knock-down of multiple 218

genes (Gordon et al., 2016; Wendt et al., 2016; Yao et al., 2016). 219

Challenges and future directions 220

Despite the recent advances, there are several challenges that still limit the synthetic biology 221

potential of cyanobacteria. Cyanobacteria harbour multiple genome copies per cell (Watanabe et al., 222

2015), making the generation of stable transformant lines a slow process that requires extensive 223

segregation to achieve genomic homogeneity. Although homologous recombination is very efficient 224

[requiring as little as 100 bp of overlap for successful transformation (Vogel et al., 2017)], it is 225

difficult to ensure that multiple genes have been edited on the same genome copy. This makes the 226

use of elaborate synthetic biology methods challenging, and sometimes impossible. For example, 227

multiplex automated genome engineering (MAGE; Wang et al., 2009) and its counterpart yeast 228

oligo-mediated genome engineering (DiCarlo et al., 2013), which are very useful in E. coli and yeast 229

for genomic editing; and Synthetic Chromosome Recombination and Modification by LoxP-mediated 230

Evolution (SCRaMbLE), used for accelerated evolution in yeast artificial chromosomes (Dymond and 231

Boeke, 2012), face significant challenges in cyanobacteria due to their genomic redundancy. 232

Whereas CRISPR systems are available (see above), CRISPR-mediated marker-free and multiplex 233

transformation have not yet been achieved in cyanobacteria. A marker-free transformation system 234

has been reported, based on SacB toxicity in the presence of sucrose; however, this system relies on 235

two rounds of segregation—thus obtaining unmarked colonies after a couple of months—and works 236

only on cyanobacteria that can grow mixotrophically (Lea-Smith et al., 2016). 237

Success in synthetic biology applications often requires reasonably solid understanding of the target 238

biological system. However, the metabolism of cyanobacteria remains only partly elucidated. This is 239

particularly problematic for modelling, as it interferes with the predictive capability of models. More 240

reactions and major metabolic routes are being discovered even in model species (Xiong et al., 2015; 241

Chen et al., 2016; Zhang et al., 2018), whereas key regulation mechanisms remain more or less 242

unknown (Vavitsas et al., 2017; Stensjö et al., 2018). Pioneering work in understanding 243

cyanobacterial metabolism, such as the use of transposon libraries to determine essential and 244

beneficial genes (Rubin et al., 2015), as well as advances in metabolic modelling (Nogales et al., 245

2012; Knoop et al., 2013; Broddrick et al., 2016; Abernathy et al., 2017) provide essential tools for 246

studying metabolism. Good knowledge and careful manipulation of metabolism have been proven 247



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essential for metabolic engineering applications, as displayed in the production of isoprene (titer: 248

1.26 g/L) and 2,3-butanediol (titer: 12.6 g/L) in Synechococcus elongatus PCC 7942 (Gao et al., 2016; 249

Kanno et al., 2017). 250

Synthetic biology in eukaryotic algae 251

Eukaryotes present distinct advantages compared to prokaryotes for synthetic biology. This includes 252

the existence of membrane-enclosed organelles that allow exploitation of separated cellular 253

compartments (Polka et al., 2016), thus permitting the engineering of channeling and 254

compartmentalization of metabolism to enhance overall production rates and limit side reactions for 255

metabolic engineering applications. The existence of multiple genetic systems in eukaryotes 256

(nucleus, mitochondria, and chloroplasts) can also offer new design possibilities and allows 257

exploration of the coordination between the compartments, which plays a major role in numerous 258

fundamental cellular processes and is especially crucial for photosynthesis and respiration. The main 259

eukaryotic chassis are baker’s yeast and mammalian cells (Adams, 2016). In the case of 260

photosynthetic eukaryotes, synthetic biology tools have been developed for Arabidopsis thaliana 261

and Marchantia polymorpha (Boehm et al., 2017); however, unicellular chassis have only emerged 262

recently. Many eukaryotic algal genomes have been sequenced (data from NCBI Genome: 64 Green 263

