Intracellular accumulation of c-di-GMP and its regulation on self-flocculation of the bacterial cells of Zymomonas mobilis.
Zymomonas mobilis
c-di-GMP
chassis
industrial production
microbial cell factories
self-flocculation
Journal
Biotechnology and bioengineering
ISSN: 1097-0290
Titre abrégé: Biotechnol Bioeng
Pays: United States
ID NLM: 7502021
Informations de publication
Date de publication:
Nov 2023
Nov 2023
Historique:
revised:
26
06
2023
received:
27
03
2023
accepted:
17
07
2023
pubmed:
1
8
2023
medline:
1
8
2023
entrez:
1
8
2023
Statut:
ppublish
Résumé
Zymomonas mobilis is an emerging chassis for being engineered to produce bulk products due to its unique glycolysis through the Entner-Doudoroff pathway with less ATP produced for lower biomass accumulation and higher product yield. When self-flocculated, the bacterial cells are more productive, since they can self-immobilize within bioreactors for high density, and are more tolerant to stresses for higher product titers, but this morphology needs to be controlled properly to avoid internal mass transfer limitation associated with their strong self-flocculation. Herewith we explored the regulation of cyclic diguanosine monophosphate (c-di-GMP) on self-flocculation of the bacterial cells through activating cellulose biosynthesis. While ZMO1365 and ZMO0919 with GGDEF domains for diguanylate cyclase activity catalyze c-di-GMP biosynthesis, ZMO1487 with an EAL domain for phosphodiesterase activity catalyzes c-di-GMP degradation, but ZMO1055 and ZMO0401 contain the dual domains with phosphodiesterase activity predominated. Since c-di-GMP is synthesized from GTP, the intracellular accumulation of this signal molecule through deactivating phosphodiesterase activity is preferred for activating cellulose biosynthesis to flocculate the bacterial cells, because such a strategy exerts less perturbance on intracellular processes regulated by GTP. These discoveries are significant for not only engineering unicellular Z. mobilis strains with the self-flocculating morphology to boost production but also understanding mechanism underlying c-di-GMP biosynthesis and degradation in the bacterium.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3234-3243Subventions
Organisme : National Natural Science Foundation of China
Informations de copyright
© 2023 Wiley Periodicals LLC.
Références
Akoopie, A., Arriola, J. T., Magde, D., & Müller, U. F. (2021). A GTP-synthesizing ribozyme selected by metabolic coupling to an RNA polymerase ribozyme. Science Advances, 7, eabj7487.
Attwater, J., Raguram, A., Morgunov, A. S., Gianni, E., & Holliger, P. (2018). Ribozyme-catalysed RNA synthesis using triplet building blocks. eLife, 7, e35255.
Cao, L. Y., Yang, Y. F., Zhang, X., Chen, Y. H., Yao, J. W., Wang, X., Xia, J., Liu, C. G., Yang, S. H., Römling, U., & Bai, F. W. (2022). Deciphering molecular mechanism underlying self-flocculation of Zymomonas mobilis for robust production. Applied and Environmental Microbiology, 88(9), 0239821.
Carreón-Rodríguez, O. E., Gutiérrez-Ríos, R. M., Acosta, J. L., Martinez, A., & Cevallos, M. A. (2019). Phenotypic and genomic analysis of Zymomonas mobilis ZM4 mutants with enhanced ethanol tolerance. Biotechnology Reports, 23, e00328.
Cherfils, J., & Zeghouf, M. (2011). Chronicles of the GTPase switch. Nature Chemical Biology, 7, 494-495.
Dong, H. W., Bao, J., Ryu, D. D. Y., & Zhong, J. J. (2011). Design and construction of improved new vectors for Zymomonas mobilis recombinants. Biotechnology and Bioengineering, 108, 1616-1627.
Endalur Gopinarayanan, V., & Nair, N. U. (2019). Pentose metabolism in Saccharomyces cerevisiae: The need to engineer global regulatory systems. Biotechnology Journal, 14, 1800364.
Gombert, A. K., & van Maris, A. J. (2015). Improving conversion yield of fermentable sugars into fuel ethanol in 1st generation yeast-based production processes. Current Opinion in Biotechnology, 33, 81-86.
Gong, Z., Nielsen, J., & Zhou, Y. J. (2017). Engineering robustness of microbial cell factories. Biotechnology Journal, 12, 1700014.
Guan, N., Li, J., Shin, H., Du, G., Chen, J., & Liu, L. (2017). Microbial response to environmental stresses: From fundamental mechanisms to practical applications. Applied Microbiology and Biotechnology, 101, 3991-4008.
