Biochemical and genetic studies define the functions of methylthiotransferases in methanogenic and methanotrophic archaea

Boswinkle, Kaleb; Dinh, Thuc-Anh; Allen, Kylie D.

doi:10.3389/fmicb.2023.1304671

Title: Biochemical and genetic studies define the functions of methylthiotransferases in methanogenic and methanotrophic archaea

Journal Article · 23 November 2023 · Frontiers in Microbiology

DOI: https://doi.org/10.3389/fmicb.2023.1304671 · OSTI ID:2228923

Boswinkle, Kaleb ^[1]; Dinh, Thuc-Anh ^[2]; Allen, Kylie D. ^[2]

Virginia Polytechnic Institute and State University (Virginia Tech), Blacksburg, VA (United States); University of Florida, Gainesville, FL (United States)
Virginia Polytechnic Institute and State University (Virginia Tech), Blacksburg, VA (United States)

Methylthiotransferases (MTTases) are radical S-adenosylmethionine (SAM) enzymes that catalyze the addition of a methylthio (-SCH₃) group to an unreactive carbon center. These enzymes are responsible for the production of 2-methylthioadenosine (ms²A) derivatives found at position A37 of select tRNAs in all domains of life. Additionally, some bacteria contain the RimO MTTase that catalyzes the methylthiolation of the S12 ribosomal protein. Although the functions of MTTases in bacteria and eukaryotes have been established via detailed genetic and biochemical studies, MTTases from the archaeal domain of life are understudied and the substrate specificity determinants of MTTases remain unclear. Here, we report the in vitro enzymatic activities of an MTTase (C4B56_06395) from a thermophilic Ca. Methanophagales anaerobic methanotroph (ANME) as well as the MTTase from a hyperthermophilic methanogen – MJ0867 from Methanocaldococcus jannaschii. Both enzymes catalyze the methylthiolation of N⁶-threonylcarbamoyladenosine (t⁶A) and N⁶-hydroxynorvalylcarbamoyladenosine (hn⁶A) residues to produce 2-methylthio-N⁶-threonylcarbamoyladenosine (ms²t⁶A) and 2-methylthio-N⁶-hydroxynorvalylcarbamoyladenosine (ms²hn⁶A), respectively. To further assess the function of archaeal MTTases, we analyzed select tRNA modifications in a model methanogen – Methanosarcina acetivorans – and generated a deletion of the MTTase-encoding gene (MA1153). We found that M. acetivorans produces ms²hn⁶A in exponential phase of growth, but does not produce ms²t⁶A in detectable amounts. Upon deletion of MA1153, the ms²A modification was absent, thus confirming the function of MtaB-family MTTases in generating ms²hn⁶A modified nucleosides in select tRNAs.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Virginia Polytechnic Institute and State University (Virginia Tech), Blacksburg, VA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB)

Grant/Contract Number:: SC0022338

OSTI ID:: 2228923

Journal Information:: Frontiers in Microbiology, Vol. 14; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

References (73)