Algae, 9 Red algae, 9 Diatoms, 5 Dinoflagellates, 3 Brown algae). Several industrial hosts of different 264

phyla (Brodie et al., 2017) are used for biotechnology or metabolic engineering applications, 265

including Nannochloropsis sp. (Poliner et al., 2018) and diverse green algae (Scaife and Smith, 2016), 266

such as Dunaliella salina (Feng et al., 2014) and Chlorella sp. (Yuan et al., 2018). Nevertheless, most 267

of these organisms are not yet amenable to advanced synthetic biology approaches, which require 268

robust genetic tools, reliable parts, standardized high-throughput construction, and advanced 269

molecular biology techniques (Hlavova et al., 2015). Two model organisms are therefore rising as 270

interesting chassis: the unicellular green alga Chlamydomonas reinhardtii (herein referred to as 271

Chlamydomonas) and the diatom Phaeodactylum tricornutum (Nguyen et al., 2016). Both are easily 272

cultivated even at moderate to large scale (Posten, 2009) and can be transformed efficiently, with 273

known physiology and available systems-wide datasets (genome, transcriptomics, proteomics, 274

metabolomics; Scaife and Smith, 2016). Synthetic biology may allow these two model organisms to 275

become industrial hosts (Scaife et al., 2015), and the knowledge and tools developed might also be 276

applicable to other algal species (Doron et al., 2016). 277

Genetic parts 278

Many genetic elements have been characterized in, or adapted to, microalgae. Several recent 279

reviews have been published on algal synthetic biology and chloroplast genome modification (Doron 280



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et al., 2016; Scaife and Smith, 2016; Dyo and Purton, 2018; Poliner et al., 2018). Therefore, we will 281

focus here on new developments and on nuclear genetic elements. 282

Promoters and terminators. Numerous genetic parts are available for the control of gene expression 283

including diverse inducible, repressible and constitutive promoters and multiple 3′UTR/terminators 284

(Ohresser et al., 1997; Schroda et al., 2000; Fischer and Rochaix, 2001; Ferrante et al., 2008; Helliwell 285

et al., 2014; Sawyer et al., 2015; Baek et al., 2016; Lee et al., 2018; Watanabe et al., 2018; Beltran-286

Aguilar et al., 2019). The promoters are detailed in Box 2. Available nuclear 3′UTR/terminators are 287

derived from various genes such as PSAD, RBCS2, RPS29, CA1, TUB2, or RPL23 (Crozet et al., 2018). 288

Interestingly, in the context of a small transgene expressing the nanoluciferase reporter, the 289

3′UTR/terminator was found to have a stronger impact than the promoter on global expression, 290

when comparing PSAD and AR/RBCS2 promoter and terminator elements (Crozet et al., 2018). 291

Further studies will be required to precisely assess the impact of multiple combinations of genetic 292

elements on gene expression. 293

Post-transcriptional control tools. Coordinated transcription of multiple genes can be achieved 294

through use of the foot-and-mouth-disease-virus 2A peptide, which allows cistron-like gene 295

expression in eukaryotes and was found to be functional in Chlamydomonas (Rasala et al., 2012; 296

Plucinak et al., 2015; Lopez-Paz et al., 2017). To control gene expression post-transcriptionally, two 297

other versatile genetic parts were characterized: riboswitches and artificial microRNA. Riboswitches 298

are RNA sensors that bind small molecules and in turn regulate gene expression (Nguyen et al., 299

2016). These regulatory elements are particularly interesting for synthetic biology as they are 300

modular with an aptamer part that recognizes the ligand and an expression platform that controls 301

the expression. This modularity and the knowledge of the design rules of riboswitches make them 302

primed for engineering (Hallberg et al., 2017). The THI4 riboswitch identified in Chlamydomonas 303

responds to vitamin B1 and can be used to control the expression of any gene (Croft et al., 2007; 304

Moulin et al., 2013; Crozet et al., 2018). Artificial microRNA (amiRNA) is based on the endogenous 305

microRNA machinery that controls gene expression post-transcriptionally (Rogers and Chen, 2013). 306

This complex machinery was identified in Chlamydomonas (Molnar et al., 2007) and now it is 307

possible to design amiRNA that can repress the expression of any gene in a sequence-dependent 308

manner (Molnar et al., 2009). 309

Selection systems. Several antibiotic resistance genes are available in Chlamydomonas, including the 310

newly developed sulfadiazine resistance gene (Tabatabaei et al., 2019) and the well-established 311

selectable marker genes conferring resistance to paromomycin, hygromycin, spectinomycin, 312

kanamycin, and zeocin. Most of these genes are functional in numerous other algal species (Doron 313



