Deciphering the transcriptional regulation of the catabolism of lignin-derived aromatics in Rhodococcus opacus PD630

Diao, Jinjin; Carr, Rhiannon; Moon, Tae Seok

doi:10.1038/s42003-022-04069-2

Deciphering the transcriptional regulation of the catabolism of lignin-derived aromatics in Rhodococcus opacus PD630

Journal Article · Wed Oct 19 00:00:00 EDT 2022 · Communications Biology

DOI:https://doi.org/10.1038/s42003-022-04069-2· OSTI ID:1893787

Diao, Jinjin; ;

Abstract

Rhodococcus opacus PD630 has considerable potential as a platform for valorizing lignin due to its innate “biological funneling” pathways. However, the transcriptional regulation of the aromatic catabolic pathways and the mechanisms controlling aromatic catabolic operons in response to different aromatic mixtures are still underexplored. Here, we identified and studied the transcription factors for aromatic degradation using GFP-based sensors and comprehensive deletion analyses. Our results demonstrate that the funneling pathways for phenol, guaiacol, 4-hydroxybenzoate, and vanillate are controlled by transcriptional activators. The two different branches of the β-ketoadipate pathway, however, are controlled by transcriptional repressors. Additionally, promoter activity assays revealed that the substrate hierarchy in R. opacus may be ascribed to the transcriptional cross-regulation of the individual aromatic funneling pathways. These results provide clues to clarify the molecule-level mechanisms underlying the complex regulation of aromatic catabolism, which facilitates the development of R. opacus as a promising chassis for valorizing lignin.

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Research Organization:: Washington Univ., St. Louis, MO (United States)

Sponsoring Organization:: USDA; USDOE; USDOE Office of Science (SC)

Grant/Contract Number:: SC0018324

OSTI ID:: 1893787

Alternate ID(s):: OSTI ID: 2420761

Journal Information:: Communications Biology, Journal Name: Communications Biology Journal Issue: 1 Vol. 5; ISSN 2399-3642

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (50)

