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Transporters Related to Stress Responses and Their Potential Application in Synechocystis sp. PCC 6803

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Synthetic Biology of Cyanobacteria

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1080))

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Abstract

Cyanobacteria are autotrophic prokaryotes that can perform oxygenic photosynthesis. The conversion of light and carbon dioxide into green fuels and chemicals has drawn considerable interest, and several dozen products have been successfully synthesized in genetically engineered cyanobacteria. However, during cultivation, cyanobacterial cells are typically exposed to various stresses from the environment, such as acid, salt and metal stresses, as well as from the end products they synthesize, such as ethanol, butanol, and 3-hydroxypropionic acid (3-HP). These stresses hinder the accumulation of biomass and the production of chemicals or biofuels in cyanobacteria. Thus, improving the ability of cyanobacterial cells to resist stress can potentially enhance the robustness of the cyanobacterial chassis and the final yield of the target products. Toward this goal, research has been performed to explore the mechanisms by which cyanobacteria respond to various environmental perturbations and product toxicity. Among these mechanisms, transporters are membrane proteins involved in the transportation of ions, small molecules, or macromolecules across the membrane, and they have been reported to be involved in the response to common stresses in many organisms. Thus, engineering transporter-encoding genes may be a promising solution to increase the resistance of the cells against biotic and abiotic stresses. This chapter focuses on recent progress on the use of transporters related to stress responses in the model cyanobacterium Synechocystis sp. PCC 6803 and presents an updated review of their functions in stress regulation and their potential application in future chassis modifications.

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Abbreviations

Ac-COA:

AcetylcoenzymeA

ADP:

Adenosine-5′-diphosphate

ADP-GCS:

Adenosine-5′-diphosphoglucose

ADP-glucose:

Adenosine-5′-diphosphoglucose

ATP:

Adenosine-5′-triphosphate

DHAP:

Dihydroxyacetone phosphate

F6P:

d-fructose 6-phosphate

FBP:

d-fructose 1, 6-bisphosphate

G6P:

d-glucose 6-phosphate

GAP:

dl-glyceraldehyde 3-phosphate

GC-MS:

Gas chromatography-mass spectrometry

LC-MS:

Liquid chromatography-mass spectrometry

NADH:

Nicotinamide adenine dinucleotide

NADP/NADPH:

Nicotinamide adenine dinucleotide phosphate

PCA:

Principal component analysis

PCR:

Polymerase chain reaction

R5P:

d-ribose5-phosphate

RT-qPCR:

Real-time quantitative polymerase chain reaction

UDP-glucose:

Uridine 5′-diphosphoglucose

WGCNA:

Weighted correlation network analysis

References

  1. Adrio JL (2017) Oleaginous yeasts: promising platforms for the production of oleochemicals and biofuels. Biotechnol Bioeng 114(9):1915–1920. https://doi.org/10.1002/bit.26337

    Article  PubMed  CAS  Google Scholar 

  2. Matsumoto T, Tanaka T, Kondo A (2017) Engineering metabolic pathways in Escherichia coli for constructing a “microbial chassis” for biochemical production. Bioresour Technol 245(Pt B):1362–1368. https://doi.org/10.1016/j.biortech.2017.05.008

    Article  PubMed  CAS  Google Scholar 

  3. Minton NP, Ehsaan M, Humphreys CM, Little GT, Baker J, Henstra AM, Liew F, Kelly ML, Sheng L, Schwarz K, Zhang Y (2016) A roadmap for gene system development in Clostridium. Anaerobe 41:104–112. https://doi.org/10.1016/j.anaerobe.2016.05.011

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Somerville C, Youngs H, Taylor C, Davis SC, Long SP (2010) Feedstocks for lignocellulosic biofuels. Science (New York, NY) 329(5993):790–792. https://doi.org/10.1126/science.1189268

    Article  CAS  Google Scholar 

  5. Flombaum P, Gallegos JL, Gordillo RA, Rincon J, Zabala LL, Jiao N, Karl DM, Li WK, Lomas MW, Veneziano D, Vera CS, Vrugt JA, Martiny AC (2013) Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus. Proc Natl Acad Sci U S A 110(24):9824–9829. https://doi.org/10.1073/pnas.1307701110

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Knoot CJ, Ungerer JL, Wangikar PP, Pakrasi HB (2017) Cyanobacteria: promising biocatalysts for sustainable chemical production. J Biol Chem. https://doi.org/10.1074/jbc.R117.815886

  7. Koksharova OA, Wolk CP (2002) Genetic tools for cyanobacteria. Appl Microbiol Biotechnol 58(2):123–137. https://doi.org/10.1007/s00253-001-0864-9

    Article  PubMed  CAS  Google Scholar 

  8. Stanier RY, Cohen-Bazire G (1977) Phototrophic prokaryotes: the cyanobacteria. Annu Rev Microbiol 31(1):225–274. https://doi.org/10.1146/annurev.mi.31.100177.001301