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et al., 2016; Poliner et al., 2018). In addition, the Nourseothricin resistance gene (Nat) is routinely 314

used in P. tricornutum (Zaslavskaia et al., 2001), and very recently a novel selection marker, namely 315

the Blasticidin-S resistance gene (encoding Blasticidin-S-deaminase), was added to the diatom 316

toolbox (Buck et al., 2018). 317

Reporter genes. A set of reporter genes are also available, including fluorescent proteins and diverse 318

luciferases (Lauersen et al., 2015; Huang and Daboussi, 2017), which can be targeted in 319

Chlamydomonas to most compartments thanks to a collection of targeting peptides (Lauersen et al., 320

2015). Recently, the very sensitive and highly stable Nanoluciferase (Hall et al., 2012) was adapted to 321

Chlamydomonas (Crozet et al., 2018). 322

Parts for other eukaryotic microalgae. Although less diverse, genetic parts including promoters, 323

reporters and targeting peptides have been developed for other diatoms (Apt et al., 1996; 324

Rosenwasser et al., 2014; Chu et al., 2016; Doron et al., 2016; Huang and Daboussi, 2017) and for the 325

Nannochloropsis genus (Poliner et al., 2018). 326

Vectors and standardized assembly 327

The pOptimized vector collection provided the first step towards standardized genetic tools in 328

Chlamydomonas, including several reporter genes and a collection of targeting peptides with each 329

gene part flanked by unique restriction sites (Lauersen et al., 2015). This toolkit is standardized but 330

still lacks the modularity of modern cloning methodologies. More recently, we participated in the 331

development of the first Modular Cloning (MoClo) toolkit for Chlamydomonas (Crozet et al., 2018). It 332

is based on standardized golden gate cloning (Engler et al., 2008) and allows rapid and standardized 333

assembly of genes and multigenic constructs (Weber et al., 2011). Most of the genetic resources 334

cited above were standardized, validated and are openly distributed to the community (Crozet et al., 335

2018). The kit comprises 119 genetic parts, including 7 promoters, 7 5′UTRs, the CrTHI4 riboswitch, 8 336

immunological or purification tags, 9 signal/targeting peptides, 12 reporter genes, 5 antibiotic 337

resistance genes, the 2A peptide, 2 microRNA (miRNA) backbones and associated controls, and 6 3′ 338

UTR/terminators. This toolkit enables rapid building of engineered cells for both fundamental 339

research and algal biotechnology. To make Chlamydomonas and other algae easier to engineer, we 340

invite our readers to follow the proposed standard (Patron et al., 2015; Crozet et al., 2018) and to 341

share their parts openly. A molecular toolbox was created for diatoms using the Gateway standard 342

(Heijde et al., 2007). More recently, D’Adamo and colleagues used the MoClo (Weber et al., 2011) 343

and its Plant standard (Patron et al., 2015) to build plasmids later successfully used to transform P. 344

tricornutum (D’Adamo et al., 2019). 345



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A recent breakthrough in diatoms was the design of an artificial circular chromosome delivered via 346

bacterial conjugation to P. tricornutum and Thalassiosira pseudonana (Karas et al., 2015; Diner et al., 347

2017). 348

Genome editing tools 349

A recent breakthrough was the development of genome editing through Zn-Finger Nucleases, 350

Transcription Activator-Like Effector Nuclease (TALEN) and CRISPR/Cas9 for different eukaryotic 351

algae. TALENs were successfully used for P. tricornutum (Weyman et al., 2015; Serif et al., 2018), 352

whereas Zn-finger nucleases were developed for Chlamydomonas (Sizova et al., 2013; Greiner et al., 353

2017). CRISPR/Cas9 genome editing was achieved in Chlamydomonas (Shin et al., 2016; Greiner et 354

al., 2017), P. tricornutum (Nymark et al., 2016; Serif et al., 2018; Slattery et al., 2018), and T. 355

pseudonana (Hopes et al., 2016). In Chlamydomonas, efficient genome editing was also achieved 356

through the Cpf1 single-stranded DNA-dependent nuclease (Ferenczi et al., 2017). In the case of 357

