Skip to main content
SpringerLink
Log in

Sulfur Assimilation and Trafficking in Methanogens

  • Chapter
  • First Online:
Molecular Mechanisms of Microbial Evolution

Part of the book series: Grand Challenges in Biology and Biotechnology ((GCBB))

Abstract

Methanogens are ancient obligate anaerobes, originating in an early Earth period before oxygen accumulated in the atmosphere and oceans. Unlike aerobic cells, all methanogens that persist in highly sulfidic, anaerobic niches are able to grow with sulfide as the sole sulfur source. These organisms have retained a unique apparatus for the assimilation and distribution of sulfur from the ambient environment. Recent work has revealed the presence of a unique set of at least six highly conserved genes likely responsible for sulfide uptake and synthesis of persulfide groups, cysteine, homocysteine, coenzyme M, coenzyme B, and cysteinyl-tRNACys. Phylogenetic studies show that these ancient sulfur assimilatory proteins share an evolutionary history with methanogenesis enzymes, suggesting that they played a key role in supporting the development of this metabolism. Little is yet known about most methanogen pathways that mobilize sulfur to form thiolated tRNA, iron-sulfur clusters, molybdopterin, and other important cofactors. However, for at least some of these pathways, it appears that the sulfur can be assimilated directly as sulfide, which is present at high intracellular levels without causing toxic effects. The many unique aspects of sulfur assimilation and trafficking in contemporary methanogens appear to be relics of ancient metabolic processes that were prevalent on the early anaerobic Earth.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aird BA, Heinrikson RL, Westley J (1987) Isolation and characterization of a prokaryotic sulfurtransferase. J Biol Chem 262:17327–17335

    CAS  PubMed  Google Scholar 

  • Allen KD, White RH (2016) Occurrence and biosynthesis of 3-mercaptopropionic acid in Methanocaldococcus jannaschii. FEMS Microbiol Lett 363

    Article  PubMed  CAS  Google Scholar 

  • Allen KD, Wegener G, White RH (2014) Discovery of multiple modified F(430) coenzymes in methanogens and anaerobic methanotrophic archaea suggests possible new roles for F(430) in nature. Appl Environ Microbiol 80:6403–6412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allen KD, Miller DV, Rauch BJ, Perona JJ, White RH (2015) Homocysteine is biosynthesized from aspartate semialdehyde and hydrogen sulfide in methanogenic archaea. Biochemistry 54:3129–3132

    Article  CAS  PubMed  Google Scholar 

  • Atta M, Arragain S, Fontecave M, Mulliez E, Hunt JF, Luff JD, Forouhar F (2012) The methylthiolation reaction mediated by the radical-SAM enzymes. Biochim Biophys Acta 1824:1223–1230

    Article  CAS  PubMed  Google Scholar 

  • Begley TP, Ealick SE, McLafferty FW (2012) Thiamin biosynthesis: still yielding fascinating biological chemistry. Biochem Soc Trans 40:555–560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE (2000) The protein data bank. Nucleic Acids Res 28:235–242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Black KA, Dos Santos PC (2015) Shared-intermediates in the biosynthesis of thio-cofactors: mechanism and functions of cysteine desulfurases and sulfur acceptors. Biochim Biophys Acta 1853:1470–1480

    Article  CAS  PubMed  Google Scholar 

  • Blank CE (2009a) Phylogenomic dating–a method of constraining the age of microbial taxa that lack a conventional fossil record. Astrobiology 9:173–191

    Article  CAS  PubMed  Google Scholar 

  • Blank CE (2009b) Phylogenomic dating–the relative antiquity of archaeal metabolic and physiological traits. Astrobiology 9:193–219

    Article  CAS  PubMed  Google Scholar 

  • Blank CE, Kessler PS, Leigh JA (1995) Genetics in methanogens: transposon insertion mutagenesis of a Methanococcus maripaludis nifH gene. J Bacteriol 177:5773–5777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borup B, Ferry JG (2000) Cysteine biosynthesis in the Archaea: Methanosarcina thermophila utilizes O-acetylserine sulfhydrylase. FEMS Microbiol Lett 189:205–210

    Article  CAS  PubMed  Google Scholar 

  • Borziak K, Posner MG, Upadhyay A, Danson MJ, Bagby S, Dorus S (2014) Comparative genomic analysis reveals 2-oxoacid dehydrogenase complex lipoylation correlation with aerobiosis in archaea. PLoS One 9:e87063

