Consequences of the deletion of the major specialized metabolite biosynthetic pathways of Streptomyces coelicolor on the metabolome and lipidome of this strain.


Journal

Microbial biotechnology
ISSN: 1751-7915
Titre abrégé: Microb Biotechnol
Pays: United States
ID NLM: 101316335

Informations de publication

Date de publication:
Aug 2024
Historique:
received: 26 01 2024
accepted: 13 07 2024
medline: 2 8 2024
pubmed: 2 8 2024
entrez: 2 8 2024
Statut: ppublish

Résumé

Chassis strains, derived from Streptomyces coelicolor M145, deleted for one or more of its four main specialized metabolites biosynthetic pathways (CPK, CDA, RED and ACT), in various combinations, were constructed for the heterologous expression of specialized metabolites biosynthetic pathways of various types and origins. To determine consequences of these deletions on the metabolism of the deleted strains comparative lipidomic and metabolomic analyses of these strains and of the original strain were carried out. These studies unexpectedly revealed that the deletion of the peptidic clusters, RED and/or CDA, in a strain deleted for the ACT cluster, resulted into a great increase in the triacylglycerol (TAG) content, whereas the deletion of polyketide clusters, ACT and CPK had no impact on TAG content. Low or high TAG content of the deleted strains was correlated with abundance or paucity in amino acids, respectively, reflecting high or low activity of oxidative metabolism. Hypotheses based on what is known on the bio-activity and the nature of the precursors of these specialized metabolites are proposed to explain the unexpected consequences of the deletion of these pathways on the metabolism of the bacteria and on the efficiency of the deleted strains as chassis strains.

Identifiants

pubmed: 39093579
doi: 10.1111/1751-7915.14538
doi:

Substances chimiques

Triglycerides 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e14538

Subventions

Organisme : PROBIO3 "Investment for the Future Biotechnologies et Bioressources"
ID : n°11-BTBR-0003
Organisme : ANR INNOVANTIBIO from the "Direction Générale des Armées" (DGA) et "l'Agence de l'Innovation de Défense" (AID)
ID : ANR-17-ASTR-0018
Organisme : ANR BioSound-IR
ID : ANR-15-CE09-0002
Organisme : Public Institutions: CNRS and University Paris-Saclay

Informations de copyright

© 2024 The Author(s). Microbial Biotechnology published by John Wiley & Sons Ltd.

