Artificial complementary chromatic acclimation gene expression system in Escherichia coli

Ariyanti D., Ikebukuro K., Sode K.

Department of Biotechnology and Life Science, Graduate School of Engineering, Tokyo University of Agriculture and Technology, 2-24-16 Naka-cho, Koganei, Tokyo 184-8588, Japan; Faculty of Biotechnology, Sumbawa University of Technology, Olat Maras, Moyo Hulu, Sumbawa, West Nusa Tenggara 84371, Indonesia; Joint Department of Biomedical Engineering, The University of North Carolina at Chapel Hill and North Carolina State University, Chapel Hill, NC 27599, United States


Abstract

Background: The development of multiple gene expression systems, especially those based on the physical signals, such as multiple color light irradiations, is challenging. Complementary chromatic acclimation (CCA), a photoreversible process that facilitates the control of cellular expression using light of different wavelengths in cyanobacteria, is one example. In this study, an artificial CCA systems, inspired by type III CCA light-regulated gene expression, was designed by employing a single photosensor system, the CcaS/CcaR green light gene expression system derived from Synechocystis sp. PCC6803, combined with G-box (the regulator recognized by activated CcaR), the cognate cpcG2 promoter, and the constitutively transcribed promoter, the PtrcΔLacO promoter. Results: One G-box was inserted upstream of the cpcG2 promoter and a reporter gene, the rfp gene (green light-induced gene expression), and the other G-box was inserted between the PtrcΔLacO promoter and a reporter gene, the bfp gene (red light-induced gene expression). The Escherichia coli transformants with plasmid-encoded genes were evaluated at the transcriptional and translational levels under red or green light illumination. Under green light illumination, the transcription and translation of the rfp gene were observed, whereas the expression of the bfp gene was repressed. Under red light illumination, the transcription and translation of the bfp gene were observed, whereas the expression of the rfp gene was repressed. During the red and green light exposure cycles at every 6 h, BFP expression increased under red light exposure while RFP expression was repressed, and RFP expression increased under green light exposure while BFP expression was repressed. Conclusion: An artificial CCA system was developed to realize a multiple gene expression system, which was regulated by two colors, red and green lights, using a single photosensor system, the CcaS/CcaR system derived from Synechocystis sp. PCC6803, in E. coli. The artificial CCA system functioned repeatedly during red and green light exposure cycles. These results demonstrate the potential application of this CCA gene expression system for the production of multiple metabolites in a variety of microorganisms, such as cyanobacteria. © 2021, The Author(s).

Artificial complementary chromatic acclimation; CcaS/CcaR; Escherichia coli; Gene expression system


Journal

Microbial Cell Factories

Publisher: BioMed Central Ltd

Volume 20, Issue 1, Art No 128, Page – , Page Count


Journal Link: https://www.scopus.com/inward/record.uri?eid=2-s2.0-85109343662&doi=10.1186%2fs12934-021-01621-3&partnerID=40&md5=ba5edebbbde9a3f94dc490b05cae3b00

