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Title: Thioredoxin-linked redox control of metabolism in Methanocaldococcus jannaschii, an evolutionarily deeply-rooted hyperthermophilic methanogenic archaeon

Author
item SUSANTI, DWI - Virginia Bioinformatics Institute
item WONG, JOSHUA - University Of California
item Vensel, William
item LOGANATHAN, USHA - Virginia Bioinformatics Institute
item DESANTIS, REBECCA - Christian Albrechts University
item SCHMITZ, RUTH - Christian Albrechts University
item BALAERA, MONICA - Consejo Superior De Investigaciones Cientificas (CSIC)
item BUCHANAN, BOB - University Of California
item MUKHOPADHYAY, BISWARUP - Virginia Bioinformatics Institute

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/7/2014
Publication Date: 2/18/2014
Publication URL: http://dx.doi.org/10.1073/pnas.1324240111
Citation: Susanti, D., Wong, J.H., Vensel, W.H., Loganathan, U., Desantis, R., Schmitz, R., Balaera, M., Buchanan, B.B., Mukhopadhyay, B. 2014. Thioredoxin-linked redox control of metabolism in Methanocaldococcus jannaschii, an evolutionarily deeply-rooted hyperthermophilic methanogenic archaeon. Proceedings of the National Academy of Sciences. 111(7):2608-2613. DOI:10.1073/pnas.1324240111.

Interpretive Summary: This study extends thioredoxin (Trx)-based oxidative redox regulation to the archaea, the third domain of life. Our study suggests that Trx is nearly ubiquitous in anaerobic methanogens, enabling them to recover from oxidative stress and synchronize cellular processes, including methane biogenesis, with the availability of reductants. As methane is a valuable fuel, an end product of anaerobic biodegradation and a potent greenhouse gas, Trx may now be considered a critical participant in the global carbon cycle, climate change, and bioenergy production. Because methanogenesis developed before the oxygenation of the earth, our work raises the possibility that Trx functioned in a complex redox regulatory network in anaerobic prokaryotes at least 2.5 billion years ago.

Technical Abstract: Thioredoxin (Trx), a small redox protein, controls multiple processes in eukaryotes and bacteria by changing the thiol redox status of selected proteins. We have investigated this aspect in methanarchaea. These ancient methanogens produce methane almost exclusively from H2 plus CO2 carried approximately two Trx homologs, whereas nutritionally versatile members possessed four to eight. Methanocaldococcus jannaschii—a deeply rooted hyperthermophilic methanogen carried two Trx homologs, canonical Trx1 that reduced insulin and accepted electrons from Escherichia coli thioredoxin reductase and atypical Trx2. Proteomic analyses with air-oxidized extracts treated with reduced Trx1 revealed 152 potential targets representing a range of processes—including methanogenesis, biosynthesis, transcription, translation, and oxidative response. In enzyme assays, Trx1 activated two selected targets following partial deactivation by O2, validating proteomics observations: methylene tetrahydromethanopterin dehydrogenase, a methanogenesis enzyme, and sulfite reductase, a detoxification enzyme. The results suggest that Trx assists methanogens in combating oxidative stress and synchronizing metabolic activities with availability of reductant, making it a critical factor in the global carbon cycle and methane emission.