    Article  PubMed  CAS  Google Scholar 

  9. Wang B, Pugh S, Nielsen D, Zhang W, Meldrum D (2013a) Engineering cyanobacteria for photosynthetic production of 3-hydroxybutyrate directly from CO2. Metab Eng 16:68–77. https://doi.org/10.1016/j.ymben.2013.01.001

    Article  PubMed  CAS  Google Scholar 

  10. Gao Z, Zhao H, Li Z, Tan X, Lu X (2012) Photosynthetic production of ethanol from carbon dioxide in genetically engineered cyanobacteria. Energy Environ Sci 5(12):9857–9865. https://doi.org/10.1039/C2EE22675H

    Article  CAS  Google Scholar 

  11. Wang Y, Sun T, Gao X, Shi M, Wu L, Chen L, Zhang W (2016) Biosynthesis of platform chemical 3-hydroxypropionic acid (3-HP) directly from CO2 in cyanobacterium Synechocystis sp. PCC 6803. Metab Eng 34:60–70. https://doi.org/10.1016/j.ymben.2015.10.008

    Article  PubMed  CAS  Google Scholar 

  12. Hirokawa Y, Suzuki I, Hanai T (2015) Optimization of isopropanol production by engineered cyanobacteria with a synthetic metabolic pathway. J Biosci Bioeng 119(5):585–590. https://doi.org/10.1016/j.jbiosc.2014.10.005

    Article  PubMed  CAS  Google Scholar 

  13. Li Y, Rao N, Yang F, Zhang Y, Yang Y, Liu HM, Guo F, Huang J (2014) Biocomputional construction of a gene network under acid stress in Synechocystis sp. PCC 6803. Res Microbiol 165(6):420–428. https://doi.org/10.1016/j.resmic.2014.04.004

    Article  PubMed  CAS  Google Scholar 

  14. Marin K, Suzuki L, Yamaguchi K, Ribbeck K, Yamamoto H, Kanesaki Y, Hagemann M, Murata N (2003) Identification of histidine kinases that act as sensors in the perception of salt stress in Synechocystis sp PCC 6803. Proc Natl Acad Sci U S A 100(15):9061–9066. https://doi.org/10.1073/pnas.1532302100

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Wang J, Wu G, Chen L, Zhang W (2013c) Cross-species transcriptional network analysis reveals conservation and variation in response to metal stress in cyanobacteria. BMC Genomics 14(1):112. https://doi.org/10.1186/1471-2164-14-112

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Castielli O, De la Cerda B, Navarro JA, Hervas M, De la Rosa MA (2009) Proteomic analyses of the response of cyanobacteria to different stress conditions. FEBS Lett 583(11):1753–1758. https://doi.org/10.1016/j.febslet.2009.03.069

    Article  PubMed  CAS  Google Scholar 

  17. Los DA, Zorina A, Sinetova M, Kryazhov S, Mironov K, Zinchenko VV (2010) Stress sensors and signal transducers in cyanobacteria. Sensors (Basel) 10(3):2386–2415. https://doi.org/10.3390/s100302386

    Article  CAS  Google Scholar 

  18. Uchiyama J, Asakura R, Kimura M, Moriyama A, Tahara H, Kobayashi Y, Kubo Y, Yoshihara T, Ohta H (2012) Slr0967 and Sll0939 induced by the SphR response regulator in Synechocystis sp. PCC 6803 are essential for growth under acid stress conditions. Biochim Biophys Acta 1817(8):1270–1276. https://doi.org/10.1016/j.bbabio.2012.03.028

    Article  PubMed  CAS  Google Scholar 

  19. Ren Q, Shi M, Chen L, Wang J, Zhang W (2014) Integrated proteomic and metabolomic characterization of a novel two-component response regulator Slr1909 involved in acid tolerance in Synechocystis sp. PCC 6803. J Proteome 109:76–89. https://doi.org/10.1016/j.jprot.2014.06.021

    Article  CAS  Google Scholar 

  20. Liang CW, Zhang XW, Chi XY, Guan XY, Li YX, Qin S, Shao HB (2011) Serine/threonine protein kinase SpkG is a candidate for high salt resistance in the unicellular cyanobacterium Synechocystis sp PCC 6803. PLoS One 6(5):e18718. https://doi.org/10.1371/journal.pone.0018718

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Sun T, Xu L, Wu L, Song Z, Chen L, Zhang W (2017) Identification of a new target slr0946 of the response regulator Sll0649 involving cadmium tolerance in Synechocystis sp. PCC 6803. Front Microbiol 8:1582. https://doi.org/10.3389/fmicb.2017.01582

    Article  PubMed  PubMed Central  Google Scholar 

  22. Tian X, Chen L, Wang J, Qiao J, Zhang W (2013) Quantitative proteomics reveals dynamic responses of Synechocystis sp. PCC 6803 to next-generation biofuel butanol. J Proteome 78(1):326–345. https://doi.org/10.1016/j.jprot.2012.10.002