doi: 10.1186/s12934-021-01621-3

Issn: 14752859

Type: All Open Access, Gold, Green


References

Narikawa, R., Suzuki, F., Yoshihara, S., Higashi, S., Watanabe, M., Ikeuchi, M., Novel photosensory two-component system (PixA-NixB-NixC) involved in the regulation of positive and negative phototaxis of cyanobacterium Synechocystis sp. PCC6803 (2011) Plant Cell Physiol, 52, pp. 2214-2224. , COI: 1:CAS:528:DC%2BC3MXhs1WgsbjE; Song, J.Y., Cho, H.S., Cho, J.I., Jeon, J.S., Lagarias, J.C., Park, Y.I., Near-UV cyanobacterichrome signaling system elicits negative phototaxis in the cyanobacterium Synechocystis sp. PCC6803 (2011) Proc Natl Acad Sci, 108, pp. 10780-10785. , COI: 1:CAS:528:DC%2BC3MXovV2htbY%3D; Yoshihara, S., Shimada, T., Matsuoka, D., Zikihara, K., Kohchi, T., Tokutomi, S., Reconstruction of blue-green reversible photoconversion of cyanobacterial photoreceptor, PixJ1, in phycocyanobilin-producing Escherichia coli (2006) Biochemistry, 45, pp. 3775-3784. , COI: 1:CAS:528:DC%2BD28Xhtlersbo%3D; Terauchi, K., Montgomery, B.L., Grossman, A.R., Lagarias, J.C., Kehoe, D.M., RcaE is complementary chromatic adaptation photoreceptor required for green and red responsiveness (2004) Mol Microbiol, 51, pp. 576-577; Hirose, Y., Shimada, T., Narikawa, R., Katayama, M., Ikeuchi, M., Cyanobacteriochrome CcaS is the green light receptor that induces the expression of phycobilisome linker protein (2008) Proc Natl Acad Sci, 105, pp. 9528-9533. , COI: 1:CAS:528:DC%2BD1cXovVOjsbc%3D; Hirose, Y., Narikawa, R., Katayama, M., Ikeuchi, M., Cyanobacteriochrome CcaS regulates phycoerythrin accumulation in Nostoc punctiforme, a group II chromatic adapter (2010) Proc Natl Acad Sci, 107, pp. 8854-8859. , COI: 1:CAS:528:DC%2BC3cXmsFWmu7o%3D; Abe, K., Miyake, K., Nakamura, M., Kojima, K., Ferri, S., Ikebukuro, K., Sode, K., Engineering of a green-light inducible gene expression system in Synechocystis sp. PCC6803 (2014) Microbial Biotechnol, 7, pp. 177-183. , COI: 1:CAS:528:DC%2BC2cXislelsb4%3D; Miyake, K., Abe, K., Ferri, S., Nakajima, M., Kojima, K., Ikebukuro, K., Sode, K., Green light-inducible lytic system for cyanobacterial cells (2014) Biotechnol Biofuels, 7, p. 56; Badary, A., Abe, K., Ferri, S., Kojima, K., Sode, K., The development and characterization of an exogenous green-light-regulated gene expression system in marine cyanobacteria (2015) Mar Biotechnol, 17, pp. 245-251. , COI: 1:CAS:528:DC%2BC2MXhvV2rtr8%3D; Badary, A., Takamatsu, S., Nakajima, M., Ferri, S., Lindblad, P., Sode, K., Glycogen production in marine cyanobacterial strain Synechococcus sp. NKBG 15041c (2018) Mar Biotechnol, 20, pp. 109-117. , COI: 1:CAS:528:DC%2BC1cXhtVKrsL8%3D; Nakajima, M., Abe, K., Ferry, S., Sode, K., Development of light-regulated cell recovery system for non-photosynthetic bacteria (2016) Microb Cell Fact, 15, p. 31; Nakajima, M., Ferri, S., Rögner, M., Sode, K., Construction of a miniaturized chromatic acclimation sensor from cyanobacteria with reversed response to a light signal (2016) Sci Rep, 6, p. 37595. , COI: 1:CAS:528:DC%2BC28XitFSmtbrO; Kobayashi, S., Nakajima, M., Asano, R., Ferreira, E.A., Abe, K., Tamagnini, P., Atsumi, S., Sode, K., Application of an engineered chromatic acclimation sensor for red light-regulated gene expression in cyanobacteria (2019) Algal Res, 44, p. 101691; Kehoe, D.M., Gutu, A., Responding to color: the regulation of complementary chromatic adaptation (2006) Annu Rev Plant Biol, 57, pp. 127-150. , COI: 1:CAS:528:DC%2BD28XosVKhsbk%3D; Gutu, A., Kehoe, D.M., Emerging perspectives on the mechanism, regulation, and distribution of light color acclimation in cyanobacteria (2012) Mol Plant, 5, pp. 1-13. , COI: 