Methanogens: a window into ancient sulfur metabolism Liu, Yuchen; Beer, Laura L.; Whitman, William B. Trends in Microbiology, Vol. 20, Issue 5 https://doi.org/10.1016/j.tim.2012.02.002	journal	May 2012
The host-associated archaeome Borrel, Guillaume; Brugère, Jean-François; Gribaldo, Simonetta Nature Reviews Microbiology, Vol. 18, Issue 11 https://doi.org/10.1038/s41579-020-0407-y	journal	July 2020
tRNA's modifications bring order to gene expression Gustilo, Estella M.; Vendeix, Franck AP; Agris, Paul F. Current Opinion in Microbiology, Vol. 11, Issue 2 https://doi.org/10.1016/j.mib.2008.02.003	journal	April 2008
MODOMICS: An Operational Guide to the Use of the RNA Modification Pathways Database Boccaletto, Pietro; Bagiński, Błażej Methods in Molecular Biology https://doi.org/10.1007/978-1-0716-1307-8_26	book	January 2021
Purification and Use of tRNA for Enzymatic Post-translational Addition of Amino Acids to Proteins Avcilar-Kucukgoze, Irem; Gamper, Howard; Hou, Ya-Ming STAR Protocols, Vol. 1, Issue 3 https://doi.org/10.1016/j.xpro.2020.100207	journal	December 2020
[27] Rapid colorimetric micromethod for the quantitation of complexed iron in biological samples Fish, Wayne W. Methods in Enzymology https://doi.org/10.1016/0076-6879(88)58067-9	book	January 1988
Electron Paramagnetic Resonance Evidence for a Novel Interconversion of [3Fe-4S]+ and [4Fe-4S]+Clusters with Endogenous Iron and Sulfide in Anaerobic Ribonucleotide Reductase Activase in Vitro Liu, Aimin; Gräslund, Astrid Journal of Biological Chemistry, Vol. 275, Issue 17 https://doi.org/10.1074/jbc.275.17.12367	journal	April 2000
Functional characterization of the YmcB and YqeV tRNA methylthiotransferases of Bacillus subtilis Anton, Brian P.; Russell, Susan P.; Vertrees, Jason Nucleic Acids Research, Vol. 38, Issue 18 https://doi.org/10.1093/nar/gkq364	journal	May 2010
Methanogenesis Lyu, Zhe; Shao, Nana; Akinyemi, Taiwo Current Biology, Vol. 28, Issue 13 https://doi.org/10.1016/j.cub.2018.05.021	journal	July 2018
Specificity in the biosynthesis of the universal tRNA nucleoside N⁶-threonylcarbamoyl adenosine (t⁶A)—TsaD is the gatekeeper Swinehart, William; Deutsch, Christopher; Sarachan, Kathryn L. RNA, Vol. 26, Issue 9 https://doi.org/10.1261/rna.075747.120	journal	May 2020
Structural basis for tRNA methylthiolation by the radical SAM enzyme MiaB Esakova, Olga A.; Grove, Tyler L.; Yennawar, Neela H. Nature, Vol. 597, Issue 7877 https://doi.org/10.1038/s41586-021-03904-6	journal	September 2021
Abundance of 4Feâ4S motifs in the genomes of methanogens and other prokaryotes Major, Tiffany A.; Burd, Henry; Whitman, William B. FEMS Microbiology Letters, Vol. 239, Issue 1 https://doi.org/10.1016/j.femsle.2004.08.027	journal	October 2004
Techniques for Cultivating Methanogens Wolfe, Ralph S. Methods in Methane Metabolism, Part A https://doi.org/10.1016/B978-0-12-385112-3.00001-9	book	March 2011
Identification of an Intermediate Methyl Carrier in the Radical S -Adenosylmethionine Methylthiotransferases RimO and MiaB Landgraf, Bradley J.; Arcinas, Arthur J.; Lee, Kyung-Hoon Journal of the American Chemical Society, Vol. 135, Issue 41 https://doi.org/10.1021/ja4048448	journal	October 2013
Identification of Eukaryotic and Prokaryotic Methylthiotransferase for Biosynthesis of 2-Methylthio-N6-threonylcarbamoyladenosine in tRNA Arragain, Simon; Handelman, Samuel K.; Forouhar, Farhad Journal of Biological Chemistry, Vol. 285, Issue 37 https://doi.org/10.1074/jbc.M110.106831	journal	September 2010