    Article  CAS  Google Scholar 

  23. Wang J, Chen L, Huang S, Liu J, Ren X, Tian X, Qiao J, Zhang W (2012) RNA-seq based identification and mutant validation of gene targets related to ethanol resistance in cyanobacterial Synechocystis sp. PCC 6803. Biotechnol Biofuels 5(1):89. https://doi.org/10.1186/1754-6834-5-89

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Balat M, Balat H (2009) Recent trends in global production and utilization of bio-ethanol fuel. Appl Energy 86(11):2273–2282. https://doi.org/10.1016/j.apenergy.2009.03.015

    Article  CAS  Google Scholar 

  25. Demirbas A (2008) The importance of bioethanol and biodiesel from biomass. Energ Source B 3(2):177–185. https://doi.org/10.1080/15567240600815117

    Article  CAS  Google Scholar 

  26. Qian K, Appels L, Baeyens J, Dewil R, Tan TW (2014) Energy-efficient production of cassava-based bio-ethanol. Adv Biosci Biotechnol 05(12):925–939. https://doi.org/10.4236/abb.2014.512107

    Article  Google Scholar 

  27. Ducat DC, Way JC, Silver PA (2011) Engineering cyanobacteria to generate high-value products. Trends Biotechnol 29(2):95–103. https://doi.org/10.1016/j.tibtech.2010.12.003

    Article  PubMed  CAS  Google Scholar 

  28. Haft RJ, Keating DH, Schwaegler T, Schwalbach MS, Vinokur J, Tremaine M, Peters JM, Kotlajich MV, Pohlmann EL, Ong IM, Grass JA, Kiley PJ, Landick R (2014) Correcting direct effects of ethanol on translation and transcription machinery confers ethanol tolerance in bacteria. Proc Natl Acad Sci U S A 111(25):E2576–E2585. https://doi.org/10.1073/pnas.1401853111

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Uden NV (1985) Chapter 2–ethanol toxicity and ethanol tolerance in yeasts. Annu Rep Ferment Process 8:11–58. https://doi.org/10.1016/B978-0-12-040308-0.50006-9

    Article  Google Scholar 

  30. Zhu Y, Pei G, Niu X, Shi M, Zhang M, Chen L, Zhang W (2015) Metabolomic analysis reveals functional overlapping of three signal transduction proteins in regulating ethanol tolerance in cyanobacterium Synechocystis sp. PCC 6803. Mol BioSyst 11(3):770–782. https://doi.org/10.1039/c4mb00651h

    Article  PubMed  CAS  Google Scholar 

  31. Song Z, Chen L, Wang J, Lu Y, Jiang W, Zhang W (2014) A transcriptional regulator Sll0794 regulates tolerance to biofuel ethanol in photosynthetic Synechocystis sp. PCC 6803. Mol Cell Proteomics Mcp 13(12):3519. https://doi.org/10.1074/mcp.M113.035675

    Article  PubMed  CAS  Google Scholar 

  32. Ding J, Huang X, Zhang L, Zhao N, Yang D, Zhang K (2009) Tolerance and stress response to ethanol in the yeast Saccharomyces cerevisiae. Appl Microbiol Biotechnol 85(2):253–263. https://doi.org/10.1007/s00253-009-2223-1

    Article  PubMed  CAS  Google Scholar 

  33. Foo JL, Jensen HM, Dahl RH, George K, Keasling JD, Lee TS, Leong S, Mukhopadhyay A (2014) Improving microbial biogasoline production in Escherichia coli using tolerance engineering. MBio 5(6):e01932. https://doi.org/10.1128/mBio.01932-14

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Stanley D, Bandara A, Fraser S, Chambers PJ, Stanley GA (2010) The ethanol stress response and ethanol tolerance of Saccharomyces cerevisiae. J Appl Microbiol 109(1):13–24. https://doi.org/10.1111/j.1365-2672.2009.04657.x

    Article  PubMed  CAS  Google Scholar 

  35. Teixeira MC, Godinho CP, Cabrito TR, Mira NP, Sa-Correia I (2012) Increased expression of the yeast multidrug resistance ABC transporter Pdr18 leads to increased ethanol tolerance and ethanol production in high gravity alcoholic fermentation. Microb Cell Factories 11:98. https://doi.org/10.1186/1475-2859-11-98

    Article  CAS  Google Scholar 

  36. Jia WQ, Zhang LJ, Wu D, Liu S, Gong X, Cui ZH, Cui N, Cao HY, Rao LB, Wang C (2015) Sucrose transporter AtSUC9 mediated by a low sucrose level is involved in Arabidopsis abiotic stress resistance by regulating sucrose distribution and ABA accumulation. Plant Cell Physiol 56(8):1574–1587. https://doi.org/10.1093/pcp/pcv082

    Article  PubMed  CAS  Google Scholar 

  37. Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, Miyajima N, Hirosawa M, Sugiura M, Sasamoto S, Kimura T, Hosouchi T, Matsuno A, Muraki A, Nakazaki N, Naruo K, Okumura S, Shimpo S, Takeuchi C, Wada T, Watanabe A, Yamada M, Yasuda M, Tabata S (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions (supplement). DNA Res Intl J Rapid Publ Rep Genes Genomes 3(3):185–209. https://doi.org/10.1093/dnares/3.3.109