Chlamydomonas, a library of mapped mutants generated through insertional mutagenesis is a useful 358

resource for reverse genetics (Li et al., 2016b). A very recent study reported that DNA integration 359

through homologous recombination was enabled through a knock-down of a LigIV homolog, thus 360

decreasing the NHEJ in profit of Homologous Recombination (HR) (Angstenberger et al., 2019). 361

Challenges and future directions 362

The development of all the tools described above is nourishing synthetic biology in photosynthetic 363

eukaryotes, and is particularly useful for metabolic engineering applications. Several successes were 364

achieved in recent years, such as the production of terpenes in Chlamydomonas (Lauersen et al., 365

2016; Wichmann et al., 2018) and P. tricornutum (D’Adamo et al., 2019), and other compounds such 366

as alkanes in Chlamydomonas (Sorigue et al., 2016; Yunus et al., 2018) and astaxanthin in D. salina 367

(Anila et al., 2016). Synthetic biology of microalgae is not exclusively restricted to metabolic 368

engineering. For example, the possibility to harness photosynthesis to generate electrical power is 369

currently being considered. Extraction of photocurrents from photosystem II using exogenous 370

quinone as a redox mediator was investigated (Longatte et al., 2015; Longatte et al., 2016). The 371

redesign of the QA binding site of Chlamydomonas allowed reduction of exogenous quinones (Fu et 372

al., 2017) and this strategy provided, 10–60 µA/cm-2 for 1 hour on a high surface electrode (Longatte 373

et al., 2018). 374

Despite all the recent advances enabling synthetic biology in eukaryotic algae, some challenges 375

remain. Some of these challenges relate to the relatively recent development of photosynthetic 376

microorganisms as model chassis for engineering. Relative to more established heterotrophic 377

microbes, there are fewer genetic components and they are not as well characterized. In particular, 378



14

whereas transcriptional characteristics in cyanobacteria that are relevant for metabolic engineering 379

applications have recently been reviewed (Stensjö et al., 2018), much more work is needed to 380

characterize promoters, especially the commonly used light-responsive promoters. Moreover, non-381

modularity in expression (commonly observed when promoters are coupled with different gene 382

sequences) is not well understood. These are important considerations for true standardization of 383

components, required for predictability and reproducibility of synthetic biology approaches in 384

photosynthetic microbes. More extensive characterization of componentry is required to improve 385

their utility and application in photosynthetic microbes for synthetic biology projects. 386

Expression of transgenes is often problematic since they are randomly integrated in the genome, 387

leading to multiple insertions, gene knockout, position effects and long-term silencing. It should be 388

possible in the future to solve some of these issues using, as in mammals, a landing pad for 389

transgene insertion through site-specific recombination flanked by insulators (Raab and Kamakaka, 390

2010; Duportet et al., 2014). Another solution might be to use the recently published strategy 391

demonstrated in the model diatom P. tricornutum in other algae, which allows a shift in the balance 392

of DNA repair from NHEJ to HR (Angstenberger et al, ACS Synth Biol, 2018 DOI 393

10.1021/acssynbio.8b00234). Low transgene expression, which is often problematic in 394

Chlamydomonas, was recently circumvented using introns (Baier et al., 2018; Wichmann et al., 395

2018). It could also be improved by targeting specific loci known to be stable and highly expressed. 396

The recently-developed diatom artificial circular chromosome (Karas et al., 2015; Diner et al., 2017) 397

could allow genome engineering without random integration in native chromosomes. This paves the 398

way for the next frontier in algal engineering, which is certainly the (re)design of natural 399

chromosomes or entire genomes as in yeast (Richardson et al., 2017). 400

Beyond molecular tools, algal synthetic biology will require the development of single cell 401

approaches and automation based on microfluidics (Best et al., 2016; Kim et al., 2016) and robotized 402

platforms for DNA assembly, strain handling and phenotyping to allow high-throughput building and 403

testing of advanced designs, possibly improved through directed evolution. 404

Concluding remarks 405

Photosynthetic microorganisms represent attractive chassis for synthetic biology applications, and 406

significant recent advances demonstrate their potential. However, there are some challenges that 407

remain to be overcome and opportunities yet to be exploited in order to realize this potential (see 408

