1932

Abstract

Archaea are major contributors to biogeochemical cycles, possess unique metabolic capabilities, and resist extreme stress. To regulate the expression of genes encoding these unique programs, archaeal cells use gene regulatory networks (GRNs) composed of transcription factor proteins and their target genes. Recent developments in genetics, genomics, and computational methods used with archaeal model organisms have enabled the mapping and prediction of global GRN structures. Experimental tests of these predictions have revealed the dynamical function of GRNs in response to environmental variation. Here, we review recent progress made in this area, from investigating the mechanisms of transcriptional regulation of individual genes to small-scale subnetworks and genome-wide global networks. At each level, archaeal GRNs consist of a hybrid of bacterial, eukaryotic, and uniquely archaeal mechanisms. We discuss this theme from the perspective of the role of individual transcription factors in genome-wide regulation, how these proteins interact to compile GRN topological structures, and how these topologies lead to emergent, high-level GRN functions. We conclude by discussing how systems biology approaches are a fruitful avenue for addressing remaining challenges, such as discovering gene function and the evolution of GRNs.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-genet-120116-023413
2017-11-27
2024-06-23
Loading full text...

Full text loading...

/deliver/fulltext/genet/51/1/annurev-genet-120116-023413.html?itemId=/content/journals/10.1146/annurev-genet-120116-023413&mimeType=html&fmt=ahah

Literature Cited

  1. Adebali O, Zhulin IB. 1.  2017. Aquerium: a web application for comparative exploration of domain-based protein occurrences on the taxonomically clustered genome tree. Proteins 85:72–77 [Google Scholar]
  2. Allers T, Barak S, Liddell S, Wardell K, Mevarech M. 2.  2010. Improved strains and plasmid vectors for conditional overexpression of His-tagged proteins in Haloferax volcanii. Appl. Environ. Microbiol. 76:1759–69 [Google Scholar]
  3. Alon U. 3.  2006. An Introduction to Systems Biology: Design Principles of Biological Circuits Boca Raton, FL: CRC Press, Taylor & Francis Group [Google Scholar]
  4. Ammar R, Torti D, Tsui K, Gebbia M, Durbic T. 4.  et al. 2012. Chromatin is an ancient innovation conserved between Archaea and Eukarya. eLife 1:e00078 [Google Scholar]
  5. Arrieta-Ortiz ML, Hafemeister C, Bate AR, Chu T, Greenfield A. 5.  et al. 2015. An experimentally supported model of the Bacillus subtilis global transcriptional regulatory network. Mol. Syst. Biol. 11:839 [Google Scholar]
  6. Babski J, Haas KA, Näther-Schindler D, Pfeiffer F, Förstner KU. 6.  et al. 2016. Genome-wide identification of transcriptional start sites in the haloarchaeon Haloferax volcanii based on differential RNA-Seq (dRNA-Seq). BMC Genom 17:629 [Google Scholar]
  7. Babski J, Maier LK, Heyer R, Jaschinski K, Prasse D. 7.  et al. 2014. Small regulatory RNAs in Archaea. RNA Biol 11:484–93 [Google Scholar]
  8. Baliga NS, Bjork SJ, Bonneau R, Pan M, Iloanusi C. 8.  et al. 2004. Systems level insights into the stress response to UV radiation in the halophilic archaeon Halobacterium NRC-1. Genome Res 14:1025–35 [Google Scholar]
  9. Baliga NS, DasSarma S. 9.  1999. Saturation mutagenesis of the TATA box and upstream activator sequence in the haloarchaeal bop gene promoter. J. Bacteriol. 181:2513–18 [Google Scholar]
  10. Baliga NS, Goo YA, Ng WV, Hood L, Daniels CJ, DasSarma S. 10.  2000. Is gene expression in Halobacterium NRC-1 regulated by multiple TBP and TFB transcription factors?. Mol. Microbiol. 36:1184–85 [Google Scholar]