    Article  CAS  Google Scholar 

  38. Fisher MA, Boyarskiy S, Yamada MR, Kong N, Bauer S, Tullman-Ercek D (2014) Enhancing tolerance to short-chain alcohols by engineering the Escherichia coli AcrB efflux pump to secrete the non-native substrate n-butanol. ACS Synth Biol 3(1):30–40. https://doi.org/10.1021/sb400065q

    Article  PubMed  CAS  Google Scholar 

  39. Cavet JS, Borrelly GP, Robinson NJ (2003) Zn, Cu and Co in cyanobacteria: selective control of metal availability. FEMS Microbiol Rev 27(2–3):165–181. https://doi.org/10.1016/S0168-6445(03)00050-0

    Article  PubMed  CAS  Google Scholar 

  40. Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environment. EXS 101(101):133–164. https://doi.org/10.1007/978-3-7643-8340-4_6

    Article  PubMed  PubMed Central  Google Scholar 

  41. Huertas MJ, Lopez-Maury L, Giner-Lamia J, Sanchez-Riego AM, Florencio FJ (2014) Metals in cyanobacteria: analysis of the copper, nickel, cobalt and arsenic homeostasis mechanisms. Life (Basel) 4(4):865–886. https://doi.org/10.3390/life4040865

    Article  CAS  Google Scholar 

  42. Gandini C, Schmidt SB, Husted S, Schneider A, Leister D (2017) The transporter SynPAM71 is located in the plasma membrane and thylakoids, and mediates manganese tolerance in Synechocystis PCC6803. New Phytol 215(1):256–268. https://doi.org/10.1111/nph.14526

    Article  PubMed  CAS  Google Scholar 

  43. Schneider A, Steinberger I, Herdean A, Gandini C, Eisenhut M, Kurz S, Morper A, Hoecker N, Ruhle T, Labs M, Flugge UI, Geimer S, Schmidt SB, Husted S, Weber APM, Spetea C, Leister D (2016) The evolutionarily conserved protein PHOTOSYNTHESIS AFFECTED MUTANT71 is required for efficient manganese uptake at the thylakoid membrane in Arabidopsis. Plant Cell 28(4):892–910. https://doi.org/10.1105/tpc.15.00812

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Millaleo R, Reyes-Diaz M, Alberdi M, Ivanov AG, Krol M, Huner NP (2013) Excess manganese differentially inhibits photosystem I versus II in Arabidopsis thaliana. J Exp Bot 64(1):343–354. https://doi.org/10.1093/jxb/ers339

    Article  PubMed  CAS  Google Scholar 

  45. Nable RO, Houtz RL, Cheniae GM (1988) Early inhibition of photosynthesis during development of Mn toxicity in tobacco. Plant Physiol 86(4):1136–1142. https://doi.org/10.1104/pp.86.4.1136

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Clairmont KB, Hagar WG, Davis EA (1986) Manganese toxicity to chlorophyll synthesis in tobacco callus. Plant Physiol 80(1):291–293. https://doi.org/10.1104/pp.80.1.291

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Li M, Zhu Q, Hu CW, Chen L, Liu ZL, Kong ZM (2007) Cobalt and manganese stress in the microalga Pavlova viridis (Prymnesiophyceae): effects on lipid peroxidation and antioxidant enzymes. J Environ Sci (China) 19(11):1330–1335. https://doi.org/10.1016/s1001-0742(07)60217-4

    Article  CAS  Google Scholar 

  48. Checchetto V, Segalla A, Sato Y, Bergantino E, Szabo I, Uozumi N (2016) Involvement of potassium transport systems in the response of Synechocystis PCC 6803 cyanobacteria to external pH change, high-intensity light stress and heavy metal stress. Plant Cell Physiol 57(4):862–877. https://doi.org/10.1093/pcp/pcw032

    Article  PubMed  CAS  Google Scholar 

  49. Kobayashi M, Okada K, Ikeuchi M (2005) A suppressor mutation in the alpha-phycocyanin gene in the light/glucose-sensitive phenotype of the psbK-disruptant of the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 46(9):1561–1567. https://doi.org/10.1093/pcp/pci169

    Article  PubMed  CAS  Google Scholar 

  50. Tahara H, Uchiyama J, Yoshihara T, Matsumoto K, Ohta H (2012) Role of Slr1045 in environmental stress tolerance and lipid transport in the cyanobacterium Synechocystis sp. PCC6803. Biochim Biophys Acta 1817(8):1360–1366. https://doi.org/10.1016/j.bbabio.2012.02.035

    Article  PubMed  CAS  Google Scholar 

  51. Malinverni JC, Silhavy TJ (2009) An ABC transport system that maintains lipid asymmetry in the Gram-negative outer membrane. Proc Natl Acad Sci U S A 106(19):8009–8014. https://doi.org/10.1073/pnas.0903229106