Références

Abbas, A.S. & Edwards, C. (1990) Effects of metals on Streptomyces coelicolor growth and actinorhodin production. Applied and Environmental Microbiology, 56, 675–680.
AlOkda, A. & Van Raamsdonk, J.M. (2023) Evolutionarily conserved role of thioredoxin systems in determining longevity. Antioxidants (Basel), 12, 944.
Anastassiadis, S., Aivasidis, A. & Wandrey, C. (2002) Citric acid production by Candida strains under intracellular nitrogen limitation. Applied Microbiology and Biotechnology, 60, 81–87.
Apel, C., Levasseur, M., Lejeune, C., Korch, S.B., Guerard, F., David, M. et al. (2023) Metabolic adjustments in response to ATP spilling by the small DX protein in a Streptomyces strain. Frontiers in Cell and Development Biology, 11, 1129009.
Arabolaza, A., Rodriguez, E., Altabe, S., Alvarez, H. & Gramajo, H. (2008) Multiple pathways for triacylglycerol biosynthesis in Streptomyces coelicolor. Applied and Environmental Microbiology, 74, 2573–2582.
Bang, S.S., Baumann, P. & Sawyer, M.H. (1977) Properties of 1‐phosphofructokinase from Pseudomonas putida. Canadian Journal of Microbiology, 23, 721–725.
Bednarz, B., Kotowska, M. & Pawlik, K.J. (2019) Multi‐level regulation of coelimycin synthesis in Streptomyces coelicolor A3(2). Applied Microbiology and Biotechnology, 103, 6423–6434.
Bentley, S.D., Chater, K.F., Cerdeno‐Tarraga, A.M., Challis, G.L., Thomson, N.R., James, K.D. et al. (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature, 417, 141–147.
Berdy, J. (2005) Bioactive microbial metabolites. Journal of Antibiotics (Tokyo), 58, 1–26.
Bhowmick, S., Shenouda, M.L. & Tschowri, N. (2023) Osmotic stress responses and the biology of the second messenger c‐di‐AMP in Streptomyces. Microlife, 4, uqad020.
Bibb, M.J. (2005) Regulation of secondary metabolism in streptomycetes. Current Opinion in Microbiology, 8, 208–215.
Bibb, M.J., Janssen, G.R. & Ward, J.M. (1985) Cloning and analysis of the promoter region of the erythromycin resistance gene (ermE) of Streptomyces erythraeus. Gene, 38, 215–226.
Bishop, A., Fielding, S., Dyson, P. & Herron, P. (2004) Systematic insertional mutagenesis of a streptomycete genome: a link between osmoadaptation and antibiotic production. Genome Research, 14, 893–900.
Coze, F., Gilard, F., Tcherkez, G., Virolle, M.J. & Guyonvarch, A. (2013) Carbon‐flux distribution within Streptomyces coelicolor metabolism: a comparison between the actinorhodin‐producing strain M145 and its non‐producing derivative M1146. PLoS One, 8, e84151.
David, M., Lejeune, C., Abreu, S., Thibessard, A., Leblond, P., Chaminade, P. et al. (2020) Negative correlation between lipid content and antibiotic activity in Streptomyces: general rule and exceptions. Antibiotics (Basel), 9, 280.
Deniset‐Besseau, A., Prater, C.B., Virolle, M.J. & Dazzi, A. (2014) Monitoring TriAcylGlycerols accumulation by atomic force microscopy based infrared spectroscopy in Streptomyces species for biodiesel applications. Journal of Physical Chemistry Letters, 5, 654–658.
Dulermo, T., Lejeune, C., Aybeke, E., Abreu, S., Bleton, J., David, M. et al. (2023) Genome analysis of a variant of Streptomyces coelicolor M145 with high lipid content and poor ability to synthetize antibiotics. Microorganisms, 11, 1470.
Esnault, C., Dulermo, T., Smirnov, A., Askora, A., David, M., Deniset‐Besseau, A. et al. (2017) Strong antibiotic production is correlated with highly active oxidative metabolism in Streptomyces coelicolor M145. Scientific Reports, 7, 200.
Flinspach, K., Westrich, L., Kaysser, L., Siebenberg, S., Gomez‐Escribano, J.P., Bibb, M. et al. (2010) Heterologous expression of the biosynthetic gene clusters of coumermycin A(1), clorobiocin and caprazamycins in genetically modified Streptomyces coelicolor strains. Biopolymers, 93, 823–832.
Furumoto, H., Nanthirudjanar, T., Kume, T., Izumi, Y., Park, S.B., Kitamura, N. et al. (2016) 10‐oxo‐trans‐11‐octadecenoic acid generated from linoleic acid by a gut lactic acid bacterium Lactobacillus plantarum is cytoprotective against oxidative stress. Toxicology and Applied Pharmacology, 296, 1–9.
Godinez, O., Dyson, P., del Sol, R., Barrios‐Gonzalez, J., Millan‐Pacheco, C. & Mejia, A. (2015) Targeting the osmotic stress response for strain improvement of an industrial producer of secondary metabolites. Journal of Microbiology and Biotechnology, 25, 1787–1795.
Gomez‐Escribano, J.P. & Bibb, M.J. (2011) Engineering Streptomyces coelicolor for heterologous expression of secondary metabolite gene clusters. Microbial Biotechnology, 4, 207–215.
Gomez‐Escribano, J.P., Song, L., Fox, D.J., Yeo, V., Bibb, M.J., Challis, G. et al. (2012) Structure and biosynthesis of the unusual polyketide alkaloid coelimycin P1, a metabolic product of the cpk gene cluster of Streptomyces coelicolor M145. Chemical Science, 3, 2716–2720.
Granozzi, C., Billetta, R., Passantino, R., Sollazzo, M. & Puglia, A.M. (1990) A breakdown in macromolecular synthesis preceding differentiation in Streptomyces coelicolor A3(2). Journal of General Microbiology, 136, 713–716.
Guijas, C., Rodriguez, J.P., Rubio, J.M., Balboa, M.A. & Balsinde, J. (2014) Phospholipase A2 regulation of lipid droplet formation. Biochimica et Biophysica Acta, 1841, 1661–1671.
Hashem, I. & Van Impe, J.F.M. (2021) A game theoretic analysis of the dual function of antibiotics. Frontiers in Microbiology, 12, 812788.
Hopwood, D.A. & Wright, H.M. (1983) CDA is a new chromosomally‐determined antibiotic from Streptomyces coelicolor A3(2). Journal of General Microbiology, 129, 3575–3579.
Imlay, J.A. (2019) Where in the world do bacteria experience oxidative stress? Environmental Microbiology, 21, 521–530.
Juguet, M., Lautru, S., Francou, F.X., Nezbedova, S., Leblond, P., Gondry, M. et al. (2009) An iterative nonribosomal peptide synthetase assembles the pyrrole‐amide antibiotic congocidine in Streptomyces ambofaciens. Chemistry & Biology, 16, 421–431.
Kamzolova, S.V., Lunina, J.N., Samoilenko, V.A. & Morgunov, I.G. (2022) Effect of nitrogen concentration on the biosynthesis of citric acid, protein, and lipids in the yeast Yarrowia lipolytica. Biomolecules, 12, 1421.