  11. Baliga NS, Kennedy SP, Ng WV, Hood L, DasSarma S. 11.  2001. Genomic and genetic dissection of an archaeal regulon. PNAS 98:2521–25 [Google Scholar]
  12. Battesti A, Majdalani N, Gottesman S. 12.  2011. The RpoS-mediated general stress response in Escherichia coli. Annu. Rev. Microbiol. 65:189–213 [Google Scholar]
  13. Bauer M, Marschaus L, Reuff M, Besche V, Sartorius-Neef S, Pfeifer F. 13.  2008. Overlapping activator sequences determined for two oppositely oriented promoters in halophilic Archaea. Nucleic Acids Res 36:598–606 [Google Scholar]
  14. Bell SD. 14.  2005. Archaeal transcriptional regulation—variation on a bacterial theme?. Trends Microbiol 13:262–65 [Google Scholar]
  15. Bell SD, Cairns SS, Robson RL, Jackson SP. 15.  1999. Transcriptional regulation of an archaeal operon in vivo and in vitro. Mol. Cell 4:971–82 [Google Scholar]
  16. Bell SD, Jackson SP. 16.  2000. Mechanism of autoregulation by an archaeal transcriptional repressor. J. Biol. Chem. 275:31624–29 [Google Scholar]
  17. Bhardwaj N, Carson MB, Abyzov A, Yan KK, Lu H, Gerstein MB. 17.  2010. Analysis of combinatorial regulation: scaling of partnerships between regulators with the number of governed targets. PLOS Comput. Biol. 6:e1000755 [Google Scholar]
  18. Blombach F, Smollett KL, Grohmann D, Werner F. 18.  2016. Molecular mechanisms of transcription initiation—structure, function, and evolution of TFE/TFIIE-like factors and open complex formation. J. Mol. Biol. 428:2592–606 [Google Scholar]
  19. Bonneau R, Baliga NS, Deutsch EW, Shannon P, Hood L. 19.  2004. Comprehensive de novo structure prediction in a systems-biology context for the archaea Halobacterium sp. NRC-1. Genome Biol. 5:R52 [Google Scholar]
  20. Bonneau R, Facciotti MT, Reiss DJ, Schmid AK, Pan M. 20.  et al. 2007. A predictive model for transcriptional control of physiology in a free living cell. Cell 131:1354–65 [Google Scholar]
  21. Bonneau R, Reiss DJ, Shannon P, Facciotti M, Hood L. 21.  et al. 2006. The Inferelator: an algorithm for learning parsimonious regulatory networks from systems-biology data sets de novo. Genome Biol 7:R36 [Google Scholar]
  22. Bowers KJ, Wiegel J. 22.  2011. Temperature and pH optima of extremely halophilic archaea: a mini-review. Extremophiles 15:119–28 [Google Scholar]
  23. Brinkman AB, Bell SD, Lebbink RJ, de Vos WM, van der Oost J. 23.  2002. The Sulfolobus solfataricus Lrp-like protein LysM regulates lysine biosynthesis in response to lysine availability. J. Biol. Chem. 277:29537–49 [Google Scholar]
  24. Brooks AN, Reiss DJ, Allard A, Wu WJ, Salvanha DM. 24.  et al. 2014. A system-level model for the microbial regulatory genome. Mol. Syst. Biol. 10:740 [Google Scholar]
  25. Brooks AN, Turkarslan S, Beer KD, Lo FY, Baliga NS. 25.  2011. Adaptation of cells to new environments. Wiley Interdiscip. Rev. Syst. Biol. Med. 3:544–61 [Google Scholar]
  26. Bult CJ, White O, Olsen GJ, Zhou L, Fleischmann RD. 26.  et al. 1996. Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 273:1058–73 [Google Scholar]
  27. Buxton GV. 27.  1987. Radiation chemistry of the liquid state: (1) water and homogeneous aqueous solutions. Radiation Chemistry: Principles and Applications Farhataziz, MAJ Rodgers 321–50 New York: VCH Publ. [Google Scholar]
  28. Canganella F, Wiegel J. 28.  2014. Anaerobic thermophiles. Life 4:77–104 [Google Scholar]
  29. Charlesworth JC, Burns BP. 29.  2015. Untapped resources: biotechnological potential of peptides and secondary metabolites in archaea. Archaea 2015:282035 [Google Scholar]