Quantitative Analysis of Coenzyme F430 in Environmental Samples: A New Diagnostic Tool for Methanogenesis and Anaerobic Methane Oxidation Kaneko, Masanori; Takano, Yoshinori; Chikaraishi, Yoshito Analytical Chemistry, Vol. 86, Issue 7 https://doi.org/10.1021/ac500305j	journal	March 2014
Genetic Methods for Methanosarcina Species Buan, Nicole; Kulkarni, Gargi; Metcalf, William Methods in Methane Metabolism, Part A https://doi.org/10.1016/B978-0-12-385112-3.00002-0	book	March 2011
Landscape of Post-Transcriptional tRNA Modifications in Streptomyces albidoflavus J1074 as Portrayed by Mass Spectrometry and Genomic Data Mining Koshla, Oksana; Vogt, Lea-Marie; Rydkin, Oleksandr Journal of Bacteriology, Vol. 205, Issue 1 https://doi.org/10.1128/jb.00294-22	journal	January 2023
Reverse Methanogenesis and Respiration in Methanotrophic Archaea Timmers, Peer H. A.; Welte, Cornelia U.; Koehorst, Jasper J. Archaea, Vol. 2017 https://doi.org/10.1155/2017/1654237	journal	January 2017
Structure of a methyl-coenzyme M reductase from Black Sea mats that oxidize methane anaerobically Shima, Seigo; Krueger, Martin; Weinert, Tobias Nature, Vol. 481, Issue 7379 https://doi.org/10.1038/nature10663	journal	November 2011
Atlas of the Radical SAM Superfamily: Divergent Evolution of Function Using a “Plug and Play” Domain Holliday, Gemma L.; Akiva, Eyal; Meng, Elaine C. Methods in Enzymology https://doi.org/10.1016/bs.mie.2018.06.004	book	July 2018
Complete Genome Sequence of the Methanogenic Archaeon, Methanococcus jannaschii Bult, C. J.; White, O.; Olsen, G. J. Science, Vol. 273, Issue 5278 https://doi.org/10.1126/science.273.5278.1058	journal	August 1996
Post-Transcriptional Modifications of the Anticodon Loop Region: Alterations in Isoaccepting Species of tRNA's During Development in Bacillus subtilis Vold, Barbara S. Journal of Bacteriology, Vol. 135, Issue 1 https://doi.org/10.1128/jb.135.1.124-132.1978	journal	July 1978
Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods Sofia, H. J. Nucleic Acids Research, Vol. 29, Issue 5 https://doi.org/10.1093/nar/29.5.1097	journal	March 2001
The biosynthetic pathway of coenzyme F430 in methanogenic and methanotrophic archaea Zheng, Kaiyuan; Ngo, Phong D.; Owens, Victoria L. Science, Vol. 354, Issue 6310 https://doi.org/10.1126/science.aag2947	journal	October 2016
Genetic techniques for studies of methyl-coenzyme M reductase from Methanosarcina acetivorans C2A Nayak, Dipti D.; Metcalf, William W. Enzymes of Energy Technology https://doi.org/10.1016/bs.mie.2018.10.012	book	November 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
Cysteine Is Not the Sulfur Source for Iron-Sulfur Cluster and Methionine Biosynthesis in the Methanogenic Archaeon Methanococcus maripaludis Liu, Yuchen; Sieprawska-Lupa, Magdalena; Whitman, William B. Journal of Biological Chemistry, Vol. 285, Issue 42 https://doi.org/10.1074/jbc.M110.152447	journal	August 2010
A genetic system for Archaea of the genus Methanosarcina: Liposome-mediated transformation and construction of shuttle vectors Metcalf, W. W.; Zhang, J. K.; Apolinario, E. Proceedings of the National Academy of Sciences, Vol. 94, Issue 6 https://doi.org/10.1073/pnas.94.6.2626	journal	March 1997
The modified base isopentenyladenosine and its derivatives in tRNA Schweizer, Ulrich; Bohleber, Simon; Fradejas-Villar, Noelia RNA Biology, Vol. 14, Issue 9 https://doi.org/10.1080/15476286.2017.1294309	journal	March 2017
MiaB Protein Is a Bifunctional Radical-S-Adenosylmethionine Enzyme Involved in Thiolation and Methylation of tRNA Pierrel, Fabien; Douki, Thierry; Fontecave, Marc Journal of Biological Chemistry, Vol. 279, Issue 46 https://doi.org/10.1074/jbc.M408562200	journal	November 2004