Outstanding Questions). 409

Current research is focused on only a few model species; there is enormous diversity yet to be 410

tapped in photosynthetic microorganism clades. Even in model species, metabolic processes are not 411



15

fully elucidated and therefore cannot be fully exploited. Other valuable chassis organisms and 412

component sources are waiting to be discovered. Cyanobacteria are clearly the front runner in terms 413

of model prokaryotic photosynthetic microorganisms, but their multiple genome copies slows the 414

production of stable transformants and creates barriers for the development and application of 415

some valuable synthetic biology tools. For both prokaryotes and eukaryotes, random integration 416

presents problems in control and predictability of transgene behavior; mechanisms for more precise 417

control of insertion and expression are required. 418

Going forwards, further development of standardized parts, high-throughput assembly systems, and 419

other synthetic biology methods will be required. Toolboxes remain limited in eukaryotic systems, 420

particularly for the diatom P. tricornutum, which has emerged even more recently as a model. An 421

improved understanding of the biology and physiology of photosynthetic microorganisms will 422

improve our ability to develop and apply synthetic biology tools. 423

For microbial cell factory/metabolic engineering applications, production rate, yield, and titer are 424

critical, especially for high volume, low value products (Vickers et al., 2010). Photosynthesis is not an 425

efficient process, although recent impressive advances in engineering to improve photosynthetic 426

efficiency can deliver significant photosynthetic yield benefits (South et al., 2019). Converting this 427

fixed carbon into improved yields, and increasing rates and titers, remain challenges for many 428

products, including fuels and commodity biochemicals, which are particularly attractive for 429

photosynthetic systems compared to high value/low volume products where the technoeconomic 430

evaluation may return more positively in systems that are easier to engineer. Solving these 431

challenges will require significant engineering and application of clever synthetic biology tools. For 432

practical application, the potential to use non-arable land for production and to deploy engineered 433

organisms in extreme environments are both attractive. Photoautotrophic production may be 434

required for applications in desert and extra-planetary (i.e. beyond Earth) environments (Llorente et 435

al., 2018). Achieving sufficient light penetration into cultures without loss of the growth medium 436

(especially in high-density cultures required for high titers) also represents a challenge in bulk 437

production systems. Mixotrophic growth, while failing to fully exploit the free carbon and energy 438

available through photosynthesis, improves growth rates and yields in cyanobacteria (Kanno and 439

Atsumi, 2017; Matson and Atsumi, 2018) and may be required to reach maximum potential. An 440

under-developed opportunity for metabolic engineering applications is the use of consortia, where a 441

photosynthetic microbe provides the sugar or other carbon source for a heterotroph that acts as the 442

production platform (Ducat et al., 2012; Fedeson and Ducat, 2017; Ramos-Martinez et al., 2017). 443

This provides the benefits of both photoautotrophy and engineerability. 444



16

More broadly, expanding applications where photosynthetic microorganisms provide key 445

advantages beyond microbial cell factories is an attractive option. Microbial fuel cells for energy 446

storage, exploiting paired autotrophy and extremophile capabilities for bespoke applications such as 447

environmental remediation, and engineered symbiosis for applications such as nitrogen fixation, are 448

likely future targets. 449

450

Acknowledgements 451

KV was supported by a CSIRO Synthetic Biology Future Science Fellowship and by the European 452

Union and Greek national funds through the Operational Program "Competitiveness, 453

Entrepreneurship and Innovation", under the call “RESEARCH-CREATE-INNOVATE” (project 454

code:15282). MHV was supported by a CSIRO PhD Top-Up Scholarship. CEV was supported by the 455

CSIRO-UQ Synthetic Biology Alliance. This work was supported in part by Agence Nationale de la 456

Recherche Grant ANR-17-CE05-0008 and LABEX DYNAMO ANR-LABX-011. 457

458

Tables 459

460

461

Table 1. Overview of cyanobacterial promoters

Characteristics Example References

Constitutive Pcpc560 (Huang et al., 2010; Zhou et al., 2014; Englund et al., 2016;

