Tuning Gene Expression by Phosphate in the Methanogenic Archaeon Methanococcus maripaludis
Abstract
Methanococcus maripaludis is a rapidly growing, hydrogenotrophic, and genetically tractable methanogen with unique capabilities to convert formate and CO2 to CH4. The existence of genome-scale metabolic models and an established, robust system for both large-scale and continuous cultivation make it amenable for industrial applications. However, the lack of molecular tools for differential gene expression has hindered its application as a microbial cell factory to produce biocatalysts and biochemicals. In this study, a library of differentially regulated promoters was designed and characterized based on the pst promoter, which responds to the inorganic phosphate concentration in the growth medium. Gene expression increases by 4- to 6-fold when the medium phosphate drops to growthlimiting concentrations. Hence, this regulated system decouples growth from heterologous gene expression without the need for adding an inducer. The minimal pst promoter is identified and contains a conserved AT-rich region, a factor B recognition element, and a TATA box for phosphate-dependent regulation. Rational changes to the factor B recognition element and start codon had no significant impact on expression; however, changes to the transcription start site and the 5' untranslated region resulted in the differential protein production with regulation remaining intact. Compared to a previous expression system based uponmore »
- Authors:
-
[1];
- Department of Microbiology, University of Georgia, Athens, Georgia 30602, United States
- Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, Texas 77030, United States
- Corporate Strategic Research, ExxonMobil Research & Engineering Company, Annandale, New Jersey 08801, United States
- Publication Date:
- Research Org.:
- Univ. of Georgia, Athens, GA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1826833
- Alternate Identifier(s):
- OSTI ID: 1831428; OSTI ID: 1831807
- Grant/Contract Number:
- SC0018028
- Resource Type:
- Published Article
- Journal Name:
- ACS Synthetic Biology
- Additional Journal Information:
- Journal Name: ACS Synthetic Biology Journal Volume: 10 Journal Issue: 11; Journal ID: ISSN 2161-5063
- Publisher:
- American Chemical Society
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 60 APPLIED LIFE SCIENCES; heterologous gene expression; gene regulation; promoter; phosphate; 5' untranslated region; Methanococcus maripaludis; heterologous gene expression, gene regulation, promoter, phosphate, 5′ untranslated region, Methanococcus maripaludis
Citation Formats
Akinyemi, Taiwo S., Shao, Nana, Lyu, Zhe, Drake, Ian J., Liu, Yuchen, and Whitman, William B. Tuning Gene Expression by Phosphate in the Methanogenic Archaeon Methanococcus maripaludis. United States: N. p., 2021.
Web. doi:10.1021/acssynbio.1c00322.
Akinyemi, Taiwo S., Shao, Nana, Lyu, Zhe, Drake, Ian J., Liu, Yuchen, & Whitman, William B. Tuning Gene Expression by Phosphate in the Methanogenic Archaeon Methanococcus maripaludis. United States. https://doi.org/10.1021/acssynbio.1c00322
Akinyemi, Taiwo S., Shao, Nana, Lyu, Zhe, Drake, Ian J., Liu, Yuchen, and Whitman, William B. Tue .
"Tuning Gene Expression by Phosphate in the Methanogenic Archaeon Methanococcus maripaludis". United States. https://doi.org/10.1021/acssynbio.1c00322.