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bouvier D, Labessan N, Clemancey M, Latour JM, Ravanat JL, Fontecave M, Atta M (2014) TtcA a new tRNA-thioltransferase with an Fe-S cluster. Nucleic Acids Res 42:7960–7970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boyd JM, Endrizzi JA, Hamilton TL, Christopherson MR, Mulder DW, Downs DM, Peters JW (2011) FAD binding by ApbE protein from Salmonella enterica: a new class of FAD-binding proteins. J Bacteriol 193:887–895

    Article  CAS  PubMed  Google Scholar 

  • Bult CJ, White O, Olsen GJ, Zhou L, Fleischmann RD, Sutton GG, Blake JA, FitzGerald LM, Clayton RA, Gocayne JD, Kerlavage AR, Dougherty BA, Tomb JF, Adams MD, Reich CI, Overbeek R, Kirkness EF, Weinstock KG, Merrick JM, Glodek A, Scott JL, Geoghagen NS, Venter JC (1996) Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 273:1058–1073

    Article  CAS  PubMed  Google Scholar 

  • Canfield DE, Habicht KS, Thamdrup B (2000) The Archean sulfur cycle and the early history of atmospheric oxygen. Science 288:658–661

    Article  CAS  PubMed  Google Scholar 

  • Carlson BA, Xu XM, Kryukov GV, Rao M, Berry MJ, Gladyshev VN, Hatfield DL (2004) Identification and characterization of phosphoseryl-tRNA[Ser]Sec kinase. Proc Natl Acad Sci U S A 101:12848–12853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cipollone R, Ascenzi P, Visca P (2007) Common themes and variations in the rhodanese superfamily. IUBMB Life 59:51–59

    Article  CAS  PubMed  Google Scholar 

  • Costa KC, Leigh JA (2014) Metabolic versatility in methanogens. Curr Opin Biotechnol 29:70–75

    Article  CAS  PubMed  Google Scholar 

  • Cronan JE (2016) Assembly of lipoic acid on its cognate enzymes: an extraordinary and essential biosynthetic pathway. Microbiol Mol Biol Rev 80:429–450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daniels L, Belay N, Rajagopal BS (1986) Assimilatory reduction of sulfate and sulfite by methanogenic bacteria. Appl Environ Microbiol 51:703–709

    CAS  PubMed  PubMed Central  Google Scholar 

  • Deka RK, Brautigam CA, Liu WZ, Tomchick DR, Norgard MV (2013) The TP0796 lipoprotein of Treponema pallidum is a bimetal-dependent FAD pyrophosphatase with a potential role in flavin homeostasis. J Biol Chem 288:11106–11121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dridi B, Raoult D, Drancourt M (2011) Archaea as emerging organisms in complex human microbiomes. Anaerobe 17:56–63

    Article  PubMed  Google Scholar 

  • Duin EC, Madadi-Kahkesh S, Hedderich R, Clay MD, Johnson MK (2002) Heterodisulfide reductase from Methanothermobacter marburgensis contains an active-site [4Fe-4S] cluster that is directly involved in mediating heterodisulfide reduction. FEBS Lett 512:263–268

    Article  CAS  PubMed  Google Scholar 

  • Ermler U, Grabarse W, Shima S, Goubeaud M, Thauer RK (1997) Crystal structure of methyl-coenzyme M reductase: the key enzyme of biological methane formation. Science 278:1457–1462

    Article  CAS  PubMed  Google Scholar 

  • Eser BE, Zhang X, Chanani PK, Begley TP, Ealick SE (2016) From suicide enzyme to catalyst: the iron-dependent sulfide transfer in Methanococcus jannaschii thiamin thiazole biosynthesis. J Am Chem Soc 138:3639–3642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evans PN, Parks DH, Chadwick GL, Robbins SJ, Orphan VJ, Golding SD, Tyson GW (2015) Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics. Science 350:434–438

    Article  CAS  PubMed  Google Scholar 

  • Forchhammer K, Bock A (1991) Selenocysteine synthase from Escherichia coli. Analysis of the reaction sequence. J Biol Chem 266:6324–6328

    CAS  PubMed  Google Scholar 

  • Fraser WT, Blei E, Fry SC, Newman MF, Reay DS, Smith KA, McLeod AR (2015) Emission of methane, carbon monoxide, carbon dioxide and short-chain hydrocarbons from vegetation foliage under ultraviolet irradiation. Plant Cell Environ 38:980–989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fukunaga R, Yokoyama S (2007a) Structural insights into the first step of RNA-dependent cysteine biosynthesis in archaea. Nat Struct Mol Biol 14:272–279

    Article  CAS  PubMed  Google Scholar 

  • Fukunaga R, Yokoyama S (2007b) Structural insights into the second step of RNA-dependent cysteine biosynthesis in archaea: crystal structure of Sep-tRNA:Cys-tRNA synthase from Archaeoglobus fulgidus. J Mol Biol 370:128–141