Lejeune, C., Abreu, S., Chaminade, P., Dulermo, T., David, M., Werten, S. et al. (2021) Impact of phosphate availability on membrane lipid content of the model strains, Streptomyces lividans and Streptomyces coelicolor. Frontiers in Microbiology, 12, 623919.
Li, H., Pan, Y. & Liu, G. (2022) Multiplying the heterologous production of spinosad through tandem amplification of its biosynthetic gene cluster in Streptomyces coelicolor. Microbial Biotechnology, 15, 1550–1560.
Lv, G., Xu, Y., Tu, Y., Cheng, X., Zeng, B., Huang, J. et al. (2021) Effects of nitrogen and phosphorus limitation on fatty acid contents in Aspergillus oryzae. Frontiers in Microbiology, 12, 739569.
Maltsev, Y., Kulikovskiy, M. & Maltseva, S. (2023) Nitrogen and phosphorus stress as a tool to induce lipid production in microalgae. Microbial Cell Factories, 22, 239.
Millan‐Oropeza, A., Henry, C., Blein‐Nicolas, M., Aubert‐Frambourg, A., Moussa, F., Bleton, J. et al. (2017) Quantitative proteomics analysis confirmed oxidative metabolism predominates in Streptomyces coelicolor versus glycolytic metabolism in Streptomyces lividans. Journal of Proteome Research, 16, 2597–2613.
Millan‐Oropeza, A., Rebois, R., David, M., Moussa, F., Dazzi, A., Bleton, J. et al. (2017) Attenuated total reflection Fourier transform infrared (ATR FT‐IR) for rapid determination of microbial cell lipid content: correlation with gas chromatography‐mass spectrometry (GC‐MS). Applied Spectroscopy, 71, 2344–2352.
Newton, G.L., Buchmeier, N. & Fahey, R.C. (2008) Biosynthesis and functions of mycothiol, the unique protective thiol of actinobacteria. Microbiology and Molecular Biology Reviews, 72, 471–494.
Oftadeh, O. & Hatzimanikatis, V. (2024) Genome‐scale models of metabolism and expression predict the metabolic burden of recombinant protein expression. Metabolic Engineering, 84, 109–116.
Okamoto, S., Taguchi, T., Ochi, K. & Ichinose, K. (2009) Biosynthesis of actinorhodin and related antibiotics: discovery of alternative routes for quinone formation encoded in the act gene cluster. Chemistry & Biology, 16, 226–236.
Olukoshi, E.R. & Packter, N.M. (1994) Importance of stored triacylglycerols in Streptomyces: possible carbon source for antibiotics. Microbiology, 140(Pt 4), 931–943.
Pawlik, K., Kotowska, M., Chater, K.F., Kuczek, K. & Takano, E. (2007) A cryptic type I polyketide synthase (cpk) gene cluster in Streptomyces coelicolor A3(2). Archives of Microbiology, 187, 87–99.
Pucer, A., Brglez, V., Payre, C., Pungercar, J., Lambeau, G. & Petan, T. (2013) Group X secreted phospholipase A(2) induces lipid droplet formation and prolongs breast cancer cell survival. Molecular Cancer, 12, 111.
Puglia, A.M., Vohradsky, J. & Thompson, C.J. (1995) Developmental control of the heat‐shock stress regulon in Streptomyces coelicolor. Molecular Microbiology, 17, 737–746.
Santucci, P., Johansen, M.D., Point, V., Poncin, I., Viljoen, A., Cavalier, J.F. et al. (2019) Nitrogen deprivation induces triacylglycerol accumulation, drug tolerance and hypervirulence in mycobacteria. Scientific Reports, 9, 8667.
Shaheryar, Z.A., Khan, M.A., Hameed, H., Zaidi, S.A.A., Anjum, I. & Rahman, M.S.U. (2023) Lauric acid provides neuroprotection against oxidative stress in mouse model of hyperglycaemic stroke. European Journal of Pharmacology, 956, 175990.
Subirats, J., Sharpe, H., Santoro, D. & Topp, E. (2023) Modeling antibiotic concentrations in the vicinity of antibiotic‐producing bacteria at the Micron scale. Applied and Environmental Microbiology, 89, e0026123.
Sulheim, S., Kumelj, T., van Dissel, D., Salehzadeh‐Yazdi, A., Du, C., van Wezel, G.P. et al. (2020) Enzyme‐constrained models and omics analysis of Streptomyces coelicolor reveal metabolic changes that enhance heterologous production. iScience, 23, 101525.
Takano, E., Gramajo, H.C., Strauch, E., Andres, N., White, J. & Bibb, M.J. (1992) Transcriptional regulation of the redD transcriptional activator gene accounts for growth‐phase‐dependent production of the antibiotic undecylprodigiosin in Streptomyces coelicolor A3(2). Molecular Microbiology, 6, 2797–2804.
Tenconi, E., Traxler, M., Tellatin, D., van Wezel, G.P. & Rigali, S. (2020) Prodiginines postpone the onset of sporulation in Streptomyces coelicolor. Antibiotics (Basel), 9, 847.
Tenconi, E., Traxler, M.F., Hoebreck, C., van Wezel, G.P. & Rigali, S. (2018) Production of prodiginines is part of a programmed cell death process in Streptomyces coelicolor. Frontiers in Microbiology, 9, 1742.
Thanapipatsiri, A., Claesen, J., Gomez‐Escribano, J.P., Bibb, M. & Thamchaipenet, A. (2015) A Streptomyces coelicolor host for the heterologous expression of type III polyketide synthase genes. Microbial Cell Factories, 14, 145.
Tian, J., Jiang, Q., Bao, X., Yang, F., Li, Y., Sun, H. et al. (2023) Plant‐derived squalene supplementation improves growth performance and alleviates acute oxidative stress‐induced growth retardation and intestinal damage in piglets. Animal Nutrition, 15, 386–398.
Usenik, A. & Legisa, M. (2010) Evolution of allosteric citrate binding sites on 6‐phosphofructo‐1‐kinase. PLoS One, 5, e15447.
Virolle, M.J. (2020) A challenging view: antibiotics play a role in the regulation of the energetic metabolism of the producing bacteria. Antibiotics (Basel), 9, 83.
Wang, L., Cai, Y., Zhu, L., Guo, H. & Yu, B. (2014) Major role of NAD‐dependent lactate dehydrogenases in the production of l‐lactic acid with high optical purity by the thermophile Bacillus coagulans. Applied and Environmental Microbiology, 80, 7134–7141.
Wang, W., Li, S., Li, Z., Zhang, J., Fan, K., Tan, G. et al. (2020) Harnessing the intracellular triacylglycerols for titer improvement of polyketides in Streptomyces. Nature Biotechnology, 38, 76–83.
Wang, Y., Zhang, S., Zhu, Z., Shen, H., Lin, X., Jin, X. et al. (2018) Systems analysis of phosphate‐limitation‐induced lipid accumulation by the oleaginous yeast Rhodosporidium toruloides. Biotechnology for Biofuels, 11, 148.
Wierzchowska, K., Zieniuk, B., Nowak, D. & Fabiszewska, A. (2021) Phosphorus and nitrogen limitation as a part of the strategy to stimulate microbial lipid biosynthesis. Applied Sciences, 11, 11819.
Wu, S., Hu, C., Jin, G., Zhao, X. & Zhao, Z.K. (2010) Phosphate‐limitation mediated lipid production by Rhodosporidium toruloides. Bioresource Technology, 101, 6124–6129.