@article{osti_1826833,
title = {Tuning Gene Expression by Phosphate in the Methanogenic Archaeon Methanococcus maripaludis},
author = {Akinyemi, Taiwo S. and Shao, Nana and Lyu, Zhe and Drake, Ian J. and Liu, Yuchen and Whitman, William B.},
abstractNote = {Methanococcus maripaludis is a rapidly growing, hydrogenotrophic, and genetically tractable methanogen with unique capabilities to convert formate and CO2 to CH4. The existence of genome-scale metabolic models and an established, robust system for both large-scale and continuous cultivation make it amenable for industrial applications. However, the lack of molecular tools for differential gene expression has hindered its application as a microbial cell factory to produce biocatalysts and biochemicals. In this study, a library of differentially regulated promoters was designed and characterized based on the pst promoter, which responds to the inorganic phosphate concentration in the growth medium. Gene expression increases by 4- to 6-fold when the medium phosphate drops to growthlimiting concentrations. Hence, this regulated system decouples growth from heterologous gene expression without the need for adding an inducer. The minimal pst promoter is identified and contains a conserved AT-rich region, a factor B recognition element, and a TATA box for phosphate-dependent regulation. Rational changes to the factor B recognition element and start codon had no significant impact on expression; however, changes to the transcription start site and the 5' untranslated region resulted in the differential protein production with regulation remaining intact. Compared to a previous expression system based upon the histone promoter, this regulated expression system resulted in significant improvements in the expression of a key methanogenic enzyme complex, methyl-coenzyme M reductase, and the potentially toxic arginine methyltransferase MmpX.},
doi = {10.1021/acssynbio.1c00322},
journal = {ACS Synthetic Biology},
number = 11,
volume = 10,
place = {United States},
year = {Tue Oct 19 00:00:00 EDT 2021},
month = {Tue Oct 19 00:00:00 EDT 2021}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1021/acssynbio.1c00322
https://doi.org/10.1021/acssynbio.1c00322
Other availability
Search WorldCat to find libraries that may hold this journal
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Fine-Tuned Protein Production in Methanosarcina acetivorans C2A
journal, June 2018
- Karim, Ann A.; Gestaut, Daniel R.; Fincker, Maeva
- ACS Synthetic Biology, Vol. 7, Issue 8
Two Transcription Factors Related with the Eucaryal Transcription Factors TATA-binding Protein and Transcription Factor IIB Direct Promoter Recognition by an Archaeal RNA Polymerase
journal, November 1996
- Hausner, Winfried; Wettach, Jörn; Hethke, Carina
- Journal of Biological Chemistry, Vol. 271, Issue 47
Regulatory Response of Methanococcus maripaludis to Alanine, an Intermediate Nitrogen Source
journal, October 2002
- Lie, T. J.; Leigh, J. A.
- Journal of Bacteriology, Vol. 184, Issue 19
Effects of H2 and Formate on Growth Yield and Regulation of Methanogenesis in Methanococcus maripaludis
journal, January 2013
- Costa, K. C.; Yoon, S. H.; Pan, M.
- Journal of Bacteriology, Vol. 195, Issue 7
Engineering Robust Production Microbes for Large-Scale Cultivation
journal, June 2019
- Wehrs, Maren; Tanjore, Deepti; Eng, Thomas
- Trends in Microbiology, Vol. 27, Issue 6
Facilitating Protein Expression with Portable 5′-UTR Secondary Structures in Bacillus licheniformis
journal, April 2020
- Xiao, Jun; Peng, Bing; Su, Zhaowei
- ACS Synthetic Biology, Vol. 9, Issue 5
Initiation of translation in prokaryotes and eukaryotes
journal, July 1999
- Kozak, Marilyn
- Gene, Vol. 234, Issue 2, p. 187-208
An alternative resource allocation strategy in the chemolithoautotrophic archaeon Methanococcus maripaludis
journal, April 2021
- Müller, Albert L.; Gu, Wenyu; Patsalo, Vadim
- Proceedings of the National Academy of Sciences, Vol. 118, Issue 16
Bypassing the Need for the Transcriptional Activator EarA through a Spontaneous Deletion in the BRE Portion of the fla Operon Promoter in Methanococcus maripaludis
journal, July 2017
- Ding, Yan; Berezuk, Alison; Khursigara, Cezar M.
- Frontiers in Microbiology, Vol. 8
Comparison of mRNA features affecting translation initiation and reinitiation
journal, October 2012
- Osterman, Ilya A.; Evfratov, Sergey A.; Sergiev, Petr V.
- Nucleic Acids Research, Vol. 41, Issue 1
Parallel evolution of transcriptome architecture during genome reorganization
journal, July 2011
- Yoon, S. H.; Reiss, D. J.; Bare, J. C.
- Genome Research, Vol. 21, Issue 11, p. 1892-1904
Methanogenesis
journal, July 2018
- Lyu, Zhe; Shao, Nana; Akinyemi, Taiwo
- Current Biology, Vol. 28, Issue 13
Divergent transcriptional and translational signals in Archaea
journal, January 2005
- Torarinsson, Elfar; Klenk, Hans-Peter; Garrett, Roger A.