Güvener, Z. T., & Harwood, C. S. (2007). Subcellular location characteristics of the Pseudomonas aeruginosa GGDEF protein, WspR, indicate that it produces cyclic-di-GMP in response to growth on surfaces. Molecular Microbiology, 66, 1459-1473.
He, M., Wu, B., Qin, H., Ruan, Z., Tan, F., Wang, J., Shui, Z., Dai, L., Zhu, Q., Pan, K., Tang, X., Wang, W., & Hu, Q. (2014). Zymomonas mobilis: A novel platform for future biorefineries. Biotechnology for Biofuels, 7, 101.
Hengge, R. (2021). High-specificity local and global c-di-GMP signaling. Trends in Microbiology, 29, 993-1003.
Hoang, T. T., Karkhoff-Schweizer, R. R., Kutchma, A. J., & Schweizer, H. P. (1998). A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: Application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene, 212, 77-86.
Hu, D., Wang, Z., He, M., & Ma, Y. (2021). Functional gene identification and corresponding tolerant mechanism of high furfural-tolerant Zymomonas mobilis strain F211. Frontiers in Microbiology, 12, 736583.
Jenal, U., Reinders, A., & Lori, C. (2012). Cyclic di-GMP: Second messenger extraordinaire. Nature Reviews Microbiology, 15, 217-284.
Jones-Burrage, S. E., Kremer, T. A., & McKinlay, J. B. (2019). Cell aggregation and aerobic respiration are important for Zymomonas mobilis ZM4 survival in an aerobic minimal medium. Applied and Environmental Microbiology, 85(10), e00193-19.
Kalnenieks, U. (2006). Physiology of Zymomonas mobilis: Some unanswered questions. Advances in Microbial Physiology, 51, 73-117.
Kuchma, S. L., Brothers, K. M., Merritt, J. H., Liberati, N. T., Ausubel, F. M., & O'toole, G. A. (2007). BifA, a cyclic-di-GMP phosphodiesterase, inversely regulates biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. Journal of Bacteriology, 189, 8165-8178.
Ling, H., Teo, W., Chen, B. B., Leong, S. S. J., & Chang, M. W. (2014). Microbial tolerance engineering toward biochemical production: From lignocellulose to products. Current Opinion in Biotechnology, 29, 99-106.
Li, R., Shen, W., Yang, Y., Du, J., Li, M., & Yang, S. (2021). Investigation of the impact of a broad range of temperatures on the physiological and transcriptional profiles of Zymomonas mobilis ZM4 for high-temperature-tolerant recombinant strain development. Biotechnology for Biofuels, 14, 146.
Li, X., Thomason, L. C., Sawitzke, J. A., Costantino, N., & Court, D. L. (2013). Positive and negative selection using the tetA-sacB cassette: Recombineering and P1 transduction in Escherichia coli. Nucleic Acids Research, 41, e204.
Lindenberg, S., Klauck, G., Pesavento, C., Klauck, E., & Hengge, R. (2013). The EAL domain protein YciR acts as a trigger enzyme in a c-di-GMP signalling cascade in E. coli biofilm control. The EMBO Journal, 32, 2001-2014.
Lori, C., Ozaki, S., Steiner, S., et al. (2015). Cyclic di-GMP acts as a cell cycle oscillator to drive chromosome replication. Nature, 523, 236-239.
Masuho, I., Balaji, S., Muntean, B. S., et al. (2020). A global map of G protein signaling regulation by RGS proteins. Cell, 183, 503-521.
Mienda, B. S., & Dräger, A. (2021). Genome-scale metabolic modeling of Escherichia coli and its chassis design for synthetic biology applications. In M. A. Marchisio (Ed.), Computational methods in synthetic biology (Vol. 2189, pp. 217-229). Springer Nature.
Mitsui, R., & Yamada, R. (2021). Saccharomyces cerevisiae as a microbial cell factory. In V. Singh (Ed.), Microbial cell factories engineering for production of biomolecules (pp. 319-333). Academic Press.
Morgan, J. L., McNamara, J. T., & Zimmer, J. (2014). Mechanism of activation of bacterial cellulose synthase by cyclic di-GMP. Nature Structural & Molecular Biology, 21, 489-496.
Nesbitt, N. M., Arora, D. P., Johnson, R. A., & Boon, E. M. (2015). Modification of a bi-functional diguanylate cyclase-phosphodiesterase to efficiently produce cyclic diguanylate monophosphate. Biotechnology Reports (Amsterdam, Netherlands), 7, 30-37.