  30. Charoensawan V, Wilson D, Teichmann SA. 30.  2010. Genomic repertoires of DNA-binding transcription factors across the tree of life. Nucleic Acids Res 38:7364–77 [Google Scholar]
  31. Chen L, Brugger K, Skovgaard M, Redder P, She Q. 31.  et al. 2005. The genome of Sulfolobus acidocaldarius, a model organism of the Crenarchaeota. J. Bacteriol. 187:4992–99 [Google Scholar]
  32. Cline MS, Smoot M, Cerami E, Kuchinsky A, Landys N. 32.  et al. 2007. Integration of biological networks and gene expression data using Cytoscape. Nature Protoc 2:2366–82 [Google Scholar]
  33. Cohen O, Doron S, Wurtzel O, Dar D, Edelheit S. 33.  et al. 2016. Comparative transcriptomics across the prokaryotic tree of life. Nucleic Acids Res 44:46–53 [Google Scholar]
  34. Coker JA, DasSarma S. 34.  2007. Genetic and transcriptomic analysis of transcription factor genes in the model halophilic Archaeon: coordinate action of TbpD and TfbA. BMC Genet 8:61 [Google Scholar]
  35. Costa KC, Leigh JA. 35.  2014. Metabolic versatility in methanogens. Curr. Opin. Biotechnol. 29:70–75 [Google Scholar]
  36. Darnell CL, Schmid AK. 36.  2015. Systems biology approaches to defining transcription regulatory networks in halophilic archaea. Methods 86:102–14 [Google Scholar]
  37. Darnell CL, Tonner PD, Gulli JG, Schmidler S, Schmid AK. 37.  2017. Systematic discovery of archaeal transcription factor functions in regulatory networks through quantitative phenotyping analysis. mSystems 2:e00032–17 [Google Scholar]
  38. De Smet R, Marchal K. 38.  2010. Advantages and limitations of current network inference methods. Nat. Rev. Microbiol. 8:717–29 [Google Scholar]
  39. Decker KB, Hinton DM. 39.  2013. Transcription regulation at the core: similarities among bacterial, archaeal, and eukaryotic RNA polymerases. Annu. Rev. Microbiol. 67:113–39 [Google Scholar]
  40. Deppenmeier U, Johann A, Hartsch T, Merkl R, Schmitz RA. 40.  et al. 2002. The genome of Methanosarcina mazei: evidence for lateral gene transfer between bacteria and archaea. J. Mol. Microbiol. Biotechnol. 4:453–61 [Google Scholar]
  41. Ding Y, Nash J, Berezuk A, Khursigara CM, Langelaan DN. 41.  et al. 2016. Identification of the first transcriptional activator of an archaellum operon in a euryarchaeon. Mol. Microbiol. 102:54–70 [Google Scholar]
  42. Domagalski JL, Eugster HP, Jones BF. 42.  1990. Trace metal geochemistry of Walker, Mono, and Great Salt Lakes. Fluid–Mineral Interactions: A Tribute to H. P. Eugster RJ Spencer, I-M Chou 315–53 Washington, DC: Geochem. Soc. [Google Scholar]
  43. Dufour YS, Donohue TJ. 43.  2012. Signal correlations in ecological niches can shape the organization and evolution of bacterial gene regulatory networks. Adv. Microb. Physiol. 61:1–36 [Google Scholar]
  44. Dufour YS, Imam S, Koo BM, Green HA, Donohue TJ. 44.  2012. Convergence of the transcriptional responses to heat shock and singlet oxygen stresses. PLOS Genet 8:e1002929 [Google Scholar]
  45. Ehlers C, Jäger D, Schmitz RA. 45.  2011. Establishing a markerless genetic exchange system for Methanosarcina mazei strain Gö1 for constructing chromosomal mutants of small RNA genes. Archaea 2011:439608 [Google Scholar]
  46. Esser D, Hoffmann L, Pham TK, Brasen C, Qiu W. 46.  et al. 2016. Protein phosphorylation and its role in archaeal signal transduction. FEMS Microbiol. Rev. 40:625–47 [Google Scholar]
  47. Facciotti MT, Reiss DJ, Pan M, Kaur A, Vuthoori M. 47.  et al. 2007. General transcription factor specified global gene regulation in archaea. PNAS 104:4630–35 [Google Scholar]