Cdk5rap1-Mediated 2-Methylthio Modification of Mitochondrial tRNAs Governs Protein Translation and Contributes to Myopathy in Mice and Humans Wei, Fan-Yan; Zhou, Bo; Suzuki, Takeo Cell Metabolism, Vol. 21, Issue 3 https://doi.org/10.1016/j.cmet.2015.01.019	journal	March 2015
tRNA Modification Profiles and Codon-Decoding Strategies in Methanocaldococcus jannaschii Yu, Ningxi; Jora, Manasses; Solivio, Beulah Journal of Bacteriology, Vol. 201, Issue 9 https://doi.org/10.1128/JB.00690-18	journal	February 2019
A Vastly Increased Chemical Variety of RNA Modifications Containing a Thioacetal Structure Dal Magro, Christina; Keller, Patrick; Kotter, Annika Angewandte Chemie International Edition, Vol. 57, Issue 26 https://doi.org/10.1002/anie.201713188	journal	April 2018
Lysine 2,3-Aminomutase and a Newly Discovered Glutamate 2,3-Aminomutase Produce β-Amino Acids Involved in Salt Tolerance in Methanogenic Archaea Tunçkanat, Taylan; Gendron, Aleksei; Sadler, Zoie Biochemistry, Vol. 61, Issue 11 https://doi.org/10.1021/acs.biochem.2c00014	journal	May 2022
Radical S -Adenosylmethionine Enzymes Broderick, Joan B.; Duffus, Benjamin R.; Duschene, Kaitlin S. Chemical Reviews, Vol. 114, Issue 8 https://doi.org/10.1021/cr4004709	journal	January 2014
Pathways of Iron and Sulfur Acquisition, Cofactor Assembly, Destination, and Storage in Diverse Archaeal Methanogens and Alkanotrophs Johnson, Christina; England, Alexis; Munro-Ehrlich, Mason Journal of Bacteriology, Vol. 203, Issue 17 https://doi.org/10.1128/JB.00117-21	journal	August 2021
Biosynthesis of coenzyme F430 in methanogenic bacteria. Identification of 15,173-seco-F430-173-acid as an intermediate Pfaltz, Andreas; Kobelt, Andre; Huster, Rudolf European Journal of Biochemistry, Vol. 170, Issue 1-2 https://doi.org/10.1111/j.1432-1033.1987.tb13722.x	journal	December 1987
Structure of an F430 Variant from Archaea Associated with Anaerobic Oxidation of Methane Mayr, Stefan; Latkoczy, Christopher; Krüger, Martin Journal of the American Chemical Society, Vol. 130, Issue 32 https://doi.org/10.1021/ja802929z	journal	August 2008
Archaea Are Interactive Components of Complex Microbiomes Moissl-Eichinger, Christine; Pausan, Manuela; Taffner, Julian Trends in Microbiology, Vol. 26, Issue 1 https://doi.org/10.1016/j.tim.2017.07.004	journal	January 2018
TRAM, a predicted RNA-binding domain, common to tRNA uracil methylation and adenine thiolation enzymes Anantharaman, Vivek; Koonin, Eugene V.; Aravind, L. FEMS Microbiology Letters, Vol. 197, Issue 2 https://doi.org/10.1111/j.1574-6968.2001.tb10606.x	journal	April 2001
Conservation and Diversification of tRNA t6A-Modifying Enzymes across the Three Domains of Life Su, Chenchen; Jin, Mengqi; Zhang, Wenhua International Journal of Molecular Sciences, Vol. 23, Issue 21 https://doi.org/10.3390/ijms232113600	journal	November 2022
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 Thauer, Rudolf K. Biochemistry, Vol. 58, Issue 52 https://doi.org/10.1021/acs.biochem.9b00164	journal	April 2019
Markerless Mutagenesis in Methanococcus maripaludis Demonstrates Roles for Alanine Dehydrogenase, Alanine Racemase, and Alanine Permease Moore, B. C.; Leigh, J. A. Journal of Bacteriology, Vol. 187, Issue 3 https://doi.org/10.1128/JB.187.3.972-979.2005	journal	January 2005
Lysine tRNAs fromBacillus subtilis168: structural analysis Vold, Barbara S.; Keith, Duane E.; Buck, Martine Nucleic Acids Research, Vol. 10, Issue 10 https://doi.org/10.1093/nar/10.10.3125	journal	January 1982