    Article  CAS  PubMed  Google Scholar 

  • Galagan JE, Nusbaum C, Roy A, Endrizzi MG, Macdonald P, FitzHugh W, Calvo S, Engels R, Smirnov S, Atnoor D, Brown A, Allen N, Naylor J, Stange-Thomann N, DeArellano K, Johnson R, Linton L, McEwan P, McKernan K, Talamas J, Tirrell A, Ye W, Zimmer A, Barber RD, Cann I, Graham DE, Grahame DA, Guss AM, Hedderich R, Ingram-Smith C, Kuettner HC, Krzycki JA, Leigh JA, Li W, Liu J, Mukhopadhyay B, Reeve JN, Smith K, Springer TA, Umayam LA, White O, White RH, Conway de Macario E, Ferry JG, Jarrell KF, Jing H, Macario AJ, Paulsen I, Pritchett M, Sowers KR, Swanson RV, Zinder SH, Lander E, Metcalf WW, Birren B (2002) The genome of M. acetivorans reveals extensive metabolic and physiological diversity. Genome Res 12:532–542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graham DE (2011) 2-oxoacid metabolism in methanogenic CoM and CoB biosynthesis. Methods Enzymol 494:301–326

    Article  CAS  PubMed  Google Scholar 

  • Graham DE, White RH (2002) Elucidation of methanogenic coenzyme biosyntheses: from spectroscopy to genomics. Nat Prod Rep 19:133–147

    Article  CAS  PubMed  Google Scholar 

  • Graham DE, Xu H, White RH (2002) Identification of coenzyme M biosynthetic phosphosulfolactate synthase: a new family of sulfonate-biosynthesizing enzymes. J Biol Chem 277:13421–13429

    Article  CAS  PubMed  Google Scholar 

  • Graham DE, Taylor SM, Wolf RZ, Namboori SC (2009) Convergent evolution of coenzyme M biosynthesis in the Methanosarcinales: cysteate synthase evolved from an ancestral threonine synthase. Biochem J 424:467–478

    Article  CAS  PubMed  Google Scholar 

  • Hauenstein SI, Perona JJ (2008) Redundant synthesis of cysteinyl-tRNACys in Methanosarcina mazei. J Biol Chem 283:22007–22017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hauenstein SI, Hou YM, Perona JJ (2008) The homotetrameric phosphoseryl-tRNA synthetase from Methanosarcina mazei exhibits half-of-the-sites activity. J Biol Chem 283:21997–22006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Helgadottir S, Sinapah S, Soll D, Ling J (2012) Mutational analysis of Sep-tRNA:Cys-tRNA synthase reveals critical residues for tRNA-dependent cysteine formation. FEBS Lett 586:60–63

    Article  CAS  PubMed  Google Scholar 

  • Hepowit NL, de Vera IM, Cao S, Fu X, Wu Y, Uthandi S, Chavarria NE, Englert M, Su D, Sll D, Kojetin DJ, Maupin-Furlow JA (2016) Mechanistic insight into protein modification and sulfur mobilization activities of noncanonical E1 and associated ubiquitin-like proteins of Archaea. FEBS J 283:3567–3586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hidese R, Mihara H, Esaki N (2011) Bacterial cysteine desulfurases: versatile key players in biosynthetic pathways of sulfur-containing biofactors. Appl Microbiol Biotechnol 91:47–61

    Article  CAS  PubMed  Google Scholar 

  • Hohn MJ, Park HS, O’Donoghue P, Schnitzbauer M, Soll D (2006) Emergence of the universal genetic code imprinted in an RNA record. Proc Natl Acad Sci U S A 103:18095–18100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holland HD (2006) The oxygenation of the atmosphere and oceans. Philos Trans R Soc Lond Ser B Biol Sci 361:903–915

    Article  CAS  Google Scholar 

  • Hu Y, Ribbe MW (2011) Biosynthesis of nitrogenase FeMoco. Coord Chem Rev 255:1218–1224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hug LA, Baker BJ, Anantharaman K, Brown CT, Probst AJ, Castelle CJ, Butterfield CN, Hernsdorf AW, Amano Y, Ise K, Suzuki Y, Dudek N, Relman DA, Finstad KM, Amundson R, Thomas BC, Banfield JF (2016) A new view of the tree of life. Nat Microbiol 1:16048