  48. Farkas JA, Picking JW, Santangelo TJ. 48.  2013. Genetic techniques for the Archaea. Annu. Rev. Genet. 47:539–61 [Google Scholar]
  49. Fiebig A, Herrou J, Willett J, Crosson S. 49.  2015. General stress signaling in the Alphaproteobacteria. Annu. Rev. Genet. 49:603–25 [Google Scholar]
  50. Finn RD, Mistry J, Schuster-Bockler B, Griffiths-Jones S, Hollich V. 50.  et al. 2006. Pfam: clans, web tools and services. Nucleic Acids Res 34:D247–51 [Google Scholar]
  51. Fiorentino G, Ronca R, Cannio R, Rossi M, Bartolucci S. 51.  2007. MarR-like transcriptional regulator involved in detoxification of aromatic compounds in Sulfolobus solfataricus. J. Bacteriol. 189:7351–60 [Google Scholar]
  52. Fu X, Liu R, Sanchez I, Silva-Sanchez C, Hepowit NL. 52.  et al. 2016. Ubiquitin-like proteasome system represents a eukaryotic-like pathway for targeted proteolysis in archaea. mBio 7:e00379–16 [Google Scholar]
  53. Fukui T, Atomi H, Kanai T, Matsumi R, Fujiwara S, Imanaka T. 53.  2005. Complete genome sequence of the hyperthermophilic archaeon Thermococcus kodakaraensis KOD1 and comparison with Pyrococcus genomes. Genome Res 15:352–63 [Google Scholar]
  54. Galagan JE, Nusbaum C, Roy A, Endrizzi MG, Macdonald P. 54.  et al. 2002. The genome of M. acetivorans reveals extensive metabolic and physiological diversity. Genome Res 12:532–42 [Google Scholar]
  55. Gama-Castro S, Salgado H, Santos-Zavaleta A, Ledezma-Tejeida D, Muñiz-Rascado L. 55.  et al. 2016. RegulonDB version 9.0: high-level integration of gene regulation, coexpression, motif clustering and beyond. Nucleic Acids Res 44:D133–43 [Google Scholar]
  56. Gehring AM, Walker JE, Santangelo TJ. 56.  2016. Transcription regulation in Archaea. J. Bacteriol. 198:1906–17 [Google Scholar]
  57. Gindner A, Hausner W, Thomm M. 57.  2014. The TrmB family: a versatile group of transcriptional regulators in Archaea. Extremophiles 18:925–36 [Google Scholar]
  58. Götz D, Paytubi S, Munro S, Lundgren M, Bernander R, White MF. 58.  2007. Responses of hyperthermophilic crenarchaea to UV irradiation. Genome Biol 8:R220 [Google Scholar]
  59. Greenfield A, Hafemeister C, Bonneau R. 59.  2013. Robust data-driven incorporation of prior knowledge into the inference of dynamic regulatory networks. Bioinformatics 29:1060–67 [Google Scholar]
  60. Grohmann D, Werner F. 60.  2011. Recent advances in the understanding of archaeal transcription. Curr. Opin. Microbiol. 14:328–34 [Google Scholar]
  61. Gruber TM, Gross CA. 61.  2003. Multiple σ subunits and the partitioning of bacterial transcription space. Annu. Rev. Microbiol. 57:441–66 [Google Scholar]
  62. Hain J, Reiter WD, Hudepohl U, Zillig W. 62.  1992. Elements of an archaeal promoter defined by mutational analysis. Nucleic Acids Res 20:5423–28 [Google Scholar]
  63. Harbison CT, Gordon DB, Lee TI, Rinaldi NJ, Macisaac KD. 63.  et al. 2004. Transcriptional regulatory code of a eukaryotic genome. Nature 431:99–104 [Google Scholar]
  64. Hartman AL, Norais C, Badger JH, Delmas S, Haldenby S. 64.  et al. 2010. The complete genome sequence of Haloferax volcanii DS2, a model archaeon. PLOS ONE 5:e9605 [Google Scholar]
  65. Hattori T, Shiba H, Ashiki K, Araki T, Nagashima YK. 65.  et al. 2016. Anaerobic growth of haloarchaeon Haloferax volcanii by denitrification is controlled by the transcription regulator NarO. J. Bacteriol. 198:1077–86 [Google Scholar]
  66. Hecker M, Pane-Farre J, Volker U. 66.  2007. SigB-dependent general stress response in Bacillus subtilis and related gram-positive bacteria. Annu. Rev. Microbiol. 61:215–36 [Google Scholar]