A Unique RNA Fold in the RumA-RNA-Cofactor Ternary Complex Contributes to Substrate Selectivity and Enzymatic Function Lee, Tom T.; Agarwalla, Sanjay; Stroud, Robert M. Cell, Vol. 120, Issue 5 https://doi.org/10.1016/j.cell.2004.12.037	journal	March 2005
Two Fe-S clusters catalyze sulfur insertion by radical-SAM methylthiotransferases Forouhar, Farhad; Arragain, Simon; Atta, Mohamed Nature Chemical Biology, Vol. 9, Issue 5 https://doi.org/10.1038/nchembio.1229	journal	March 2013
Gene expression and ultrastructure of meso- and thermophilic methanotrophic consortia: Interspecies interaction within AOM consortia Krukenberg, Viola; Riedel, Dietmar; Gruber-Vodicka, Harald R. Environmental Microbiology, Vol. 20, Issue 5 https://doi.org/10.1111/1462-2920.14077	journal	April 2018
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Bradford, Marion M. Analytical Biochemistry, Vol. 72, Issue 1-2 https://doi.org/10.1016/0003-2697(76)90527-3	journal	May 1976
Profiling of RNA modifications by multiplexed stable isotope labelling Kellner, Stefanie; Neumann, Jennifer; Rosenkranz, David Chemical Communications, Vol. 50, Issue 26 https://doi.org/10.1039/c3cc49114e	journal	January 2014
Metagenome and mRNA expression analyses of anaerobic methanotrophic archaea of the ANME-1 group Meyerdierks, Anke; Kube, Michael; Kostadinov, Ivaylo Environmental Microbiology, Vol. 12, Issue 2 https://doi.org/10.1111/j.1462-2920.2009.02083.x	journal	February 2010
First Step in Catalysis of the Radical S -Adenosylmethionine Methylthiotransferase MiaB Yields an Intermediate with a [3Fe-4S] ⁰ -Like Auxiliary Cluster Zhang, Bo; Arcinas, Arthur J.; Radle, Matthew I. Journal of the American Chemical Society, Vol. 142, Issue 4 https://doi.org/10.1021/jacs.9b11093	journal	January 2020
Transfer RNA modifications: nature's combinatorial chemistry playground: Transfer RNA modifications Jackman, Jane E.; Alfonzo, Juan D. Wiley Interdisciplinary Reviews: RNA, Vol. 4, Issue 1 https://doi.org/10.1002/wrna.1144	journal	November 2012
The growing tree of Archaea: new perspectives on their diversity, evolution and ecology Adam, Panagiotis S.; Borrel, Guillaume; Brochier-Armanet, Céline The ISME Journal, Vol. 11, Issue 11 https://doi.org/10.1038/ismej.2017.122	journal	August 2017
RadicalSAM.org: A Resource to Interpret Sequence-Function Space and Discover New Radical SAM Enzyme Chemistry Oberg, Nils; Precord, Timothy W.; Mitchell, Douglas A. ACS Bio & Med Chem Au, Vol. 2, Issue 1 https://doi.org/10.1021/acsbiomedchemau.1c00048	journal	December 2021
RimO, a MiaB-like enzyme, methylthiolates the universally conserved Asp88 residue of ribosomal protein S12 in Escherichia coli Anton, B. P.; Saleh, L.; Benner, J. S. Proceedings of the National Academy of Sciences, Vol. 105, Issue 6 https://doi.org/10.1073/pnas.0708608105	journal	February 2008
Genetic Systems for Hydrogenotrophic Methanogens Sarmiento, Felipe B.; Leigh, John A.; Whitman, William B. Methods in Methane Metabolism, Part A https://doi.org/10.1016/B978-0-12-385112-3.00003-2	book	March 2011
Radical S -Adenosylmethionine Enzymes in Human Health and Disease Landgraf, Bradley J.; McCarthy, Erin L.; Booker, Squire J. Annual Review of Biochemistry, Vol. 85, Issue 1 https://doi.org/10.1146/annurev-biochem-060713-035504	journal	June 2016
Post-transcriptional modification in archaeal tRNAs: identities and phylogenetic relations of nucleotides from mesophilic and hyperthermophilic Methanococcales McCloskey, J. A. Nucleic Acids Research, Vol. 29, Issue 22 https://doi.org/10.1093/nar/29.22.4699	journal	November 2001
