Changes in intracellular energetic and metabolite states due to increased galactolipid levels in Synechococcus elongatus PCC 7942.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
05 01 2023
05 01 2023
Historique:
received:
27
09
2022
accepted:
20
12
2022
entrez:
5
1
2023
pubmed:
6
1
2023
medline:
10
1
2023
Statut:
epublish
Résumé
The lipid composition of thylakoid membranes is conserved from cyanobacteria to green plants. However, the biosynthetic pathways of galactolipids, the major components of thylakoid membranes, are known to differ substantially between cyanobacteria and green plants. We previously reported on a transformant of the unicellular rod-shaped cyanobacterium Synechococcus elongatus PCC 7942, namely SeGPT, in which the synthesis pathways of the galactolipids monogalactosyldiacylglycerol and digalactosyldiacylglycerol are completely replaced by those of green plants. SeGPT exhibited increased galactolipid content and could grow photoautotrophically, but its growth rate was slower than that of wild-type S. elongatus PCC 7942. In the present study, we investigated pleiotropic effects that occur in SeGPT and determined how its increased lipid content affects cell proliferation. Microscopic observations revealed that cell division and thylakoid membrane development are impaired in SeGPT. Furthermore, physiological analyses indicated that the bioenergetic state of SeGPT is altered toward energy storage, as indicated by increased levels of intracellular ATP and glycogen. We hereby report that we have identified a new promising candidate as a platform for material production by modifying the lipid synthesis system in this way.
Identifiants
pubmed: 36604524
doi: 10.1038/s41598-022-26760-4
pii: 10.1038/s41598-022-26760-4
pmc: PMC9816115
doi:
Substances chimiques
Galactolipids
0
Glycogen
9005-79-2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
259Commentaires et corrections
Type : ErratumIn
Informations de copyright
© 2023. The Author(s).
Références
Luan, G., Zhang, S. & Lu, X. Engineering cyanobacteria chassis cells toward more efficient photosynthesis. Curr. Opin. Biotechnol. 62, 1–6. https://doi.org/10.1016/j.copbio.2019.07.004 (2020).
doi: 10.1016/j.copbio.2019.07.004
pubmed: 31505401
Kato, Y., Inabe, K., Hidese, R., Kondo, A. & Hasunuma, T. Metabolomics-based engineering for biofuel and bio-based chemical production in microalgae and cyanobacteria: A review. Bioresour. Technol. 344, 126196. https://doi.org/10.1016/j.biortech.2021.126196 (2022).
doi: 10.1016/j.biortech.2021.126196
pubmed: 34710610
Meng, X., Liu, L. & Chen, X. Bacterial photosynthesis: state-of-the-art in light-driven carbon fixation in engineered bacteria. Curr. Opin. Microbiol. 69, 102174. https://doi.org/10.1016/j.mib.2022.102174 (2022).
doi: 10.1016/j.mib.2022.102174
pubmed: 35797938
Treece, T. R., Gonzales, J. N., Pressley, J. R. & Atsumi, S. Synthetic biology approaches for improving chemical production in cyanobacteria. Front. Bioeng. Biotechnol. 10, 869195. https://doi.org/10.3389/fbioe.2022.869195 (2022).
doi: 10.3389/fbioe.2022.869195
pubmed: 35372310
pmcid: 8965691
Liu, D. et al. Engineering biology approaches for food and nutrient production by cyanobacteria. Curr. Opin. Biotechnol. 67, 1–6. https://doi.org/10.1016/j.copbio.2020.09.011 (2021).
doi: 10.1016/j.copbio.2020.09.011
pubmed: 33129046
Jaiswal, D., Sahasrabuddhe, D. & Wangikar, P. P. Cyanobacteria as cell factories: The roles of host and pathway engineering and translational research. Curr. Opin. Biotechnol. 73, 314–322. https://doi.org/10.1016/j.copbio.2021.09.010 (2022).
doi: 10.1016/j.copbio.2021.09.010
pubmed: 34695729
Wang, W., Liu, X. & Lu, X. Engineering cyanobacteria to improve photosynthetic production of alka(e)nes. Biotechnol. Biofuels 6, 69. https://doi.org/10.1186/1754-6834-6-69 (2013).
doi: 10.1186/1754-6834-6-69
pubmed: 23641684
pmcid: 3679977
Katayama, N., Iijima, H. & Osanai, T. Production of bioplastic compounds by genetically manipulated and metabolic engineered cyanobacteria. Adv. Exp. Med. Biol. 1080, 155–169. https://doi.org/10.1007/978-981-13-0854-3_7 (2018).