- Environmental Microbiology, Vol. 7, Issue 1
Elucidation of the biosynthesis of the methane catalyst coenzyme F430
journal, February 2017
- Moore, Simon J.; Sowa, Sven T.; Schuchardt, Christopher
- Nature, Vol. 543, Issue 7643
Abundance of 4Feâ4S motifs in the genomes of methanogens and other prokaryotes
journal, October 2004
- Major, Tiffany A.; Burd, Henry; Whitman, William B.
- FEMS Microbiology Letters, Vol. 239, Issue 1
The conserved ribonuclease aCPSF1 triggers genome-wide transcription termination of Archaea via a 3′-end cleavage mode
journal, August 2020
- Yue, Lei; Li, Jie; Zhang, Bing
- Nucleic Acids Research, Vol. 48, Issue 17
A genome-scale metabolic model of Methanococcus maripaludis S2 for CO 2 capture and conversion to methane
journal, January 2014
- Goyal, Nishu; Widiastuti, Hanifah; Karimi, I. A.
- Mol. BioSyst., Vol. 10, Issue 5
Methanogenesis marker protein 10 (Mmp10) from Methanosarcina acetivorans is a radical S -adenosylmethionine methylase that unexpectedly requires cobalamin
journal, May 2019
- Radle, Matthew I.; Miller, Danielle V.; Laremore, Tatiana N.
- Journal of Biological Chemistry, Vol. 294, Issue 31
Quantitative proteomics of nutrient limitation in the hydrogenotrophic methanogen Methanococcus maripaludis
journal, January 2009
- Xia, Qiangwei; Wang, Tiansong; Hendrickson, Erik L.
- BMC Microbiology, Vol. 9, Issue 1
Selective electrocatalytic conversion of methane to fuels and chemicals
journal, November 2018
- Xie, Shunji; Lin, Shengqi; Zhang, Qinghong
- Journal of Energy Chemistry, Vol. 27, Issue 6
Influence of Nitrogen and Phosphorus on Microalgal Growth, Biomass, Lipid, and Fatty Acid Production: An Overview
journal, February 2021
- Yaakob, Maizatul Azrina; Mohamed, Radin Maya Saphira Radin; Al-Gheethi, Adel
- Cells, Vol. 10, Issue 2
Global Responses of Methanococcus maripaludis to Specific Nutrient Limitations and Growth Rate
journal, January 2008
- Hendrickson, E. L.; Liu, Y.; Rosas-Sandoval, G.
- Journal of Bacteriology, Vol. 190, Issue 6
Transplanting the pathway engineering toolbox to methanogens
journal, October 2019
- Lyu, Zhe; Whitman, William B.
- Current Opinion in Biotechnology, Vol. 59
Electricity from methane by reversing methanogenesis
journal, May 2017
- McAnulty, Michael J.; G. Poosarla, Venkata; Kim, Kyoung-Yeol
- Nature Communications, Vol. 8, Issue 1
The biosynthetic pathway of coenzyme F430 in methanogenic and methanotrophic archaea
journal, October 2016
- Zheng, Kaiyuan; Ngo, Phong D.; Owens, Victoria L.
- Science, Vol. 354, Issue 6310
Metabolic Engineering and Synthetic Biology: Synergies, Future, and Challenges
journal, March 2019
- García-Granados, Raúl; Lerma-Escalera, Jordy Alexis; Morones-Ramírez, José R.
- Frontiers in Bioengineering and Biotechnology, Vol. 7
A new and efficient phosphate starvation inducible expression system for Lactococcus lactis
journal, July 2008
- Sirén, Noora; Salonen, Kalle; Leisola, Matti
- Applied Microbiology and Biotechnology, Vol. 79, Issue 5
Cysteine Is Not the Sulfur Source for Iron-Sulfur Cluster and Methionine Biosynthesis in the Methanogenic Archaeon Methanococcus maripaludis
journal, August 2010
- Liu, Yuchen; Sieprawska-Lupa, Magdalena; Whitman, William B.
- Journal of Biological Chemistry, Vol. 285, Issue 42
Evolution of the archaeal and mammalian information processing systems: towards an archaeal model for human disease
journal, June 2016
- Lyu, Zhe; Whitman, William B.
- Cellular and Molecular Life Sciences, Vol. 74, Issue 2
In vivo definition of an archaeal promoter
journal, April 1995
- Palmer, J. R.; Daniels, C. J.