Ruffing et al., 2016; Ferreira et al., 2018; Li et al., 2018; Liu

and Pakrasi, 2018)

Inducible

CO2 PcpcB (Sengupta et al., 2019)

Cobalt PcoaT (Peca et al., 2008; Guerrero et al., 2012; Englund et al., 2016)

Copper PpetE (Briggs et al., 1990; Guerrero et al., 2012; Englund et al., 2016)

Green-light PcpcG2 (Abe et al., 2014a)

Heavy metals Psmt (Guerrero et al., 2012)

Light PpsbA2 (Englund et al., 2016; Li et al., 2018)

Nickel PnrsB (Peca et al., 2008; Englund et al., 2016)

Nitrite PnirA (Qi et al., 2005)

Rhamnose PrhaBAD (Kelly et al., 2018)

UV-B PpsbA3 (Máté et al., 1998)

Zinc PziaA (Peca et al., 2008; Englund et al., 2016)

Repressible

CO2 Prbc (Sengupta et al., 2019)

High light intensity PcpcB (Sengupta et al., 2019)



17

LacI

(IPTG Inducible)

Ptrc (Huang et al., 2010; Guerrero et al., 2012; Oliver et al., 2013;

Markley et al., 2015; Ferreira et al., 2018; Li et al., 2018)

TetR

(aTc Inducible)

L03 (Huang and Lindblad, 2013; Zess et al., 2016; Ferreira et al.,

2018)

462

463

Figure legends 464

465

Figure 1: Design-Build-Test cycle using photosynthetic microorganisms. Recent technologies have 466

expanded the capabilities and throughput of this cycle by providing improved tools and design 467

options, greater build capacity, and more efficient and informative strain characterization. Overview 468

of modular cloning system based on that in Weber et al. (2011). 469

470

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ADVANCES

• New synthetic biology advances in photosynthetic microorganisms are aimed at making genetic engineering more facile and offer more options for applications. A key factor for the successful establishment of photosynthetic microbes as synthetic biology hosts is the development of standardized circuits and techniques.

• New tools such as artificial circular chromosomes for more controlled assembly and expression, modular cloning kits, component libraries, and genome editing tools are accelerating development of applications in photosynthetic microorganisms

• The increasing availability of genome sequences and genome scale models can be exploited for identification and harvesting of useful genetic components



OUTSTANDING QUESTIONS

• What genetic diversity are we missing by focusing on relatively few model photosynthetic microorganisms, and how do we most easily access it for new chassis organisms and circuits? Will expansion into new organisms come at the expense of needed development in current chassis?

• Can the problems resulting from multiple genome copies in cyanobacteria be overcome using novel technologies?

• Can new mechanisms for precise control of transgene insertion and expression be developed?

• For metabolic engineering applications, which engineered processes and products will provide the rates, yields and titers required for economic viability? Which outcomes can be delivered in a short time frame, and which will require sustained long-term investment?

• For other applications, where else will photosynthetic microorganisms shine compared to more easily-engineered model systems?



BOX 1. Promoters for cyanobacterial synthetic

biology

Promoters, characterized using reporter genes, are used for transcriptional regulation. Numerous studies have identified and characterized promoters in cyanobacteria. Cyanobacteria have been classically studied as model photosynthetic organisms and, as a result, several key parts of the synthetic biology toolbox are sourced from photosynthesis genes. The light-inducible promoter driving expression of the D1 subunit of Photosystem II (psbA2) is commonly used, due to strong expression in the light and repression under limited UV (Máté et al., 1998)

Heterologous promoters, broadly LacI-repressible and metal-inducible promoters, have also been characterized in cyanobacteria. LacI-inducible promoters, such as ptac and ptrc, are well characterized in eubacteria. However, cyanobacteria have fundamental differences in their transcription machinery (Stensjö et al., 2018); consequently, the same elements behave differently than in other eubacteria [cyanobacteria are part of the eubacteria (Cavalier-Smith, 2010)]. The main distinction is reduced efficiency of repression by LacI, rendering the construction of tightly-controlled on/off transcriptional circuits practically impossible in cyanobacteria (Guerrero et al., 2012; Huang and Lindblad, 2013; Oliver et al., 2013; Camsund and Lindblad, 2014).