doi: 10.1007/978-981-13-0854-3_7
pubmed: 30091095
Liang, F. Y., Lindberg, P. & Lindblad, P. Engineering photoautotrophic carbon fixation for enhanced growth and productivity. Sustain. Energ Fuels 2, 2583–2600. https://doi.org/10.1039/c8se00281a (2018).
doi: 10.1039/c8se00281a
Meng, H. et al. Over-expression of an electron transport protein OmcS provides sufficient NADH for D-lactate production in cyanobacterium. Biotechnol. Biofuels 14, 109. https://doi.org/10.1186/s13068-021-01956-4 (2021).
doi: 10.1186/s13068-021-01956-4
pubmed: 33926521
pmcid: 8082822
Ungerer, J., Lin, P. C., Chen, H. Y. & Pakrasi, H. B. Adjustments to photosystem stoichiometry and electron transfer proteins are key to the remarkably fast growth of the cyanobacterium Synechococcus elongatus UTEX 2973. MBio https://doi.org/10.1128/mBio.02327-17 (2018).
doi: 10.1128/mBio.02327-17
pubmed: 29437923
pmcid: 5801466
Wada, H. & Murata, N. Synechocystis Pcc6803 mutants defective in desaturation of fatty-acids. Plant Cell Physiol. 30, 971–978 (1989).
Dorne, A. J., Joyard, J. & Douce, R. Do thylakoids really contain phosphatidylcholine?. Proc. Natl. Acad. Sci. U S A 87, 71–74. https://doi.org/10.1073/pnas.87.1.71 (1990).
doi: 10.1073/pnas.87.1.71
pubmed: 11607049
pmcid: 53201
Sato, N. & Murata, N. Lipid biosynthesis in the blue-green-alga, Anabaena-variabilis.1. Lipid Classes. Biochem. Biophys. Acta. 710, 271–278 (1982).
doi: 10.1016/0005-2760(82)90109-6
Awai, K. et al. Comparative genomic analysis revealed a gene for monoglucosyldiacylglycerol synthase, an enzyme for photosynthetic membrane lipid synthesis in cyanobacteria. Plant Physiol. 141, 1120–1127. https://doi.org/10.1104/pp.106.082859 (2006).
doi: 10.1104/pp.106.082859
pubmed: 16714404
pmcid: 1489894
Awai, K., Ohta, H. & Sato, N. Oxygenic photosynthesis without galactolipids. Proc. Natl. Acad. Sci. U S A 111, 13571–13575. https://doi.org/10.1073/pnas.1403708111 (2014).
doi: 10.1073/pnas.1403708111
pubmed: 25197079
pmcid: 4169966
Shimojima, M. et al. Cloning of the gene for monogalactosyldiacylglycerol synthase and its evolutionary origin. Proc. Natl. Acad. Sci. U S A 94, 333–337. https://doi.org/10.1073/pnas.94.1.333 (1997).
doi: 10.1073/pnas.94.1.333
pubmed: 8990209
pmcid: 19336
Dormann, P., Balbo, I. & Benning, C. Arabidopsis galactolipid biosynthesis and lipid trafficking mediated by DGD1. Science 284, 2181–2184. https://doi.org/10.1126/science.284.5423.2181 (1999).
doi: 10.1126/science.284.5423.2181
pubmed: 10381884
Awai, K., Watanabe, H., Benning, C. & Nishida, I. Digalactosyldiacylglycerol is required for better photosynthetic growth of Synechocystis sp PCC6803 under phosphate limitation. Plant Cell Physiol. 48, 1517–1523. https://doi.org/10.1093/pcp/pcm134 (2007).
doi: 10.1093/pcp/pcm134
pubmed: 17932115
Sakurai, I., Mizusawa, N., Wada, H. & Sato, N. Digalactosyldiacylglycerol is required for stabilization of the oxygen-evolving complex in photosystem II. Plant Physiol. 145, 1361–1370. https://doi.org/10.1104/pp.107.106781 (2007).
doi: 10.1104/pp.107.106781
pubmed: 17921339
pmcid: 2151706
Jarvis, P. et al. Galactolipid deficiency and abnormal chloroplast development in the Arabidopsis MGD synthase 1 mutant. Proc. Natl. Acad. Sci. U S A 97, 8175–8179. https://doi.org/10.1073/pnas.100132197 (2000).