- Journal of Bacteriology, Vol. 177, Issue 7
Functionally distinct genes regulated by hydrogen limitation and growth rate in methanogenic Archaea
journal, May 2007
- Hendrickson, E. L.; Haydock, A. K.; Moore, B. C.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 21
The archaeal RNA chaperone TRAM0076 shapes the transcriptome and optimizes the growth of Methanococcus maripaludis
journal, August 2019
- Li, Jie; Zhang, Bo; Zhou, Liguang
- PLOS Genetics, Vol. 15, Issue 8
Identification of a unique Radical SAM methyltransferase required for the sp3-C-methylation of an arginine residue of methyl-coenzyme M reductase
journal, May 2018
- Deobald, Darja; Adrian, Lorenz; Schöne, Christian
- Scientific Reports, Vol. 8, Issue 1
Control regions of an archaeal gene
journal, December 1991
- Hausner, Winfried; Frey, Gerhard; Thomm, Michael
- Journal of Molecular Biology, Vol. 222, Issue 3
Flux measurements and maintenance energy for carbon dioxide utilization by Methanococcus maripaludis
journal, September 2015
- Goyal, Nishu; Padhiary, Mrutyunjay; Karimi, Iftekhar A.
- Microbial Cell Factories, Vol. 14, Issue 1
Identification of the first transcriptional activator of an archaellum operon in a euryarchaeon: Transcriptional activator of archaellum operon
journal, July 2016
- Ding, Yan; Nash, John; Berezuk, Alison
- Molecular Microbiology, Vol. 102, Issue 1
Factor requirements for transcription in the Archaeon Sulfolobus shibatae
journal, May 1997
- Qureshi, S. A.
- The EMBO Journal, Vol. 16, Issue 10
Methyl (Alkyl)-Coenzyme M Reductases: Nickel F-430-Containing Enzymes Involved in Anaerobic Methane Formation and in Anaerobic Oxidation of Methane or of Short Chain Alkanes
journal, April 2019
- Thauer, Rudolf K.
- Biochemistry, Vol. 58, Issue 52
Exploring Hydrogenotrophic Methanogenesis: a Genome Scale Metabolic Reconstruction of Methanococcus maripaludis
journal, October 2016
- Richards, Matthew A.; Lie, Thomas J.; Zhang, Juan
- Journal of Bacteriology, Vol. 198, Issue 24
Temperature, template topology, and factor requirements of archaeal transcription
journal, December 1998
- Bell, S. D.; Jaxel, C.; Nadal, M.
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 26
Engineering glucose metabolism of Escherichia coli under nitrogen starvation
journal, January 2017
- Chubukov, Victor; Desmarais, John James; Wang, George
- npj Systems Biology and Applications, Vol. 3, Issue 1
Mechanism and regulation of transcription in archaea
journal, April 2001
- Bell, Stephen D.; Jackson, Stephen P.
- Current Opinion in Microbiology, Vol. 4, Issue 2
A Flexible System for Cultivation of Methanococcus and Other Formate-Utilizing Methanogens
journal, January 2017
- Long, Feng; Wang, Liangliang; Lupa, Boguslaw
- Archaea, Vol. 2017
Effects of growth conditions on archaellation and N-glycosylation in Methanococcus maripaludis
journal, February 2016
- Ding, Yan; Lau, Zoe; Logan, Susan M.
- Microbiology, Vol. 162, Issue 2
Identification and Genomic Analysis of Transcription Factors in Archaeal Genomes Exemplifies Their Functional Architecture and Evolutionary Origin
journal, February 2010
- Perez-Rueda, E.; Janga, S. C.
- Molecular Biology and Evolution, Vol. 27, Issue 6
Regulation of nif Expression in Methanococcus maripaludis
journal, February 2005
- Lie, Thomas J.; Wood, Gwendolyn E.; Leigh, John A.