  67. Helmann JD. 67.  2016. Bacillus subtilis extracytoplasmic function (ECF) σ factors and defense of the cell envelope. Curr. Opin. Microbiol. 30:122–32 [Google Scholar]
  68. Hendrickson EL, Kaul R, Zhou Y, Bovee D, Chapman P. 68.  et al. 2004. Complete genome sequence of the genetically tractable hydrogenotrophic methanogen Methanococcus maripaludis. J. Bacteriol. 186:6956–69 [Google Scholar]
  69. Heyer R, Dorr M, Jellen-Ritter A, Spath B, Babski J. 69.  et al. 2012. High throughput sequencing reveals a plethora of small RNAs including tRNA derived fragments in Haloferax volcanii. RNA Biol 9:1011–18 [Google Scholar]
  70. Hubmacher D, Matzanke BF, Anemuller S. 70.  2003. Effects of iron limitation on the respiratory chain and the membrane cytochrome pattern of the Euryarchaeon Halobacterium salinarum. Biol. Chem. 384:1565–73 [Google Scholar]
  71. Humbard MA, Miranda HV, Lim JM, Krause DJ, Pritz JR. 71.  et al. 2010. Ubiquitin-like small archaeal modifier proteins (SAMPs) in Haloferax volcanii. Nature 463:54–60 [Google Scholar]
  72. Hwang S, Cordova B, Abdo M, Pfeiffer F, Maupin-Fantiurlow JA. 72.  2017. ThiN as a versatile domain of transcriptional repressors and catalytic enzymes of thiamine biosynthesis. J. Bacteriol. 199:e00810–16 [Google Scholar]
  73. Imlay JA. 73.  2003. Pathways of oxidative damage. Annu. Rev. Microbiol. 57:395–418 [Google Scholar]
  74. Isom CE, Turner JL, Lessner DJ, Karr EA. 74.  2013. Redox-sensitive DNA binding by homodimeric Methanosarcina acetivorans MsvR is modulated by cysteine residues. BMC Microbiol 13:163 [Google Scholar]
  75. Jäger D, Pernitzsch SR, Richter AS, Backofen R, Sharma CM, Schmitz RA. 75.  2012. An archaeal sRNA targeting cis- and trans-encoded mRNAs via two distinct domains. Nucleic Acids Res 40:10964–79 [Google Scholar]
  76. Jäger D, Sharma CM, Thomsen J, Ehlers C, Vogel J, Schmitz RA. 76.  2009. Deep sequencing analysis of the Methanosarcina mazei Gö1 transcriptome in response to nitrogen availability. PNAS 106:21878–82 [Google Scholar]
  77. Kanai T, Akerboom J, Takedomi S, van de Werken HJ, Blombach F. 77.  et al. 2007. A global transcriptional regulator in Thermococcus kodakaraensis controls the expression levels of both glycolytic and gluconeogenic enzyme–encoding genes. J. Biol. Chem. 282:33659–70 [Google Scholar]
  78. Karr EA. 78.  2010. The methanogen-specific transcription factor MsvR regulates the fpaA-rlp-rub oxidative stress operon adjacent to msvR in Methanothermobacter thermautotrophicus. J. Bacteriol. 192:5914–22 [Google Scholar]
  79. Karr EA. 79.  2014. Transcription regulation in the third domain. Adv. Appl. Microbiol. 89:101–33 [Google Scholar]
  80. Kashefi K, Lovley DR. 80.  2003. Extending the upper temperature limit for life. Science 301:934 [Google Scholar]
  81. Kaur A, Pan M, Meislin M, Facciotti MT, El-Gewely R, Baliga NS. 81.  2006. A systems view of haloarchaeal strategies to withstand stress from transition metals. Genome Res 16:841–54 [Google Scholar]
  82. Kaur A, Van PT, Busch CR, Robinson CK, Pan M. 82.  et al. 2010. Coordination of frontline defense mechanisms under severe oxidative stress. Mol. Syst. Biol. 6:393 [Google Scholar]
  83. Kiljunen S, Pajunen MI, Dilks K, Storf S, Pohlschroder M, Savilahti H. 83.  2014. Generation of comprehensive transposon insertion mutant library for the model archaeon, Haloferax volcanii, and its use for gene discovery. BMC Biol 12:103 [Google Scholar]
  84. Kim M, Park S, Lee SJ. 84.  2016. Global transcriptional regulator TrmB family members in prokaryotes. J. Microbiol. 54:639–45 [Google Scholar]