    Article  CAS  PubMed  Google Scholar 

  • Ida T, Sawa T, Ihara H, Tsuchiya Y, Watanabe Y, Kumagai Y, Suematsu M, Motohashi H, Fujii S, Matsunaga T, Yamamoto M, Ono K, Devarie-Baez NO, Xian M, Fukuto JM, Akaike T (2014) Reactive cysteine persulfides and S-polythiolation regulate oxidative stress and redox signaling. Proc Natl Acad Sci U S A 111:7606–7611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Itoh Y, Sekine S, Matsumoto E, Akasaka R, Takemoto C, Shirouzu M, Yokoyama S (2009) Structure of selenophosphate synthetase essential for selenium incorporation into proteins and RNAs. J Mol Biol 385:1456–1469

    Article  CAS  PubMed  Google Scholar 

  • Jackson MR, Melideo SL, Jorns MS (2012) Human sulfide:quinone oxidoreductase catalyzes the first step in hydrogen sulfide metabolism and produces a sulfane sulfur metabolite. Biochemistry 51:6804–6815

    Article  CAS  PubMed  Google Scholar 

  • Jager G, Leipuviene R, Pollard MG, Qian Q, Bjork GR (2004) The conserved Cys-X1-X2-Cys motif present in the TtcA protein is required for the thiolation of cytidine in position 32 of tRNA from Salmonella enterica serovar Typhimurium. J Bacteriol 186:750–757

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Johnson EF, Mukhopadhyay B (2005) A new type of sulfite reductase, a novel coenzyme F420-dependent enzyme, from the methanarchaeon Methanocaldococcus jannaschii. J Biol Chem 280:38776–38786

    Article  CAS  PubMed  Google Scholar 

  • Johnson EF, Mukhopadhyay B (2008) Coenzyme F420-dependent sulfite reductase-enabled sulfite detoxification and use of sulfite as a sole sulfur source by Methanococcus maripaludis. Appl Environ Microbiol 74:3591–3595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kadaba NS, Kaiser JT, Johnson E, Lee A, Rees DC (2008) The high-affinity E. coli methionine ABC transporter: structure and allosteric regulation. Science 321:250–253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kambampati R, Lauhon CT (1999) IscS is a sulfurtransferase for the in vitro biosynthesis of 4-thiouridine in Escherichia coli tRNA. Biochemistry 38:16561–16568

    Article  CAS  PubMed  Google Scholar 

  • Kambampati R, Lauhon CT (2003) MnmA and IscS are required for in vitro 2-thiouridine biosynthesis in Escherichia coli. Biochemistry 42:1109–1117

    Article  CAS  PubMed  Google Scholar 

  • Kamtekar S, Hohn MJ, Park HS, Schnitzbauer M, Sauerwald A, Soll D, Steitz TA (2007) Toward understanding phosphoseryl-tRNACys formation: the crystal structure of Methanococcus maripaludis phosphoseryl-tRNA synthetase. Proc Natl Acad Sci U S A 104:2620–2625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaster AK, Goenrich M, Seedorf H, Liesegang H, Wollherr A, Gottschalk G, Thauer RK (2011) More than 200 genes required for methane formation from H(2) and CO(2) and energy conservation are present in Methanothermobacter marburgensis and Methanothermobacter thermautotrophicus. Archaea 2011:973848

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kessler D (2006) Enzymatic activation of sulfur for incorporation into biomolecules in prokaryotes. FEMS Microbiol Rev 30:825–840

    Article  CAS  PubMed  Google Scholar 

  • Kim JH, Bothe JR, Alderson TR, Markley JL (2015) Tangled web of interactions among proteins involved in iron-sulfur cluster assembly as unraveled by NMR, SAXS, chemical crosslinking, and functional studies. Biochim Biophys Acta 1853:1416–1428

    Article  CAS  PubMed  Google Scholar 

  • Kimura S, Suzuki T (2015) Iron-sulfur proteins responsible for RNA modifications. Biochim Biophys Acta 1853:1272–1283

    Article  CAS  PubMed  Google Scholar 

  • Klenk HP, Clayton RA, Tomb JF, White O, Nelson KE, Ketchum KA, Dodson RJ, Gwinn M, Hickey EK, Peterson JD, Richardson DL, Kerlavage AR, Graham DE, Kyrpides NC, Fleischmann RD, Quackenbush J, Lee NH, Sutton GG, Gill S, Kirkness EF, Dougherty BA, McKenney K, Adams MD, Loftus B, Peterson S, Reich CI, McNeil LK, Badger JH, Glodek A, Zhou L, Overbeek R, Gocayne JD, Weidman JF, McDonald L, Utterback T, Cotton MD, Spriggs T, Artiach P, Kaine BP, Sykes SM, Sadow PW, D’Andrea KP, Bowman C, Fujii C, Garland SA, Mason TM, Olsen GJ, Fraser CM, Smith HO, Woese CR, Venter JC (1997) The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature 390:364–370