Inducible promoters are widely used in synthetic biology for intermittent controlled expression. These include promoters activated by increased metal concentration, such as copper, iron, zinc, and nickel, in the growth medium (Briggs et al., 1990; Peca et al., 2008).

These promoters show good induction ratios and are useful for experimentation, but are not suitable for large-scale applications due to the cost and the toxicity of the metal ions. A rhamnose-inducible expression system has been developed by Kelly et al. (2018), which combines strong expression and good induction, suitable for synthetic biology applications. Several riboswitches also provide tightly regulated, highly tunable expression systems in cyanobacteria (Ma et al., 2014; Ohbayashi et al., 2016; Immethun and Moon, 2018).

A very strong, constitutive, synthetic promoter (cpc560) was constructed by combining the high-level expression phycocyanin C promoter with 14 transcription factor recognition sequences (Zhou et al., 2014).

For expression characteristics of promoters in specific species, see the following references:

• Synechocystis sp. PCC 6803 (Huang et al., 2010; Huang and Lindblad, 2013; Englund et al., 2016; Liu and Pakrasi, 2018; Ferreira et al., 2018)

• Synechococcus sp. PCC 7002 (Markley et al., 2015; Ruffing et al., 2016; Zess et al., 2016)

• Synechococcus elongatus PCC 7942 (Ma et al., 2014; Qiao et al., 2017)

• Synechococcus elongatus UTEX 2973 (Li et al., 2018)

• Nostoc sp. PCC 712mix0 (Videau et al., 2016; Wegelius et al., 2018)



BOX 2. Promoters for eukaryotic algae synthetic

biology

Promoters are usually seen as the key genetic element

controlling gene expression. Despite the absolute

requirement of a promoter to recruit RNA polymerase,

other genes parts, including the untranslated regions

(UTRs) and terminators, also contribute to the

regulation of gene expression, ultimately leading to

fine-tuning of protein abundance in vivo.

In Chlamydomonas, these other gene parts used to

influence expression include regulatory sequences from

the PSAD gene (Fischer and Rochaix, 2001) and the

chimeric promoter HSP70A-RBCS2 and the RBCS2

terminator (Schroda et al., 2000) for strong constitutive

expression, as well as the NIT1 (Ohresser et al., 1997) or

METE (Helliwell et al., 2014) promoters, which are

repressible by ammonium and vitamin B12, respectively.

Three inducible promoters are known: the CYC6

promoter induced by nickel and also repressed by

copper (Ferrante et al., 2008), the sulfur starvation-

induced promoter of LHCBM9 (Sawyer et al., 2015), and

the Dunaliella LIP promoter that is light-inducible and

functional in Chlamydomonas (Baek et al., 2016).

Recent reports added two new inducible promoters to

the toolbox: a salt-inducible promoter from CrGPDH3

(Beltran-Aguilar et al., 2019) and the alcohol-inducible

promoter recently adapted from the fungus Aspergillus

nidulans (Lee et al., 2018). The latter requires the

specific transcription factor alcR and may be coupled to

another input to generate a logic gate, which should

enable more complex design of genetic circuits. In

diatoms, several promoters were developed including

constitutive or inducible ones (Huang and Daboussi,

2017). Very recently, a new promoter, namely the

endogenous V-ATPase C promoter, was isolated for

driving high level expression of transgenes in

Phaeodactylum tricornutum (Watanabe et al., 2018).



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https://www.ncbi.nlm.nih.gov/pubmed?term=Gao X%2C Gao F%2C Liu D%2C Zhang H%2C Nie X%2C Yang C %282016%29 Engineering the methylerythritol phosphate pathway in cyanobacteria for photosynthetic isoprene production from CO 2%2E Energy Environ Sci 9%3A 1400%26%23x&dopt=abstract