    Article  PubMed  PubMed Central  Google Scholar 

  52. Xu C, Fan J, Froehlich JE, Awai K, Benning C (2005) Mutation of the TGD1 chloroplast envelope protein affects phosphatidate metabolism in Arabidopsis. Plant Cell 17(11):3094–3110. https://doi.org/10.1105/tpc.105.035592

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Tahara H, Matsuhashi A, Uchiyama J, Ogawa S, Ohta H (2015) Sll0751 and Sll1041 are involved in acid stress tolerance in Synechocystis sp. PCC 6803. Photosynth Res 125(1):233–242. https://doi.org/10.1007/s11120-015-0153-6

    Article  PubMed  CAS  Google Scholar 

  54. Matsuhashi A, Tahara H, Ito Y, Uchiyama J, Ogawa S, Ohta H (2015) Slr2019, lipid A transporter homolog, is essential for acidic tolerance in Synechocystis sp PCC6803. Photosynth Res 125(1–2):267–277. https://doi.org/10.1007/s11120-015-0129-6

    Article  PubMed  CAS  Google Scholar 

  55. Hagemann M (2011) Molecular biology of cyanobacterial salt acclimation. FEMS Microbiol Rev 35(1):87–123. https://doi.org/10.1111/j.1574-6976.2010.00234.x

    Article  PubMed  CAS  Google Scholar 

  56. Li T, Zhang YN, Shi ML, Pei GS, Chen L, Zhang WW (2016) A putative magnesium transporter Slr1216 involved in sodium tolerance in cyanobacterium Synechocystis sp PCC 6803. Algal Res 17:202–210. https://doi.org/10.1016/j.algal.2016.05.003

    Article  Google Scholar 

  57. Allakhverdiev SI, Murata N (2008) Salt stress inhibits photosystems II and I in cyanobacteria. Photosynth Res 98(1–3):529–539. https://doi.org/10.1007/s11120-008-9334-x

    Article  PubMed  CAS  Google Scholar 

  58. Tan X, Du W, Lu X (2015) Photosynthetic and extracellular production of glucosylglycerol by genetically engineered and gel-encapsulated cyanobacteria. Appl Microbiol Biotechnol 99(5):2147–2154. https://doi.org/10.1007/s00253-014-6273-7

    Article  PubMed  CAS  Google Scholar 

  59. Novak JF, Stirnberg M, Roenneke B, Marin K (2011) A novel mechanism of osmosensing, a salt-dependent protein-nucleic acid interaction in the cyanobacterium Synechocystis species PCC 6803. J Biol Chem 286(5):3235–3241. https://doi.org/10.1074/jbc.M110.157032

    Article  PubMed  CAS  Google Scholar 

  60. Marin K, Zuther E, Kerstan T, Kunert A, Hagemann M (1998) The ggpS gene from Synechocystis sp. strain PCC 6803 encoding glucosyl-glycerol-phosphate synthase is involved in osmolyte synthesis. J Bacteriol 180(18):4843–4849

    PubMed  PubMed Central  CAS  Google Scholar 

  61. Hagemann M, Schoor A, Erdmann N (1996) NaCl acts as a direct modulator in the salt adaptive response: salt-dependent activation of glucosylglycerol synthesis in vivo and in vitro. J Plant Physiol 149(6):746–752. https://doi.org/10.1016/S0176-1617(96)80101-5

    Article  CAS  Google Scholar 

  62. Hagemann M, Effmert U, Kerstan T, Schoor A, Erdmann N (2001) Biochemical characterization of glucosylglycerol-phosphate synthase of Synechocystis sp. strain PCC 6803: comparison of crude, purified, and recombinant enzymes. Curr Microbiol 43(4):278–283. https://doi.org/10.1007/s002840010301

    Article  PubMed  CAS  Google Scholar 

  63. Schoor A, Hagemann M, Erdmann N (1999) Glucosylglycerol-phosphate synthase: target for ion-mediated regulation of osmolyte synthesis in the cyanobacterium synechocystis sp. strain PCC 6803. Arch Microbiol 171(2):101–106. https://doi.org/10.1007/s002030050684

    Article  PubMed  CAS  Google Scholar 

  64. Qiao J, Wang J, Chen L, Tian X, Huang S, Ren X, Zhang W (2012) Quantitative iTRAQ LC-MS/MS proteomics reveals metabolic responses to biofuel ethanol in cyanobacterial Synechocystis sp. PCC 6803. J Proteome Res 11(11):5286–5300. https://doi.org/10.1021/pr300504w

    Article  PubMed  CAS  Google Scholar 

  65. Dienst D, Georg J, Abts T, Jakorew L, Kuchmina E, Borner T, Wilde A, Duhring U, Enke H, Hess WR (2014) Transcriptomic response to prolonged ethanol production in the cyanobacterium Synechocystis sp. PCC6803. Biotechnol Biofuels 7(1):21. https://doi.org/10.1186/1754-6834-7-21

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Zhang Y, Niu X, Shi M, Pei G, Zhang X, Chen L, Zhang W (2015) Identification of a transporter Slr0982 involved in ethanol tolerance in cyanobacterium Synechocystis sp. PCC 6803. Front Microbiol 6:487. https://doi.org/10.3389/fmicb.2015.00487