    Article  CAS  PubMed  Google Scholar 

  • Klipcan L, Frenkel-Morgenstern M, Safro MG (2008) Presence of tRNA-dependent pathways correlates with high cysteine content in methanogenic Archaea. Trends Genet 24:59–63

    Article  CAS  PubMed  Google Scholar 

  • Komatsoulis GA, Abelson J (1993) Recognition of tRNA(Cys) by Escherichia coli cysteinyl-tRNA synthetase. Biochemistry 32:7435–7444

    Article  CAS  PubMed  Google Scholar 

  • Kotera M, Bayashi T, Hattori M, Tokimatsu T, Goto S, Mihara H, Kanehisa M (2010) Comprehensive genomic analysis of sulfur-relay pathway genes. Genome Inform 24:104–115

    PubMed  Google Scholar 

  • Leigh JA (2000) Nitrogen fixation in methanogens: the archaeal perspective. Curr Issues Mol Biol 2:125–131

    CAS  PubMed  Google Scholar 

  • Libiad M, Yadav PK, Vitvitsky V, Martinov M, Banerjee R (2014) Organization of the human mitochondrial hydrogen sulfide oxidation pathway. J Biol Chem 289:30901–30910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Whitman WB (2008) Metabolic, phylogenetic, and ecological diversity of the methanogenic archaea. Ann N Y Acad Sci 1125:171–189

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Sieprawska-Lupa M, Whitman WB, White RH (2010) Cysteine is not the sulfur source for iron-sulfur cluster and methionine biosynthesis in the methanogenic archaeon Methanococcus maripaludis. J Biol Chem 285:31923–31929

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Dos Santos PC, Zhu X, Orlando R, Dean DR, Soll D, Yuan J (2012a) Catalytic mechanism of Sep-tRNA:Cys-tRNA synthase: sulfur transfer is mediated by disulfide and persulfide. J Biol Chem 287:5426–5433

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Zhu X, Nakamura A, Orlando R, Soll D, Whitman WB (2012b) Biosynthesis of 4-thiouridine in tRNA in the methanogenic archaeon Methanococcus maripaludis. J Biol Chem 287(44):36683–36692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Beer LL, Whitman WB (2012c) Methanogens: a window into ancient sulfur metabolism. Trends Microbiol 20:251–258

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Beer LL, Whitman WB (2012d) Sulfur metabolism in archaea reveals novel processes. Environ Microbiol 14:2632–2644

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Long F, Wang L, Soll D, Whitman WB (2014a) The putative tRNA 2-thiouridine synthetase Ncs6 is an essential sulfur carrier in Methanococcus maripaludis. FEBS Lett 588:873–877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Nakamura A, Nakazawa Y, Asano N, Ford KA, Hohn MJ, Tanaka I, Yao M, Soll D (2014b) Ancient translation factor is essential for tRNA-dependent cysteine biosynthesis in methanogenic archaea. Proc Natl Acad Sci U S A 111(29):10520–10525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Vinyard DJ, Reesbeck ME, Suzuki T, Manakongtreecheep K, Holland PL, Brudvig GW, Soll D (2016) A [3Fe-4S] cluster is required for tRNA thiolation in archaea and eukaryotes. Proc Natl Acad Sci U S A 113(45):12703–12708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lombard J, Moreira D (2011) Early evolution of the biotin-dependent carboxylase family. BMC Evol Biol 11:232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lucas M, Encinar JA, Arribas EA, Oyenarte I, Garcia IG, Kortazar D, Fernandez JA, Mato JM, Martinez-Chantar ML, Martinez-Cruz LA (2010) Binding of S-methyl-5’-thioadenosine and S-adenosyl-L-methionine to protein MJ0100 triggers an open-to-closed conformational change in its CBS motif pair. J Mol Biol 396:800–820

    Article  CAS  PubMed  Google Scholar 

  • Lyons TW, Gill BC (2010) Ancient sulfur cycling and oxygenation of the early biosphere. Elements 6:93–99

    Article  CAS  Google Scholar 

  • Machnicka MA, Milanowska K, Osman Oglou O, Purta E, Kurkowska M, Olchowik A, Januszewski W, Kalinowski S, Dunin-Horkawicz S, Rother KM, Helm M, Bujnicki JM, Grosjean H (2013) MODOMICS: a database of RNA modification pathways--2013 update. Nucleic Acids Res 41:D262–D267

    Article  CAS  PubMed  Google Scholar 

  • Major TA, Burd H, Whitman WB (2004) Abundance of 4Fe-4S motifs in the genomes of methanogens and other prokaryotes. FEMS Microbiol Lett 239:117–123