- Journal of Biological Chemistry, Vol. 280, Issue 7
Regulation of Translation in Haloarchaea: 5′- and 3′-UTRs Are Essential and Have to Functionally Interact In Vivo
journal, February 2009
- Brenneis, Mariam; Soppa, Jörg
- PLoS ONE, Vol. 4, Issue 2
The archaeal TFIIEα homologue facilitates transcription initiation by enhancing TATA‐box recognition
journal, February 2001
- Bell, Stephen D.; Brinkman, Arie B.; van der Oost, John
- EMBO reports, Vol. 2, Issue 2
Recent Progresses in Constructing the Highly Efficient Ni Based Catalysts With Advanced Low-Temperature Activity Toward CO2 Methanation
journal, April 2020
- Lv, Chufei; Xu, Leilei; Chen, Mindong
- Frontiers in Chemistry, Vol. 8
Assembly of Methyl Coenzyme M Reductase in the Methanogenic Archaeon Methanococcus maripaludis
journal, January 2018
- Lyu, Zhe; Chou, Chau-Wen; Shi, Hao
- Journal of Bacteriology, Vol. 200, Issue 7
Elements of an archaeal promoter defined by mutational analysis
journal, January 1992
- Hain, Johannes; Reiter, Wolf-Dieter; Hüdepohl, Uwe
- Nucleic Acids Research, Vol. 20, Issue 20
Identification of a glycolytic regulon in the archaea Pyrococcus and Thermococcus
journal, July 2006
- van de Werken, Harmen J. G.; Verhees, Corné H.; Akerboom, Jasper
- FEMS Microbiology Letters, Vol. 260, Issue 1
ViennaRNA Package 2.0
journal, November 2011
- Lorenz, Ronny; Bernhart, Stephan H.; Höner zu Siederdissen, Christian
- Algorithms for Molecular Biology, Vol. 6, Issue 1
Modulating Heterologous Gene Expression with Portable mRNA-Stabilizing 5′-UTR Sequences
journal, July 2018
- Viegas, Sandra C.; Apura, Patrícia; Martínez-García, Esteban
- ACS Synthetic Biology, Vol. 7, Issue 9
The structural basis for the oriented assembly of a TBP/TFB/promoter complex
journal, November 1999
- Littlefield, O.; Korkhin, Y.; Sigler, P. B.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 24
An auto-inducible phosphate-controlled expression system of Bacillus licheniformis
journal, January 2019
- Trung, Nguyen Thanh; Hung, Nguyen Minh; Thuan, Nguyen Huy
- BMC Biotechnology, Vol. 19, Issue 1
Reversing methanogenesis to capture methane for liquid biofuel precursors
journal, January 2016
- Soo, Valerie W. C.; McAnulty, Michael J.; Tripathi, Arti
- Microbial Cell Factories, Vol. 15, Issue 1
Activation of archaeal transcription by recruitment of the TATA-binding protein
journal, April 2003
- Ouhammouch, M.; Dewhurst, R. E.; Hausner, W.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 9
Posttranslational Methylation of Arginine in Methyl Coenzyme M Reductase Has a Profound Impact on both Methanogenesis and Growth of Methanococcus maripaludis
journal, January 2020
- Lyu, Zhe; Shao, Nana; Chou, Chau-Wen
- Journal of Bacteriology, Vol. 202, Issue 3
A Fully Recombinant System for Activator-dependent Archaeal Transcription
journal, December 2004
- Ouhammouch, Mohamed; Werner, Finn; Weinzierl, Robert O. J.
- Journal of Biological Chemistry, Vol. 279, Issue 50
Biosynthesis of puromycin by Streptomyces alboniger: Characterization of puromycin N-acetyltransferase
journal, December 1985
- Vara, Jesus; Perez-Gonzalez, Jose A.; Jimenez, Antonio
- Biochemistry, Vol. 24, Issue 27
Supported Catalysts for CO2 Methanation: A Review
journal, February 2017
- Frontera, Patrizia; Macario, Anastasia; Ferraro, Marco
- Catalysts, Vol. 7, Issue 12
Crystal structure of a key enzyme for anaerobic ethane activation
journal, July 2021
- Hahn, Cedric J.; Lemaire, Olivier N.; Kahnt, Jörg
- Science, Vol. 373, Issue 6550
Determinants of transcription initiation by archaeal RNA polymerase
journal, December 2005
- Bartlett, Michael S.
- Current Opinion in Microbiology, Vol. 8, Issue 6
A biochemical framework for anaerobic oxidation of methane driven by Fe(III)-dependent respiration
journal, April 2018
- Yan, Zhen; Joshi, Prachi; Gorski, Christopher A.
- Nature Communications, Vol. 9, Issue 1
New methods for tightly regulated gene expression and highly efficient chromosomal integration of cloned genes for Methanosarcina species
journal, January 2008
- Guss, Adam M.; Rother, Michael; Zhang, Jun Kai
- Archaea, Vol. 2, Issue 3