Auteurs

Clara Lejeune (C)

Institut de Biologie Intégrative de la Cellule (I2BC, UMR 9198), Université Paris-Saclay, CEA, CNRS, Group MES (Métabolisme Energétique Des Streptomyces), Gif-sur-Yvette, France.

Sonia Abreu (S)

UFR Pharmacie, Université Paris-Saclay, CNRS, Group «Lipides, Systèmes Analytiques et Biologiques (Lip(Sys)2», Orsay, France.

Florence Guérard (F)

Institut Des Sciences Des Plantes (IPS2, UMR 9213), Université Paris-Saclay, CNRS, Plateforme «SPOmics-Métabolome», Gif-sur-Yvette, France.

Ahmed Askora (A)

Institut de Biologie Intégrative de la Cellule (I2BC, UMR 9198), Université Paris-Saclay, CEA, CNRS, Group MES (Métabolisme Energétique Des Streptomyces), Gif-sur-Yvette, France.
Department of Botany and Microbiology, Faculty of Science, Zagazig University, Zagazig, Egypt.

Michelle David (M)

Institut de Biologie Intégrative de la Cellule (I2BC, UMR 9198), Université Paris-Saclay, CEA, CNRS, Group MES (Métabolisme Energétique Des Streptomyces), Gif-sur-Yvette, France.

Pierre Chaminade (P)

UFR Pharmacie, Université Paris-Saclay, CNRS, Group «Lipides, Systèmes Analytiques et Biologiques (Lip(Sys)2», Orsay, France.

Bertrand Gakière (B)

Institut Des Sciences Des Plantes (IPS2, UMR 9213), Université Paris-Saclay, CNRS, Plateforme «SPOmics-Métabolome», Gif-sur-Yvette, France.

Marie-Joelle Virolle (MJ)

Institut de Biologie Intégrative de la Cellule (I2BC, UMR 9198), Université Paris-Saclay, CEA, CNRS, Group MES (Métabolisme Energétique Des Streptomyces), Gif-sur-Yvette, France.

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