    Article  CAS  PubMed  Google Scholar 

  • Marinoni EN, de Oliveira JS, Nicolet Y, Raulfs EC, Amara P, Dean DR, Fontecilla-Camps JC (2012) (IscS-IscU)2 complex structures provide insights into Fe2S2 biogenesis and transfer. Angew Chem Int Ed Eng 51:5439–5442

    Article  CAS  Google Scholar 

  • Maupin-Furlow JA (2013) Ubiquitin-like proteins and their roles in archaea. Trends Microbiol 21:31–38

    Article  CAS  PubMed  Google Scholar 

  • Maupin-Furlow JA (2014) Prokaryotic ubiquitin-like protein modification. Annu Rev Microbiol 68:155–175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mayr S, Latkoczy C, Kruger M, Gunther D, Shima S, Thauer RK, Widdel F, Jaun B (2008) Structure of an F430 variant from archaea associated with anaerobic oxidation of methane. J Am Chem Soc 130:10758–10767

    Article  CAS  PubMed  Google Scholar 

  • Mayumi D, Mochimaru H, Tamaki H, Yamamoto K, Yoshioka H, Suzuki Y, Kamagata Y, Sakata S (2016) Methane production from coal by a single methanogen. Science 354:222–225

    Article  CAS  PubMed  Google Scholar 

  • McCloskey JA, Graham DE, Zhou S, Crain PF, Ibba M, Konisky J, Soll D, Olsen GJ (2001) Post-transcriptional modification in archaeal tRNAs: identities and phylogenetic relations of nucleotides from mesophilic and hyperthermophilic Methanococcales. Nucleic Acids Res 29:4699–4706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mendel RR, Leimkuhler S (2015) The biosynthesis of the molybdenum cofactors. J Biol Inorg Chem 20:337–347

    Article  CAS  PubMed  Google Scholar 

  • Miller D, O’Brien K, Xu H, White RH (2014) Identification of a 5’-deoxyadenosine deaminase in Methanocaldococcus jannaschii and its possible role in recycling the radical S-adenosylmethionine enzyme reaction product 5’-deoxyadenosine. J Bacteriol 196:1064–1072

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Min B, Pelaschier JT, Graham DE, Tumbula-Hansen D, Soll D (2002) Transfer RNA-dependent amino acid biosynthesis: an essential route to asparagine formation. Proc Natl Acad Sci U S A 99:2678–2683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mino K, Ishikawa K (2003) A novel O-phospho-L-serine sulfhydrylation reaction catalyzed by O-acetylserine sulfhydrylase from Aeropyrum pernix K1. FEBS Lett 551:133–138

    Article  CAS  PubMed  Google Scholar 

  • Miranda HV, Nembhard N, Su D, Hepowit N, Krause DJ, Pritz JR, Phillips C, Soll D, Maupin-Furlow JA (2011) E1- and ubiquitin-like proteins provide a direct link between protein conjugation and sulfur transfer in archaea. Proc Natl Acad Sci U S A 108:4417–4422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mishanina TV, Libiad M, Banerjee R (2015) Biogenesis of reactive sulfur species for signaling by hydrogen sulfide oxidation pathways. Nat Chem Biol 11:457–464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mueller EG (2006) Trafficking in persulfides: delivering sulfur in biosynthetic pathways. Nat Chem Biol 2:185–194

    Article  CAS  PubMed  Google Scholar 

  • Mueller EG, Palenchar PM (1999) Using genomic information to investigate the function of ThiI, an enzyme shared between thiamin and 4-thiouridine biosynthesis. Protein Sci 8:2424–2427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mueller EG, Palenchar PM, Buck CJ (2001) The role of the cysteine residues of ThiI in the generation of 4-thiouridine in tRNA. J Biol Chem 276:33588–33595

    Article  CAS  PubMed  Google Scholar 

  • Neumann P, Lakomek K, Naumann PT, Erwin WM, Lauhon CT, Ficner R (2014) Crystal structure of a 4-thiouridine synthetase-RNA complex reveals specificity of tRNA U8 modification. Nucleic Acids Res 42:6673–6685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noma A, Sakaguchi Y, Suzuki T (2009) Mechanistic characterization of the sulfur-relay system for eukaryotic 2-thiouridine biogenesis at tRNA wobble positions. Nucleic Acids Res 37:1335–1352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Numata T, Fukai S, Ikeuchi Y, Suzuki T, Nureki O (2006a) Structural basis for sulfur relay to RNA mediated by heterohexameric TusBCD complex. Structure 14:357–366