    Article  PubMed  PubMed Central  Google Scholar 

  67. Zhang LF, Yang HM, Cui SX, Hu J, Wang J, Kuang TY, Norling B, Huang F (2009) Proteomic analysis of plasma membranes of cyanobacterium Synechocystis sp. Strain PCC 6803 in response to high pH stress. J Proteome Res 8(6):2892–2902. https://doi.org/10.1021/pr900024w

    Article  PubMed  CAS  Google Scholar 

  68. Krall L, Huege J, Catchpole G, Steinhauser D, Willmitzer L (2009) Assessment of sampling strategies for gas chromatography–mass spectrometry (GC–MS) based metabolomics of cyanobacteria. J Chromatogr B 877(27):2952–2960. https://doi.org/10.1016/j.jchromb.2009.07.006

    Article  CAS  Google Scholar 

  69. Holden CP, Storey KB (1994) 6-phosphogluconate dehydrogenase from a freeze tolerant insect: control of the hexose monophosphate shunt and NADPH production during cryprotectant synthesis. Insect Biochem Mol Biol 24(2):167–173. https://doi.org/10.1016/0965-1748(94)90083-3

    Article  CAS  Google Scholar 

  70. Zaffagnini M, Bedhomme M, Groni H, Marchand CH, Puppo C, Gontero B, Cassier-Chauvat C, Decottignies P, Lemaire SD (2012) Glutathionylation in the photosynthetic model organism Chlamydomonas reinhardtii: a proteomic survey. Mo Cell Proteomics MCP 11(2):M111.014142. https://doi.org/10.1074/mcp.M111.014142

    Article  CAS  Google Scholar 

  71. Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinforma 9(1):559. https://doi.org/10.1186/1471-2105-9-559

    Article  CAS  Google Scholar 

  72. Zhang B, Horvath S (2005) A general framework for weighted gene co-expression network analysis. Stat Appl Genet Mol Biol 4(1):1–43 Retrieved 6. https://doi.org/10.2202/1544-6115.1128

    Article  CAS  Google Scholar 

  73. Chen T, Wang J, Zeng L, Li R, Li J, Chen Y, Lin Z (2012) Significant rewiring of the transcriptome and proteome of an Escherichia coli strain harboring a tailored exogenous global regulator IrrE. PLoS One 7(7):e37126. https://doi.org/10.1371/journal.pone.0037126

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. Horinouchi T, Tamaoka K, Furusawa C, Ono N, Suzuki S, Hirasawa T, Yomo T, Shimizu H (2010) Transcriptome analysis of parallel-evolved Escherichia coli strains under ethanol stress. BMC Genomics 11:579–579. https://doi.org/10.1186/1471-2164-11-579

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. Chiang M-L, Ho W-L, Chou C-C (2008) Ethanol shock changes the fatty acid profile and survival behavior of Vibrio parahaemolyticus in various stress conditions. Food Microbiol 25(2):359–365. https://doi.org/10.1016/j.fm.2007.10.002

    Article  PubMed  CAS  Google Scholar 

  76. Couto J, Rozes N, Hogg T (1996) Ethanol-induced changes in the fatty acid composition of Lactobacillus Hilgardii, its effects on plasma membrane fluidity and relationship with ethanol tolerance. J Appl Bacteriol 81(2):126–132 (7) 7. https://doi.org/10.1111/j.1365-2672.1996.tb04489.x

    Article  CAS  Google Scholar 

  77. Heipieper HJ, Isken S, Saliola M (2000) Ethanol tolerance and membrane fatty acid adaptation in adh multiple and null mutants of Kluyveromyces lactis. Res Microbiol 151(9):777–784. https://doi.org/10.1016/S0923-2508(00)01143-8

    Article  PubMed  CAS  Google Scholar 

  78. Kajiwara S, Suga K, Sone H, Nakamura K (2000) Improved ethanol tolerance of Saccharomyces cerevisiae strains by increases in fatty acid unsaturation via metabolic engineering. Biotechnol Lett 22(23):1839–1843. https://doi.org/10.1023/a:1005632522620

    Article  CAS  Google Scholar 

  79. Pfeiffer T, Soyer OS, Bonhoeffer S (2005) The evolution of connectivity in metabolic networks. PLoS Biol 3(7):e228. https://doi.org/10.1371/journal.pbio.0030228

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. Buenrostro-Figueroa J, Tafolla-Arellano JC, Flores-Gallegos AC, Rodriguez-Herrera R, De la Garza-Toledo H, Aguilar CN (2017) Native yeasts for alternative utilization of overripe mango pulp for ethanol production. Rev Argent Microbiol. https://doi.org/10.1016/j.ram.2016.04.010

  81. Liu Y, Huang H (2017) Expression of single-domain antibody in different systems. Appl Microbiol Biotechnol. https://doi.org/10.1007/s00253-017-8644-3