Cybernetic modeling of growth in mixed, substitutable substrate environments: Preferential and simultaneous utilization Ramakrishna, Ramprasad; Ramkrishna, Doraiswami; Konopka, Allan E. Biotechnology and Bioengineering, Vol. 52, Issue 1 https://doi.org/10.1002/(SICI)1097-0290(19961005)52:1<141::AID-BIT14>3.0.CO;2-R	journal	October 1996
Mechanism‐Guided Design of Highly Efficient Protein Secretion and Lipid Conversion for Biomanufacturing and Biorefining Xie, Shangxian; Sun, Su; Lin, Furong Advanced Science https://doi.org/10.1002/advs.201801980	journal	May 2019
Dynamic models of metabolism: Review of the cybernetic approach Ramkrishna, Doraiswami; Song, Hyun-Seob AIChE Journal, Vol. 58, Issue 4 https://doi.org/10.1002/aic.13734	journal	February 2012
Positive feedback in cellular control systems Mitrophanov, Alexander Y.; Groisman, Eduardo A. BioEssays, Vol. 30, Issue 6 https://doi.org/10.1002/bies.20769	journal	January 2008
Formation of intracytoplasmic lipid inclusions by Rhodococcus opacus strain PD630 Alvarez, Hector M.; Mayer, Frank; Fabritius, Dirk Archives of Microbiology, Vol. 165, Issue 6 https://doi.org/10.1007/s002030050341	journal	June 1996
Analysis of catRABC operon for catechol degradation from phenol-degrading Rhodococcus erythropolis Veselý, M.; Knoppová, M.; Nešvera, J. Applied Microbiology and Biotechnology, Vol. 76, Issue 1 https://doi.org/10.1007/s00253-007-0997-6	journal	May 2007
Mapping the diversity of microbial lignin catabolism: experiences from the eLignin database Brink, Daniel P.; Ravi, Krithika; Lidén, Gunnar Applied Microbiology and Biotechnology, Vol. 103, Issue 10 https://doi.org/10.1007/s00253-019-09692-4	journal	April 2019
Benzoate Catabolite Repression of the Phenol Degradation in Acinetobacter calcoaceticus PHEA-2 Zhan, Yuhua; Yu, Haiying; Yan, Yongliang Current Microbiology, Vol. 59, Issue 4 https://doi.org/10.1007/s00284-009-9446-3	journal	July 2009
From lignin to valuable products–strategies, challenges, and prospects Wang, Hongliang; Pu, Yunqiao; Ragauskas, Arthur Bioresource Technology, Vol. 271 https://doi.org/10.1016/j.biortech.2018.09.072	journal	January 2019
Lignin valorization by bacterial genus Pseudomonas: State-of-the-art review and prospects Kumar, Manish; You, Siming; Beiyuan, Jingzi Bioresource Technology, Vol. 320 https://doi.org/10.1016/j.biortech.2020.124412	journal	January 2021
A field of dreams: Lignin valorization into chemicals, materials, fuels, and health-care products Becker, Judith; Wittmann, Christoph Biotechnology Advances, Vol. 37, Issue 6 https://doi.org/10.1016/j.biotechadv.2019.02.016	journal	November 2019
Opportunities and challenges in biological lignin valorization Beckham, Gregg T.; Johnson, Christopher W.; Karp, Eric M. Current Opinion in Biotechnology, Vol. 42 https://doi.org/10.1016/j.copbio.2016.02.030	journal	December 2016
Bacterial gene regulation in diauxic and non-diauxic growth Narang, Atul; Pilyugin, Sergei S. Journal of Theoretical Biology, Vol. 244, Issue 2 https://doi.org/10.1016/j.jtbi.2006.08.007	journal	January 2007
Engineering Acinetobacter baylyi ADP1 for mevalonate production from lignin-derived aromatic compounds Arvay, Erika; Biggs, Bradley W.; Guerrero, Laura Metabolic Engineering Communications, Vol. 13 https://doi.org/10.1016/j.mec.2021.e00173	journal	December 2021
The mechanisms of carbon catabolite repression in bacteria Deutscher, Josef Current Opinion in Microbiology, Vol. 11, Issue 2, p. 87-93 https://doi.org/10.1016/j.mib.2008.02.007	journal	April 2008
Opportunities, recent trends and challenges of integrated biorefinery: Part II Maity, Sunil K. Renewable and Sustainable Energy Reviews, Vol. 43 https://doi.org/10.1016/j.rser.2014.08.075	journal	March 2015
Synthetic Biology towards Engineering Microbial Lignin Biotransformation Yaguchi, Allison L.; Lee, Stephen J.; Blenner, Mark A. Trends in Biotechnology, Vol. 39, Issue 10 https://doi.org/10.1016/j.tibtech.2021.02.003	journal	October 2021
Multi-omic elucidation of aromatic catabolism in adaptively evolved Rhodococcus opacus Henson, William R.; Campbell, Tayte; DeLorenzo, Drew M. Metabolic Engineering, Vol. 49 https://doi.org/10.1016/j.ymben.2018.06.009	journal	September 2018