    Article  CAS  PubMed  Google Scholar 

  • Numata T, Ikeuchi Y, Fukai S, Suzuki T, Nureki O (2006b) Snapshots of tRNA sulphuration via an adenylated intermediate. Nature 442:419–424

    Article  CAS  PubMed  Google Scholar 

  • O’Donoghue P, Sethi A, Woese CR, Luthey-Schulten ZA (2005) The evolutionary history of Cys-tRNACys formation. Proc Natl Acad Sci U S A 102:19003–19008

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pagnier A, Nicolet Y, Fontecilla-Camps JC (2015) IscS from Archaeoglobus fulgidus has no desulfurase activity but may provide a cysteine ligand for [Fe2S2] cluster assembly. Biochim Biophys Acta 1853:1457–1463

    Article  CAS  PubMed  Google Scholar 

  • Palioura S, Sherrer RL, Steitz TA, Soll D, Simonovic M (2009) The human SepSecS-tRNASec complex reveals the mechanism of selenocysteine formation. Science 325:321–325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park CM, Weerasinghe L, Day JJ, Fukuto JM, Xian M (2015) Persulfides: current knowledge and challenges in chemistry and chemical biology. Mol BioSyst 11:1775–1785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perona JJ, Hadd A (2012) Structural diversity and protein engineering of the aminoacyl-tRNA synthetases. Biochemistry 51:8705–8729

    Article  CAS  PubMed  Google Scholar 

  • Probst AJ, Moissl-Eichinger C (2015) “Altiarchaeales”: uncultivated archaea from the subsurface. Life (Basel) 5:1381–1395

    CAS  Google Scholar 

  • Ramabhadran TV, Jagger J (1976) Mechanism of growth delay induced in Escherichia coli by near ultraviolet radiation. Proc Natl Acad Sci U S A 73:59–63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rauch BJ, Perona JJ (2016) Efficient sulfide assimilation in Methanosarcina acetivorans is mediated by the MA1715 protein. J Bacteriol 198:1974–1983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rauch BJ, Gustafson A, Perona JJ (2014) Novel proteins for homocysteine biosynthesis in anaerobic microorganisms. Mol Microbiol 94:1330–1342

    Article  CAS  PubMed  Google Scholar 

  • Rauch BJ, Klimek J, David L, Perona JJ (2017) Persulfide formation mediates cysteine and homocysteine biosynthesis in Methanosarcina acetivorans. Biochemistry 56(8):1051–1061

    Article  CAS  PubMed  Google Scholar 

  • Reich HJ, Hondal RJ (2016) Why Nature Chose Selenium. ACS Chem Biol 11:821–841

    Article  CAS  PubMed  Google Scholar 

  • Roche B, Aussel L, Ezraty B, Mandin P, Py B, Barras F (2013) Iron/sulfur proteins biogenesis in prokaryotes: formation, regulation and diversity. Biochim Biophys Acta 1827:455–469

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Hernandez A, Spears JL, Gaston KW, Limbach PA, Gamper H, Hou YM, Kaiser R, Agris PF, Perona JJ (2013) Structural and mechanistic basis for enhanced translational efficiency by 2-thiouridine at the tRNA anticodon wobble position. J Mol Biol 425(20):3888–3906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sauerwald A, Zhu W, Major TA, Roy H, Palioura S, Jahn D, Whitman WB, Yates JR, Ibba M 3rd, Soll D (2005) RNA-dependent cysteine biosynthesis in archaea. Science 307:1969–1972

    Article  CAS  PubMed  Google Scholar 

  • Scheller S, Goenrich M, Boecher R, Thauer RK, Jaun B (2010) The key nickel enzyme of methanogenesis catalyses the anaerobic oxidation of methane. Nature 465:606–608

    Article  CAS  PubMed  Google Scholar 

  • Schwartz CJ, Djaman O, Imlay JA, Kiley PJ (2000) The cysteine desulfurase, IscS, has a major role in in vivo Fe-S cluster formation in Escherichia coli. Proc Natl Acad Sci U S A 97:9009–9014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sekowska A, Kung HF, Danchin A (2000) Sulfur metabolism in Escherichia coli and related bacteria: facts and fiction. J Mol Microbiol Biotechnol 2:145–177

    CAS  PubMed  Google Scholar 

  • Shigi N (2014) Biosynthesis and functions of sulfur modifications in tRNA. Front Genet 5:67

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sousa FL, Nelson-Sathi S, Martin WF (2016) One step beyond a ribosome: the ancient anaerobic core. Biochim Biophys Acta 1857:1027–1038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spry C, Kirk K, Saliba KJ (2008) Coenzyme a biosynthesis: an antimicrobial drug target. FEMS Microbiol Rev 32:56–106