doi: 10.1073/pnas.100132197
pubmed: 10869420
pmcid: 16689
Kobayashi, K., Kondo, M., Fukuda, H., Nishimura, M. & Ohta, H. Galactolipid synthesis in chloroplast inner envelope is essential for proper thylakoid biogenesis, photosynthesis, and embryogenesis. Proc. Natl. Acad. Sci. U S A 104, 17216–17221. https://doi.org/10.1073/pnas.0704680104 (2007).
doi: 10.1073/pnas.0704680104
pubmed: 17940034
pmcid: 2040463
Shimojima, M., Tsuchiya, M. & Ohta, H. Temperature-dependent hyper-activation of monoglucosyldiacylglycerol synthase is post-translationally regulated in Synechocystis sp. PCC 6803. FEBS Lett. 583, 2372–2376. https://doi.org/10.1016/j.febslet.2009.06.033 (2009).
doi: 10.1016/j.febslet.2009.06.033
pubmed: 19549521
Apdila, E. T., Inoue, S., Shimojima, M. & Awai, K. Complete replacement of the galactolipid biosynthesis pathway with a plant-type pathway in the cyanobacterium Synechococcus elongatus PCC 7942. Plant Cell Physiol. 61, 1661–1668. https://doi.org/10.1093/pcp/pcaa090 (2020).
doi: 10.1093/pcp/pcaa090
pubmed: 32645152
Yamauchi, Y., Kaniya, Y., Kaneko, Y. & Hihara, Y. Physiological roles of the cyAbrB transcriptional regulator pair Sll0822 and Sll0359 in Synechocystis sp. strain PCC 6803. J. Bacteriol. 193, 3702–3709. https://doi.org/10.1128/JB.00284-11 (2011).
doi: 10.1128/JB.00284-11
pubmed: 21642457
pmcid: 3147526
Imashimizu, M. et al. Regulation of F0F1-ATPase from Synechocystis sp. PCC 6803 by gamma and epsilon subunits is significant for light/dark adaptation. J. Biol. Chem. 286, 26595–26602. https://doi.org/10.1074/jbc.M111.234138 (2011).
doi: 10.1074/jbc.M111.234138
pubmed: 21610078
pmcid: 3143624
Kondo, K. et al. The phototroph-specific β-hairpin structure of the γ subunit of F
doi: 10.1016/j.jbc.2021.101027
pubmed: 34339736
pmcid: 8390522
Mullineaux, C. W. & Sarcina, M. Probing the dynamics of photosynthetic membranes with fluorescence recovery after photobleaching. Trends Plant Sci. 7, 237–240. https://doi.org/10.1016/s1360-1385(02)02283-5 (2002).
doi: 10.1016/s1360-1385(02)02283-5
pubmed: 12049914
Casella, S. et al. Dissecting the native architecture and dynamics of cyanobacterial photosynthetic machinery. Mol. Plant 10, 1434–1448. https://doi.org/10.1016/j.molp.2017.09.019 (2017).
doi: 10.1016/j.molp.2017.09.019
pubmed: 29017828
Huokko, T. et al. Probing the biogenesis pathway and dynamics of thylakoid membranes. Nat. Commun. 12, 3475. https://doi.org/10.1038/s41467-021-23680-1 (2021).
doi: 10.1038/s41467-021-23680-1
pubmed: 34108457
pmcid: 8190092
Rast, A. et al. Biogenic regions of cyanobacterial thylakoids form contact sites with the plasma membrane. Nat. Plants 5, 436–446. https://doi.org/10.1038/s41477-019-0399-7 (2019).
doi: 10.1038/s41477-019-0399-7
pubmed: 30962530
Mullineaux, C. W. & Liu, L. N. Membrane dynamics in phototrophic bacteria. Annu. Rev. Microbiol. 74, 633–654. https://doi.org/10.1146/annurev-micro-020518-120134 (2020).
doi: 10.1146/annurev-micro-020518-120134
pubmed: 32689916
Jouhet, J. Importance of the hexagonal lipid phase in biological membrane organization. Front. Plant Sci. 4, 494. https://doi.org/10.3389/fpls.2013.00494 (2013).
doi: 10.3389/fpls.2013.00494
pubmed: 24348497
pmcid: 3848315
Gad, M. et al. Accumulation of plant galactolipid affects cell morphology of Escherichia coli. Biochem. Biophys. Res. Commun. 286, 114–118. https://doi.org/10.1006/bbrc.2001.5358 (2001).