  82. Mesgari-Shadi A, Sarrafzadeh MH (2017) Osmotic conditions could promote scFv antibody production in the Escherichia coli HB2151. BioImpacts BI 7(3):199–206. https://doi.org/10.15171/bi.2017.23

    Article  PubMed  PubMed Central  Google Scholar 

  83. Shin KS, Lee SK (2017) Increasing extracellular free fatty acid production in Escherichia coli by disrupting membrane transport systems. J Agric Food Chem 65(51):11243–11250. https://doi.org/10.1021/acs.jafc.7b04521

    Article  PubMed  CAS  Google Scholar 

  84. You SK, Joo YC, Kang DH, Shin SK, Hyeon JE, Woo HM, Um Y, Park C, Han SO (2017) Enhancing fatty acid production of Saccharomyces cerevisiae as an animal feed supplement. J Agric Food Chem 65(50):11029–11035. https://doi.org/10.1021/acs.jafc.7b04485

    Article  PubMed  CAS  Google Scholar 

  85. Henderson CM, Block DE (2014) Examining the role of membrane lipid composition in determining the ethanol tolerance of Saccharomyces cerevisiae. Appl Environ Microbiol 80(10):2966–2972. https://doi.org/10.1128/AEM.04151-13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. Lam FH, Ghaderi A, Fink GR, Stephanopoulos G (2014) Biofuels. Engineering alcohol tolerance in yeast. Science (New York, NY) 346(6205):71–75. https://doi.org/10.1126/science.1257859

    Article  CAS  Google Scholar 

  87. Reyes LH, Abdelaal AS, Kao KC (2013) Genetic determinants for n-butanol tolerance in evolved Escherichia coli mutants: cross adaptation and antagonistic pleiotropy between n-butanol and other stressors. Appl Environ Microbiol 79(17):5313–5320. https://doi.org/10.1128/aem.01703-13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  88. Yuan Y, Bi C, Nicolaou SA, Zingaro KA, Ralston M, Papoutsakis ET (2014) Overexpression of the Lactobacillus plantarum peptidoglycan biosynthesis murA2 gene increases the tolerance of Escherichia coli to alcohols and enhances ethanol production. Appl Microbiol Biotechnol 98(19):8399–8411. https://doi.org/10.1007/s00253-014-6004-0

    Article  PubMed  CAS  Google Scholar 

  89. Jones CM, Hernandez Lozada NJ, Pfleger BF (2015) Efflux systems in bacteria and their metabolic engineering applications. Appl Microbiol Biotechnol 99(22):9381–9393. https://doi.org/10.1007/s00253-015-6963-9

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  90. Zhang C, Chen X, Stephanopoulos G, Too HP (2016) Efflux transporter engineering markedly improves amorphadiene production in Escherichia coli. Biotechnol Bioeng 113(8):1755–1763. https://doi.org/10.1002/bit.25943

    Article  PubMed  CAS  Google Scholar 

  91. Wang J-F, Xiong Z-Q, Li S-Y, Wang Y (2013b) Enhancing isoprenoid production through systematically assembling and modulating efflux pumps in Escherichia coli. Appl Microbiol Biotechnol 97(18):8057–8067. https://doi.org/10.1007/s00253-013-5062-z

    Article  PubMed  CAS  Google Scholar 

  92. Foo JL, Leong SS (2013) Directed evolution of an E. coli inner membrane transporter for improved efflux of biofuel molecules. Biotechnol Biofuels 6(1):81. https://doi.org/10.1186/1754-6834-6-81

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  93. Siu Y, Fenno J, Lindle JM, Dunlop MJ (2017) Design and selection of a synthetic feedback loop for optimizing biofuel tolerance. ACS Synth Biol. https://doi.org/10.1021/acssynbio.7b00260

  94. Turner WJ, Dunlop MJ (2015) Trade-offs in improving biofuel tolerance using combinations of efflux pumps. ACS Synth Biol 4(10):1056–1063. https://doi.org/10.1021/sb500307w

    Article  PubMed  CAS  Google Scholar 

  95. Boyarskiy S, Davis Lopez S, Kong N, Tullman-Ercek D (2016) Transcriptional feedback regulation of efflux protein expression for increased tolerance to and production of n-butanol. Metab Eng 33(Supplement C):130–137. https://doi.org/10.1016/j.ymben.2015.11.005

    Article  PubMed  CAS  Google Scholar 

  96. Mukhopadhyay A (2015) Tolerance engineering in bacteria for the production of advanced biofuels and chemicals. Trends Microbiol 23(8):498–508. https://doi.org/10.1016/j.tim.2015.04.008

    Article  PubMed  CAS  Google Scholar 

  97. Ducat DC, Avelar-Rivas JA, Way JC, Silver PA (2012) Rerouting carbon flux to enhance photosynthetic productivity. Appl Environ Microbiol 78(8):2660–2668. https://doi.org/10.1128/AEM.07901-11

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  98. Li C, Tao F, Ni J, Wang Y, Yao F, Xu P (2015) Enhancing the light-driven production of D-lactate by engineering cyanobacterium using a combinational strategy. Sci Rep 5:9777. https://doi.org/10.1038/srep09777