    Article  CAS  PubMed  Google Scholar 

  • Su D, Ojo TT, Soll D, Hohn MJ (2012) Selenomodification of tRNA in archaea requires a bipartite rhodanese enzyme. FEBS Lett 586:717–721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Susanti D, Mukhopadhyay B (2012) An intertwined evolutionary history of methanogenic archaea and sulfate reduction. PLoS One 7:e45313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sylvers LA, Rogers KC, Shimizu M, Ohtsuka E, Soll D (1993) A 2-thiouridine derivative in tRNAGlu is a positive determinant for aminoacylation by Escherichia coli glutamyl-tRNA synthetase. Biochemistry 32:3836–3841

    Article  CAS  PubMed  Google Scholar 

  • Tchong SI, Xu H, White RH (2005) L-cysteine desulfidase: an [4Fe-4S] enzyme isolated from Methanocaldococcus jannaschii that catalyzes the breakdown of L-cysteine into pyruvate, ammonia, and sulfide. Biochemistry 44:1659–1670

    Article  CAS  PubMed  Google Scholar 

  • Thauer RK (1998) Biochemistry of methanogenesis: a tribute to Marjory Stephenson. 1998 Marjory Stephenson Prize Lecture. Microbiology 144(Pt 9):2377–2406

    Article  CAS  PubMed  Google Scholar 

  • Valentine DL (2007) Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nat Rev Microbiol 5:316–323

    Article  CAS  PubMed  Google Scholar 

  • Veerareddygari GR, Klusman TC, Mueller EG (2016) Characterization of the catalytic disulfide bond in E. coli 4-thiouridine synthetase to elucidate its functional quaternary structure. Protein Sci 25:1737–1743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walters EM, Garcia-Serres R, Naik SG, Bourquin F, Glauser DA, Schurmann P, Huynh BH, Johnson MK (2009) Role of histidine-86 in the catalytic mechanism of ferredoxin:thioredoxin reductase. Biochemistry 48:1016–1024

    Article  CAS  PubMed  Google Scholar 

  • Westley J (1973) Rhodanese. Adv Enzymol Relat Areas Mol Biol 39:327–368

    CAS  PubMed  Google Scholar 

  • White RH (2003) The biosynthesis of cysteine and homocysteine in Methanococcus jannaschii. Biochim Biophys Acta 1624:46–53

    Article  CAS  PubMed  Google Scholar 

  • Xu XM, Carlson BA, Mix H, Zhang Y, Saira K, Glass RS, Berry MJ, Gladyshev VN, Hatfield DL (2007) Biosynthesis of selenocysteine on its tRNA in eukaryotes. PLoS Biol 5:e4

    Article  PubMed  CAS  Google Scholar 

  • Yuan J, Palioura S, Salazar JC, Su D, O’Donoghue P, Hohn MJ, Cardoso AM, Whitman WB, Soll D (2006) RNA-dependent conversion of phosphoserine forms selenocysteine in eukaryotes and archaea. Proc Natl Acad Sci U S A 103:18923–18927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan J, Hohn MJ, Sherrer RL, Palioura S, Su D, Soll D (2010) A tRNA-dependent cysteine biosynthesis enzyme recognizes the selenocysteine-specific tRNA in Escherichia coli. FEBS Lett 584:2857–2861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang CM, Liu C, Slater S, Hou YM (2008) Aminoacylation of tRNA with phosphoserine for synthesis of cysteinyl-tRNA(Cys). Nat Struct Mol Biol 15:507–514

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Eser BE, Chanani PK, Begley TP, Ealick SE (2016) Structural basis for iron-mediated sulfur transfer in archael and yeast thiazole synthases. Biochemistry 55:1826–1838

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Chemistry, Portland State University, Portland, OR, USA

    John J. Perona & Camden M. Driggers

  2. Department of Biochemistry and Molecular Biology, Oregon Health and Science University, Portland, OR, USA

    John J. Perona

  3. Department of Microbiology and Immunology, University of California San Francisco, San Francisco, CA, USA

    Benjamin Julius Rauch

Authors
  1. John J. Perona
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Benjamin Julius Rauch
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Camden M. Driggers
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John J. Perona .

Editor information

Editors and Affiliations

  1. Federal University of Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil

    Pabulo H. Rampelotto

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Perona, J.J., Rauch, B.J., Driggers, C.M. (2018). Sulfur Assimilation and Trafficking in Methanogens. In: Rampelotto, P. (eds) Molecular Mechanisms of Microbial Evolution. Grand Challenges in Biology and Biotechnology. Springer, Cham. https://doi.org/10.1007/978-3-319-69078-0_14

Download citation

Publish with us

Policies and ethics

Search

Navigation