A concerted systems biology analysis of phenol metabolism in Rhodococcus opacus PD630 Roell, Garrett W.; Carr, Rhiannon R.; Campbell, Tayte Metabolic Engineering, Vol. 55 https://doi.org/10.1016/j.ymben.2019.06.013	journal	September 2019
Engineering Pseudomonas putida for efficient aromatic conversion to bioproduct using high throughput screening in a bioreactor Eng, Thomas; Banerjee, Deepanwita; Lau, Andrew K. Metabolic Engineering, Vol. 66 https://doi.org/10.1016/j.ymben.2021.04.015	journal	July 2021
An Improved CRISPR Interference Tool to Engineer Rhodococcus opacus DeLorenzo, Drew M.; Diao, Jinjin; Carr, Rhiannon ACS Synthetic Biology, Vol. 10, Issue 4 https://doi.org/10.1021/acssynbio.0c00591	journal	March 2021
Development of Chemical and Metabolite Sensors for Rhodococcus opacus PD630 DeLorenzo, Drew M.; Henson, William R.; Moon, Tae Seok ACS Synthetic Biology, Vol. 6, Issue 10 https://doi.org/10.1021/acssynbio.7b00192	journal	June 2017
Molecular Toolkit for Gene Expression Control and Genome Modification in Rhodococcus opacus PD630 DeLorenzo, Drew M.; Rottinghaus, Austin G.; Henson, William R. ACS Synthetic Biology, Vol. 7, Issue 2 https://doi.org/10.1021/acssynbio.7b00416	journal	January 2018
Enzymatic assembly of DNA molecules up to several hundred kilobases Gibson, Daniel G.; Young, Lei; Chuang, Ray-Yuan Nature Methods, Vol. 6, Issue 5, p. 343-345 https://doi.org/10.1038/nmeth.1318	journal	April 2009
Network motifs: theory and experimental approaches Alon, Uri Nature Reviews Genetics, Vol. 8, Issue 6 https://doi.org/10.1038/nrg2102	journal	June 2007
Carbon catabolite repression in bacteria: many ways to make the most out of nutrients Görke, Boris; Stülke, Jörg Nature Reviews Microbiology, Vol. 6, Issue 8, p. 613-624 https://doi.org/10.1038/nrmicro1932	journal	August 2008
Towards lignin consolidated bioprocessing: simultaneous lignin depolymerization and product generation by bacteria Salvachúa, Davinia; Karp, Eric M.; Nimlos, Claire T. Green Chemistry, Vol. 17, Issue 11 https://doi.org/10.1039/C5GC01165E	journal	January 2015
The complete genome of Rhodococcus sp. RHA1 provides insights into a catabolic powerhouse McLeod, M. P.; Warren, R. L.; Hsiao, W. W. L. Proceedings of the National Academy of Sciences, Vol. 103, Issue 42, p. 15582-15587 https://doi.org/10.1073/pnas.0607048103	journal	October 2006
Lignin valorization through integrated biological funneling and chemical catalysis Linger, J. G.; Vardon, D. R.; Guarnieri, M. T. Proceedings of the National Academy of Sciences, Vol. 111, Issue 33, p. 12013-12018 https://doi.org/10.1073/pnas.1410657111	journal	August 2014
Decoding how a soil bacterium extracts building blocks and metabolic energy from ligninolysis provides road map for lignin valorization Varman, Arul M.; He, Lian; Follenfant, Rhiannon Proceedings of the National Academy of Sciences, Vol. 113, Issue 40 https://doi.org/10.1073/pnas.1606043113	journal	September 2016
Comparative transcriptomics elucidates adaptive phenol tolerance and utilization in lipid-accumulating Rhodococcus opacus PD630 Yoneda, Aki; Henson, William R.; Goldner, Nicholas K. Nucleic Acids Research, Vol. 44, Issue 5 https://doi.org/10.1093/nar/gkw055	journal	February 2016
Regulatory noise in prokaryotic promoters: how bacteria learn to respond to novel environmental signals Lorenzo, Victor; Pérez-Martín, José Molecular Microbiology, Vol. 19, Issue 6 https://doi.org/10.1111/j.1365-2958.1996.tb02463.x	journal	March 1996
Strict and direct transcriptional repression of the pobA gene by benzoate avoids 4-hydroxybenzoate degradation in the pollutant degrader bacterium Cupriavidus necator JMP134 : Benzoate repression of 4-hydroxybenzoate catabolism Donoso, Raúl A.; Pérez-Pantoja, Danilo; González, Bernardo Environmental Microbiology, Vol. 13, Issue 6 https://doi.org/10.1111/j.1462-2920.2011.02470.x	journal	March 2011
Reversible accumulation of p-hydroxybenzoate and catechol determines the sequential decomposition of phenolic compounds in mixed substrate cultivations in pseudomonads Heinaru, Eeva; Viggor, Signe; Vedler, Eve FEMS Microbiology Ecology, Vol. 37, Issue 1 https://doi.org/10.1111/j.1574-6941.2001.tb00855.x	journal	August 2001