doi: 10.1006/bbrc.2001.5358
pubmed: 11485316
Aronsson, H. et al. Monogalactosyldiacylglycerol deficiency in Arabidopsis affects pigment composition in the prolamellar body and impairs thylakoid membrane energization and photoprotection in leaves. Plant Physiol. 148, 580–592. https://doi.org/10.1104/pp.108.123372 (2008).
doi: 10.1104/pp.108.123372
pubmed: 18641085
pmcid: 2528128
Holzl, G. et al. The role of diglycosyl lipids in photosynthesis and membrane lipid homeostasis in Arabidopsis. Plant Physiol. 150, 1147–1159. https://doi.org/10.1104/pp.109.139758 (2009).
doi: 10.1104/pp.109.139758
pubmed: 19403724
pmcid: 2705026
Wu, W. et al. Monogalactosyldiacylglycerol deficiency in tobacco inhibits the cytochrome b6f-mediated intersystem electron transport process and affects the photostability of the photosystem II apparatus. Biochim Biophys. Acta 1827, 709–722. https://doi.org/10.1016/j.bbabio.2013.02.013 (2013).
doi: 10.1016/j.bbabio.2013.02.013
pubmed: 23466336
Mi, H. L., Endo, T., Ogawa, T. & Asada, K. Thylakoid membrane-bound, nadph-specific pyridine-nucleotide dehydrogenase complex mediates cyclic electron-transport in the cyanobacterium Synechocystis Sp Pcc-68038. Plant Cell Physiol. 36, 661–668 (1995).
Battchikova, N. et al. Identification of novel Ssl0352 protein (NdhS), essential for efficient operation of cyclic electron transport around photosystem I, in NADPH: Plastoquinone oxidoreductase (NDH-1) complexes of Synechocystis sp. PCC 6803. J. Biol. Chem. 286, 36992–37001. https://doi.org/10.1074/jbc.M111.263780 (2011).
doi: 10.1074/jbc.M111.263780
pubmed: 21880717
pmcid: 3196108
Zhang, C. et al. Structural insights into NDH-1 mediated cyclic electron transfer. Nat. Commun. 11, 888. https://doi.org/10.1038/s41467-020-14732-z (2020).
doi: 10.1038/s41467-020-14732-z
pubmed: 32060291
pmcid: 7021789
Battchikova, N. & Aro, E. M. Cyanobacterial NDH-1 complexes: Multiplicity in function and subunit composition. Physiol. Plant 131, 22–32. https://doi.org/10.1111/j.1399-3054.2007.00929.x (2007).
doi: 10.1111/j.1399-3054.2007.00929.x
pubmed: 18251921
Pan, X. et al. Structural basis for electron transport mechanism of complex I-like photosynthetic NAD(P)H dehydrogenase. Nat. Commun. 11, 610. https://doi.org/10.1038/s41467-020-14456-0 (2020).
doi: 10.1038/s41467-020-14456-0
pubmed: 32001694
pmcid: 6992706
Lan, E. I. & Liao, J. C. ATP drives direct photosynthetic production of 1-butanol in cyanobacteria. Proc. Natl. Acad. Sci. U S A 109, 6018–6023. https://doi.org/10.1073/pnas.1200074109 (2012).
doi: 10.1073/pnas.1200074109
pubmed: 22474341
pmcid: 3341080
Hasunuma, T. et al. Overexpression of flv3 improves photosynthesis in the cyanobacterium Synechocystis sp. PCC6803 by enhancement of alternative electron flow. Biotechnol. Biofuels 7, 493. https://doi.org/10.1186/s13068-014-0183-x (2014).
doi: 10.1186/s13068-014-0183-x
pubmed: 25649610
pmcid: 4300077
Deschoenmaeker, F. et al. Thioredoxin pathway in Anabaena sp. PCC 7120: Activity of NADPH-thioredoxin reductase C. J. Biochem. 169, 709–719. https://doi.org/10.1093/jb/mvab014 (2021).
doi: 10.1093/jb/mvab014
pubmed: 33537746
Baker, N. R. Chlorophyll fluorescence: A probe of photosynthesis in vivo. Annu. Rev. Plant Biol. 59, 89–113. https://doi.org/10.1146/annurev.arplant.59.032607.092759 (2008).
doi: 10.1146/annurev.arplant.59.032607.092759
pubmed: 18444897