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https://scholar.google.com/scholar?as_q=Tailored carbon partitioning for phototrophic production of ( E )-�?±-bisabolene from the green microalga Chlamydomonas reinhardtii.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wichmann&as_ylo=2018&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Wlodarczyk A%2C Gnanasekaran T%2C Zygadlo A%2C Nokolunga N%2C Busck S%2C Luckner M%2C Frederik J%2C Th�fner B%2C Erik C%2C Saddik M%2C et al %282016%29 Metabolic engineering of light%2Ddriven cytochrome P450 dependent pathways into Synechocystis sp %2E PCC 6803%2E Metab Eng 33%3A 1%26%23x&dopt=abstract

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https://scholar.google.com/scholar?as_q=Metabolic engineering of light-driven cytochrome P450 dependent pathways into Synechocystis sp .&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wlodarczyk&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Xiong W%2C Cano M%2C Wang B%2C Douchi D%2C Yu J %282017%29 The plasticity of cyanobacterial carbon metabolism%2E Curr Opin Chem Biol 41%3A 12%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Xiong W%2C Lee T%2DC%2C Rommelfanger S%2C Gjersing E%2C Cano M%2C Maness P%2DC%2C Ghirardi M%2C Yu J %282015%29 Phosphoketolase pathway contributes to carbon metabolism in cyanobacteria%2E Nat Plants&dopt=abstract

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https://scholar.google.com/scholar?as_q=Phosphoketolase pathway contributes to carbon metabolism in cyanobacteria.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Xiong&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Yao L%2C Cengic I%2C Anfelt J%2C Hudson EP %282016%29 Multiple Gene Repression in Cyanobacteria Using CRISPRi%2E ACS Synth Biol 5%3A 207%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Yu J%2C Liberton M%2C Cliften PF%2C Head RD%2C Jacobs JM%2C Smith RD%2C Koppenaal DW%2C Brand JJ%2C Pakrasi HB %282015%29 Synechococcus elongatus UTEX 2973%2C a fast growing cyanobacterial chassis for biosynthesis using light and CO2%2E Sci Rep&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Yuan Y%2C Liu H%2C Li X%2C Qi W%2C Cheng D%2C Tang T%2C Zhao Q%2C Wei W%2C Sun Y %282018%29 Enhancing Carbohydrate Productivity of Chlorella sp%2E AE10 in Semi%2Dcontinuous Cultivation and Unraveling the Mechanism by Flow Cytometry%2E Appl Biochem Biotechnol 185%3A 419%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Yunus IS%2C Wichmann J%2C W�rdenweber R%2C Lauersen KJ%2C Kruse O%2C Jones PR %282018%29 Synthetic metabolic pathways for photobiological conversion of CO 2 into hydrocarbon fuel%2E Metab Eng 49%3A 201%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Zaslavskaia LA%2C Lippmeier JC%2C Kroth PG%2C Grossman AR%2C Apt KE %282001%29 Transformation of the diatom Phaeodactylum tricornutum %28Bacillariophyceae%29 with a variety of selectable marker and reporter genes%2E J Phycol 36%3A 379%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Zess EK%2C Begemann MB%2C Pfleger BF %282016%29 Construction of New Synthetic Biology Tools for the Control of Gene Expression in the Cyanobacterium Synechococcus sp Strain PCC 7002%2E Biotechnol Bioeng 113%3A 424%26%23x&dopt=abstract

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https://scholar.google.com/scholar?as_q=Construction of New Synthetic Biology Tools for the Control of Gene Expression in the Cyanobacterium Synechococcus sp Strain PCC 7002.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zess&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhang H%2C Liu Y%2C Nie X%2C Liu L%2C Hua Q%2C Zhao GP%2C Yang C %282018%29 The cyanobacterial ornithine%2Dammonia cycle involves an arginine dihydrolase article%2E Nat Chem Biol 14%3A 575%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Zhou J%2C Zhang H%2C Meng H%2C Zhu Y%2C Bao G%2C Zhang Y%2C Li Y%2C Ma Y %282014%29 Discovery of a super%2Dstrong promoter enables efficient production of heterologous proteins in cyanobacteria%2E Sci Rep&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Zhu X%2DG%2C Long SP%2C Ort DR %282010%29 Improving Photosynthetic Efficiency for Greater Yield%2E Annu Rev Plant Biol 61%3A 235%26%23x&dopt=abstract

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The synthetic biology toolkit for photosynthetic ... · 111 commercial significance. In 1999, the...

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