1:CAS:528:DC%2BC38Xht1SmtLk%3D; Montgomery, B.L., Mechanism and fitness implications of photomorphogenesis during chromatic acclimation in cyanobacteria (2016) J Exp Bot, 67 (14), pp. 4079-4090. , COI: 1:CAS:528:DC%2BC28Xhs1OntLnJ; Li, L., Alvey, R.M., Bezy, R.P., Kehoe, D.M., Inverse transcriptional activities during complementary chromatic adaptation are controlled by the response regulator RcaC binding to red and green light-responsive promoters (2008) Mol Microbiol, 68 (2), pp. 286-297. , COI: 1:CAS:528:DC%2BD1cXkvVyqtLg%3D; Kehoe, D.M., Grossman, A.R., New classes of mutants in complementary adaptation provide evidence for a novel four-step phosphorelay system (1997) J Bacteriol, 179, pp. 3914-3921. , COI: 1:CAS:528:DyaK2sXktVKhsro%3D; Alvey, R.M., Karty, J.A., Roos, E., Reilly, J.P., Kehoe, D.M., Lesions in phycoerythrin chromophore biosynthesis in Fremyella diplosiphon reveal coordinated light regulation of apoprotein and pigment biosynthetic enzyme gene expression (2003) Plant Cell, 15, pp. 2448-2463. , COI: 1:CAS:528:DC%2BD3sXotlGmtbo%3D; Li, L., Kehoe, D.M., In vivo analysis of the roles of conserved aspartate and histidine residues within a complex response regulator (2005) Mol Microbiol, 55, pp. 1538-1552. , COI: 1:CAS:528:DC%2BD2MXitl2ru70%3D; Alvey, R.M., Bezy, R.P., A light regulated OmpR-class promoter element co-ordinates light-harvesting protein and chromophore biosynthetic enzyme gene expression (2007) Mol Microbiol, 64 (2), pp. 319-332. , COI: 1:CAS:528:DC%2BD2sXltlamurw%3D; Bordowitz, J.R., Montgomery, B.L., Photoregulation of cellular morphology during complementary chromatic adaptation requires sensor-kinase-class protein RcaE in Fremyella diplosiphon (2008) J Bacteriol, 190 (11), pp. 4069-4074. , COI: 1:CAS:528:DC%2BD1cXmsVOmsbY%3D; Bezy, R.P., Kehoe, D.M., Functional characterization of cyanobacterial OmpR/PhoB class transcription factor binding site controlling light color responses (2010) J Bacteriol, 192 (22), pp. 5923-5933. , COI: 1:CAS:528:DC%2BC3MXis1Knsg%3D%3D; Registry of Standard Biological Part, , https://www.partregistry.org; Sode, K., Hatano, N., Tatara, M., Pseudo-continuous culture of marine recombinant cyanobacteria under light and dark cycle (1994) Biotechnol lett, 16 (9), pp. 973-976. , COI: 1:CAS:528:DyaK2cXmslyru7w%3D; Huang, H.H., Camsund, D., Lindblad, P., Heidorn, T., Design and characterization of molecular tools for synthetic biology approach towards developing cyanobacterial biotechnology (2010) Nucleic Acids Res, 38, pp. 2577-2593. , COI: 1:CAS:528:DC%2BC3cXlsFGnur4%3D; Camsund, D., Linblad, P., Engineered transcriptional system for cyanobacterial biotechnology (2014) Front Bioeng Biotechnol, 2, pp. 1-9; Tabor, J.J., Levskaya, A., Voigt, C.A., Multichromatic control of gene expression in Escherichia coli (2011) J Mol Biol, 405, pp. 315-324. , COI: 1:CAS:528:DC%2BC3MXktVSmtA%3D%3D; Schmidl, S.R., Sheth, R.U., Wu, A., Tabor, J.J., Refactoring and optimization of light-switchable Escherichia coli two component systems (2014) ACS Synth Biol, 3, pp. 820-831. , COI: 1:CAS:528:DC%2BC2cXhs1Sisr7J; Möglich, A., Moffat, K., Engineered photoreceptors as novel optogenetic tools (2010) Photochem Photobiol Sci, 9, pp. 1286-1300; Camsund, D., Linblad, P., Jaramillo, A., Genetically engineered light sensors for control bacterial gene expression (2011) Biotechnol J, 6, pp. 826-836. , COI: 1:CAS:528:DC%2BC3MXotlGltb8%3D; Wiltbank, L.B., Kehoe, D.M., Diverse light responses of cyanobacteria mediated by phytochrome superfamily photoreceptor (2019) Nat Rev Microbiol, 17, pp. 37-50. , COI: 1:CAS:528:DC%2BC1cXitFersbvN

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