Nogueira, C. C., Padilha, C. E. A., Dantas, J. M. M., Medeiros, F. G. M., Guilherme, A. A., Souza, D. F. S., & Santos, E. S. (2021). In-situ detoxification strategies to boost bioalcohol production from lignocellulosic biomass. Renewable Energy, 180, 914-936.
Petchiappan, A., Naik, S. Y., & Chatterji, D. (2020). Tracking the homeostasis of second messenger cyclic-di-GMP in bacteria. Biophysical Reviews, 12, 719-730.
Puligundla, P., Smogrovicova, D., Mok, C., & Obulam, V. S. R. (2019). A review of recent advances in high gravity ethanol fermentation. Renewable Energy, 133, 1366-1379.
Ross, P., Weinhouse, H., Aloni, Y., Michaeli, D., Weinberger-Ohana, P., Mayer, R., Braun, S., de Vroom, E., van der Marel, G. A., van Boom, J. H., & Benziman, M. (1987). Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature, 325, 279-281.
Rutkis, R., Strazdina, I., Balodite, E., Lasa, Z., Galinina, N., & Kalnenieks, U. (2016). The low energy-coupling respiration in Zymomonas mobilis accelerates flux in the Entner-Doudoroff pathway. PLoS One, 11, e0153866.
Schirmer, T. (2016). c-di-GMP synthesis: Structural aspects of evolution, catalysis and regulation. Journal of Molecular Biology, 428, 3683-3701.
Thongsomboon, W., Werby, S. H., & Cegelski, L. (2020). Evaluation of phosphoethanolamine cellulose production among bacterial communities using Congo red fluorescence. Journal of Bacteriology, 202, e00030-20.
Trivedi, A., Mavi, P. S., Bhatt, D., & Kumar, A. (2016). Thiol reductive stress induces cellulose-anchored biofilm formation in Mycobacterium tuberculosis. Nature Communications, 7, 11392.
Ute Römling, U., & Amikam, D. (2006). Cyclic di-GMP as a second messenger. Current Opinion in Microbiology, 9, 218-228.
Wolff, D. W., Bianchi-Smiraglia, A., & Nikiforov, M. A. (2022). Compartmentalization and regulation of GTP in control of cellular phenotypes. Trends in Molecular Medicine, 28, 758-769.
Xia, J., Liu, C. G., Zhao, X. Q., Xiao, Y., Xia, X. X., & Bai, F. W. (2018). Contribution of cellulose synthesis, formation of fibrils and their entanglement to the self-flocculation of Zymomonas mobilis. Biotechnology and Bioengineering, 115, 2714-2725.
Xia, J., Yang, Y. F., Liu, C. G., Yang, S. H., & Bai, F. W. (2019). Engineering Zymomonas mobilis for robust cellulosic ethanol production. Trends in Biotechnology, 37, 960-972.
Xu, J., Kim, J., Koestler, B. J., Choi, J. H., Waters, C. M., & Fuqua, C. (2013). Genetic analysis of Agrobacterium tumefaciens unipolar polysaccharide production reveals complex integrated control of the motile-to-sessile switch. Molecular Microbiology, 89, 929-948.
Yang, Q., Yang, Y., Tang, Y., Wang, X., Chen, Y., Shen, W., Zhan, Y., Gao, J., Wu, B., He, M. X., Chen, S. W., & Yang, S. H. (2020). Development and characterization of acidic-pH-tolerant mutants of Zymomonas mobilis through adaptation and next-generation sequencing-based genome resequencing and RNA-Seq. Biotechnology for Biofuels, 13, 1-17.
Yang, S., Mohagheghi, A., Franden, M. A., Chou, Y. C., Chen, X., Dowe, N., Himmel, M. E., & Zhang, M. (2016). Metabolic engineering of Zymomonas mobilis for 2,3-butanediol production from lignocellulosic biomass sugars. Biotechnology for Biofuels, 9, 189.
Zhang, M., Eddy, C., Deanda, K., Finkelstei, M., & Picataggio, S. (1995). Metabolic engineering of a pentose metabolism pathway in ethanologenic Zymomonas mobilis. Science, 67(5195), 240-243.
Zhao, N., Bai, Y., Liu, C. G., Zhao, X. Q., Xu, J. F., & Ba, F. W. (2014). Flocculating Zymomonas mobilis is a promising host to be engineered for fuel ethanol production from lignocellulosic biomass. Biotechnology Journal, 9, 362-371.
Zhao, X. Q., & Bai, F. W. (2009). Yeast flocculation: New story in fuel ethanol production. Biotechnology Advances, 27, 849-856.