The Path Forward for Biofuels and Biomaterials Ragauskas, Arthur J.; Williams, Charlotte K.; Davison, Brian H. Science, Vol. 311, Issue 5760, p. 484-489 https://doi.org/10.1126/science.1114736	journal	January 2006
Challenges in Engineering Microbes for Biofuels Production Stephanopoulos, Gregory Science, Vol. 315, Issue 5813, p. 801-804 https://doi.org/10.1126/science.1139612	journal	February 2007
Benzoate Catabolite Repression of the Phthalate Degradation Pathway in Rhodococcus sp. Strain DK17 Choi, Ki Young; Zylstra, Gerben J.; Kim, Eungbin Applied and Environmental Microbiology, Vol. 73, Issue 4 https://doi.org/10.1128/AEM.02379-06	journal	December 2006
Repression of Phenol Catabolism by Organic Acids in Ralstonia eutropha Ampe, Frédéric; Léonard, David; Lindley, Nicholas D. Applied and Environmental Microbiology, Vol. 64, Issue 1 https://doi.org/10.1128/AEM.64.1.1-6.1998	journal	January 1998
Effect of Aromatic Compounds on Cellular Fatty Acid Composition of Rhodococcus opacus Tsitko, Irina V.; Zaitsev, Gennadi M.; Lobanok, Anatoli G. Applied and Environmental Microbiology, Vol. 65, Issue 2 https://doi.org/10.1128/AEM.65.2.853-855.1999	journal	January 1999
Transcriptional Cross-Regulation of the Catechol and Protocatechuate Branches of the -Ketoadipate Pathway Contributes to Carbon Source-Dependent Expression of the Acinetobacter sp. Strain ADP1 pobA Gene Brzostowicz, P. C.; Reams, A. B.; Clark, T. J. Applied and Environmental Microbiology, Vol. 69, Issue 3 https://doi.org/10.1128/AEM.69.3.1598-1606.2003	journal	March 2003
PcaO Positively Regulates pcaHG of the β-Ketoadipate Pathway in Corynebacterium glutamicum Zhao, Ke-Xin; Huang, Yan; Chen, Xi Journal of Bacteriology, Vol. 192, Issue 6 https://doi.org/10.1128/JB.01338-09	journal	March 2010
Bacterial Transcriptional Regulators for Degradation Pathways of Aromatic Compounds Tropel, D.; van der Meer, J. R. Microbiology and Molecular Biology Reviews, Vol. 68, Issue 3 https://doi.org/10.1128/MMBR.68.3.474-500.2004	journal	September 2004
Characterization of the pcaR regulatory gene from Pseudomonas putida, which is required for the complete degradation of p-hydroxybenzoate. Romero-Steiner, S.; Parales, R. E.; Harwood, C. S. Journal of Bacteriology, Vol. 176, Issue 18 https://doi.org/10.1128/jb.176.18.5771-5779.1994	journal	September 1994
Repression of 4-hydroxybenzoate transport and degradation by benzoate: a new layer of regulatory control in the Pseudomonas putida beta-ketoadipate pathway. Nichols, N. N.; Harwood, C. S. Journal of bacteriology, Vol. 177, Issue 24 https://doi.org/10.1128/jb.177.24.7033-7040.1995	journal	January 1995
Novel nuclear magnetic resonance spectroscopy methods demonstrate preferential carbon source utilization by Acinetobacter calcoaceticus. Gaines, G. L.; Smith, L.; Neidle, E. L. Journal of bacteriology, Vol. 178, Issue 23 https://doi.org/10.1128/jb.178.23.6833-6841.1996	journal	January 1996
Molecular Biology of the LysR Family of Transcriptional Regulators Schell, M. A. Annual Review of Microbiology, Vol. 47, Issue 1 https://doi.org/10.1146/annurev.mi.47.100193.003121	journal	October 1993
Regulation of Carbon Catabolism in Bacillus Species Stülke, J.; Hillen, W. Annual Review of Microbiology, Vol. 54, Issue 1 https://doi.org/10.1146/annurev.micro.54.1.849	journal	October 2000
The Wood-Based Biorefinery: A Source of Carbon Fiber? Gellerstedt, Göran; Sjöholm, Elisabeth; Brodin, Ida The Open Agriculture Journal, Vol. 4, Issue 1 https://doi.org/10.2174/1874331501004010119	journal	December 2010
Recent Advances in Biosensor Technology for Potential Applications – An Overview Vigneshvar, S.; Sudhakumari, C. C.; Senthilkumaran, Balasubramanian Frontiers in Bioengineering and Biotechnology, Vol. 4 https://doi.org/10.3389/fbioe.2016.00011	journal	February 2016
Bacterial Transformation of Aromatic Monomers in Softwood Black Liquor Navas, Laura E.; Dexter, Gara; Liu, Jie Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.735000	journal	September 2021

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