Discovery of Multiple Modified F ₄₃₀ Coenzymes in Methanogens and Anaerobic Methanotrophic Archaea Suggests Possible New Roles for F ₄₃₀ in Nature Allen, Kylie D.; Wegener, Gunter; White, Robert H. Applied and Environmental Microbiology, Vol. 80, Issue 20 https://doi.org/10.1128/AEM.02202-14	journal	August 2014
Structure determination of two new amino acid-containing derivatives of adenosine from tRNA of thermophilic bacteria and archaea Reddy, Dasari M.; Crain, Pamela F.; Edmonds, Charles G. Nucleic Acids Research, Vol. 20, Issue 21 https://doi.org/10.1093/nar/20.21.5607	journal	January 1992
Influence of Temperature on tRNA Modification in Archaea: Methanococcoides burtonii (Optimum Growth Temperature [ T _opt ], 23°C) and Stetteria hydrogenophila ( T _opt , 95°C) Noon, Kathleen R.; Guymon, Rebecca; Crain, Pamela F. Journal of Bacteriology, Vol. 185, Issue 18 https://doi.org/10.1128/JB.185.18.5483-5490.2003	journal	September 2003
Diverse Mechanisms of Sulfur Decoration in Bacterial tRNA and Their Cellular Functions Zheng, Chenkang; Black, Katherine A.; Dos Santos, Patricia C. Biomolecules, Vol. 7, Issue 4 https://doi.org/10.3390/biom7010033	journal	March 2017
Biosynthesis of Sulfur-Containing tRNA Modifications: A Comparison of Bacterial, Archaeal, and Eukaryotic Pathways Čavužić, Mirela; Liu, Yuchen Biomolecules, Vol. 7, Issue 4 https://doi.org/10.3390/biom7010027	journal	March 2017
Construction and Analysis of Two Genome-Scale Deletion Libraries for Bacillus subtilis Koo, Byoung-Mo; Kritikos, George; Farelli, Jeremiah D. Cell Systems, Vol. 4, Issue 3 https://doi.org/10.1016/j.cels.2016.12.013	journal	March 2017
Analysis of Isoaccepting Transfer Ribonucleic Acid Species of Bacillus subtilis: Changes in Chromatography of Transfer Ribonucleic Acids Associated with Stage of Development Vold, Barbara S. Journal of Bacteriology, Vol. 114, Issue 1 https://doi.org/10.1128/jb.114.1.178-182.1973	journal	January 1973
Overview of Diverse Methyl/Alkyl-Coenzyme M Reductases and Considerations for Their Potential Heterologous Expression Gendron, Aleksei; Allen, Kylie D. Frontiers in Microbiology, Vol. 13 https://doi.org/10.3389/fmicb.2022.867342	journal	April 2022
Iron-sulphur clusters and the problem with oxygen Imlay, James A. Molecular Microbiology, Vol. 59, Issue 4 https://doi.org/10.1111/j.1365-2958.2006.05028.x	journal	February 2006
Zur Kenntnis des Faktors F430 aus methanogenen Bakterien: Struktur des porphinoiden Ligandsystems Pfaltz, Andreas; Jaun, Bernhard; Fassler, Alexander Helvetica Chimica Acta, Vol. 65, Issue 3 https://doi.org/10.1002/hlca.19820650320	journal	May 1982
Cas9-mediated genome editing in the methanogenic archaeon Methanosarcina acetivorans Nayak, Dipti D.; Metcalf, William W. Proceedings of the National Academy of Sciences, Vol. 114, Issue 11 https://doi.org/10.1073/pnas.1618596114	journal	March 2017
Methanethiol as a catabolite of methionine provides methylthio- group for chemical formation of 19-S-methylgeldanamycin and 17,19-dimethylthioherbimycin A Li, Shufen; Cui, Jing; Lu, Xinhua The Journal of Antibiotics, Vol. 66, Issue 8 https://doi.org/10.1038/ja.2013.31	journal	April 2013
New methods for tightly regulated gene expression and highly efficient chromosomal integration of cloned genes for Methanosarcina species Guss, Adam M.; Rother, Michael; Zhang, Jun Kai Archaea, Vol. 2, Issue 3 https://doi.org/10.1155/2008/534081	journal	January 2008
Shuttle Vector System for Methanococcus maripaludis with Improved Transformation Efficiency Walters, Alison D.; Smith, Sarah E.; Chong, James P. J. Applied and Environmental Microbiology, Vol. 77, Issue 7 https://doi.org/10.1128/AEM.02919-10	journal	February 2011