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  99. Korosh TC, Markley AL, Clark RL, McGinley LL, McMahon KD, Pfleger BF (2017) Engineering photosynthetic production of L-lysine. Metab Eng 44:273–283. https://doi.org/10.1016/j.ymben.2017.10.010

    Article  PubMed  CAS  Google Scholar 

  100. Nikkinen HL, Hakkila K, Gunnelius L, Huokko T, Pollari M, Tyystjarvi T (2012) The SigB sigma factor regulates multiple salt acclimation responses of the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 158(1):514–523. https://doi.org/10.1104/pp.111.190058

    Article  PubMed  CAS  Google Scholar 

  101. Gao X, Sun T, Pei G, Chen L, Zhang W (2016) Cyanobacterial chassis engineering for enhancing production of biofuels and chemicals. Appl Microbiol Biotechnol 100(8):3401–3413. https://doi.org/10.1007/s00253-016-7374-2

    Article  PubMed  CAS  Google Scholar 

  102. Huang F, Fulda S, Hagemann M, Norling B (2006) Proteomic screening of salt-stress-induced changes in plasma membranes of Synechocystis sp. strain PCC 6803. Proteomics 6(3):910–920. https://doi.org/10.1002/pmic.200500114

    Article  PubMed  CAS  Google Scholar 

  103. Liu J, Chen L, Wang J, Qiao J, Zhang W (2012) Proteomic analysis reveals resistance mechanism against biofuel hexane in Synechocystis sp. PCC 6803. Biotechnol Biofuels 5(1):68. https://doi.org/10.1186/1754-6834-5-68

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  104. Zhu H, Ren X, Wang J, Song Z, Shi M, Qiao J, Tian X, Liu J, Chen L, Zhang W (2013) Integrated OMICS guided engineering of biofuel butanol-tolerance in photosynthetic Synechocystis sp. PCC 6803. Biotechnol Biofuels 6(1):106. https://doi.org/10.1186/1754-6834-6-106

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  105. Nicolaou SA, Gaida SM, Papoutsakis ET (2010) A comparative view of metabolite and substrate stress and tolerance in microbial bioprocessing: from biofuels and chemicals, to biocatalysis and bioremediation. Metab Eng 12(4):307–331. https://doi.org/10.1016/j.ymben.2010.03.004

    Article  PubMed  CAS  Google Scholar 

  106. Wagner S, Baars L, Ytterberg AJ, Klussmeier A, Wagner CS, Nord O, Nygren PA, van Wijk KJ, de Gier JW (2007) Consequences of membrane protein overexpression in Escherichia coli. Mol Cell Proteomics 6(9):1527–1550. https://doi.org/10.1074/mcp.M600431-MCP200

    Article  PubMed  CAS  Google Scholar 

  107. Liu D, Xiao Y, Evans BS, Zhang F (2015) Negative feedback regulation of fatty acid production based on a malonyl-CoA sensor-actuator. ACS Synth Biol 4(2):132–140. https://doi.org/10.1021/sb400158w

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by the National Science Foundation of China (NSFC) [No. 21621004, 31770100, 31170043, 31270086, and 31370115], the National Basic Research Program of China (National “973” program) [No. 2014CB745101 and No. 2011CBA00803], and the National Science Foundation of Tianjin, China [No. 13JCQNJC09900].

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Authors and Affiliations

  1. Laboratory of Synthetic Microbiology, School of Chemical Engineering & Technology, Tianjin University, Tianjin, China

    Yaru Xie, Lei Chen, Tao Sun, Yanan Zhang, Ting Li, Xinyu Song & Weiwen Zhang

  2. Key Laboratory of Systems Bioengineering (Ministry of Education), Tianjin University, Tianjin, China

    Yaru Xie, Lei Chen, Tao Sun, Yanan Zhang, Ting Li, Xinyu Song & Weiwen Zhang

  3. SynBio Research Platform, Collaborative Innovation Center of Chemical Science and Engineering, Tianjin, China

    Yaru Xie, Lei Chen, Tao Sun, Yanan Zhang, Ting Li, Xinyu Song & Weiwen Zhang

  4. Center for Biosafety Research and Strategy, Tianjin University, Tianjin, China

    Xinyu Song & Weiwen Zhang

  5. School of Environmental Science and Engineering, Tianjin University, Tianjin, China

    Xinyu Song

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  1. Yaru Xie
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Correspondence to Xinyu Song .

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  1. School of Chemical Engineering, Tianjin University, Tianjin, China

    Weiwen Zhang

  2. Center for Biosafety Research and Strategy, Tianjin University, Tianjin, China

    Xinyu Song

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Xie, Y. et al. (2018). Transporters Related to Stress Responses and Their Potential Application in Synechocystis sp. PCC 6803. In: Zhang, W., Song, X. (eds) Synthetic Biology of Cyanobacteria. Advances in Experimental Medicine and Biology, vol 1080. Springer, Singapore. https://doi.org/10.1007/978-981-13-0854-3_2

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