  85. Kim MS, Choi AR, Lee SH, Jung HC, Bae SS. 85.  et al. 2015. A novel CO-responsive transcriptional regulator and enhanced H2 production by an engineered Thermococcus onnurineus NA1 strain. Appl. Environ. Microbiol. 81:1708–14 [Google Scholar]
  86. Koide T, Reiss DJ, Bare JC, Pang WL, Facciotti MT. 86.  et al. 2009. Prevalence of transcription promoters within archaeal operons and coding sequences. Mol. Syst. Biol. 5:285 [Google Scholar]
  87. Koonin EV. 87.  2016. Horizontal gene transfer: essentiality and evolvability in prokaryotes, and roles in evolutionary transitions. F1000Research 5:F1000 Faculty Rev.1805 [Google Scholar]
  88. Kottemann M, Kish A, Iloanusi C, Bjork S, DiRuggiero J. 88.  2005. Physiological responses of the halophilic archaeon Halobacterium sp. strain NRC1 to desiccation and γ irradiation. Extremophiles 9:219–27 [Google Scholar]
  89. Krug M, Lee SJ, Boos W, Diederichs K, Welte W. 89.  2013. The three-dimensional structure of TrmB, a transcriptional regulator of dual function in the hyperthermophilic archaeon Pyrococcus furiosus in complex with sucrose. Protein Sci 22:800–8 [Google Scholar]
  90. Lecompte O, Ripp R, Puzos-Barbe V, Duprat S, Heilig R. 90.  et al. 2001. Genome evolution at the genus level: comparison of three complete genomes of hyperthermophilic archaea. Genome Res 11:981–93 [Google Scholar]
  91. Lee SJ, Moulakakis C, Koning SM, Hausner W, Thomm M, Boos W. 91.  2005. TrmB, a sugar sensing regulator of ABC transporter genes in Pyrococcus furiosus exhibits dual promoter specificity and is controlled by different inducers. Mol. Microbiol. 57:1797–807 [Google Scholar]
  92. Lee SJ, Surma M, Hausner W, Thomm M, Boos W. 92.  2008. The role of TrmB and TrmB-like transcriptional regulators for sugar transport and metabolism in the hyperthermophilic archaeon Pyrococcus furiosus. Arch. Microbiol. 190:247–56 [Google Scholar]
  93. Leigh JA, Albers SV, Atomi H, Allers T. 93.  2011. Model organisms for genetics in the domain Archaea: methanogens, halophiles, Thermococcales and Sulfolobales. FEMS Microbiol. Rev. 35:577–608 [Google Scholar]
  94. Leyn SA, Rodionov DA. 94.  2015. Comparative genomics of DtxR family regulons for metal homeostasis in Archaea. J. Bacteriol. 197:451–58 [Google Scholar]
  95. Leyn SA, Rodionova IA, Li X, Rodionov DA. 95.  2015. Novel transcriptional regulons for autotrophic cycle genes in Crenarchaeota. J. Bacteriol. 197:2383–91 [Google Scholar]
  96. Li H, Johnson AD. 96.  2010. Evolution of transcription networks—lessons from yeasts. Curr. Biol. 20:R746–53 [Google Scholar]
  97. Li L, Li Q, Rohlin L, Kim U, Salmon K. 97.  et al. 2007. Quantitative proteomic and microarray analysis of the archaeon Methanosarcina acetivorans grown with acetate versus methanol. J. Proteome Res. 6:759–71 [Google Scholar]
  98. Li SJ, Hua ZS, Huang LN, Li J, Shi SH. 98.  et al. 2014. Microbial communities evolve faster in extreme environments. Sci. Rep. 4:6205 [Google Scholar]
  99. Littlefield O, Korkhin Y, Sigler PB. 99.  1999. The structural basis for the oriented assembly of a TBP/TFB/promoter complex. PNAS 96:13668–73 [Google Scholar]
  100. Liu H, Han J, Liu X, Zhou J, Xiang H. 100.  2011. Development of pyrF-based gene knockout systems for genome-wide manipulation of the archaea Haloferax mediterranei and Haloarcula hispanica. J. Genet. Genom. 38:261–69 [Google Scholar]
  101. Liu H, Orell A, Maes D, van Wolferen M, Lindås AC. 101.  et al. 2014. BarR, an Lrp-type transcription factor in Sulfolobus acidocaldarius, regulates an aminotransferase gene in a β-alanine responsive manner. Mol. Microbiol. 92:625–39 [Google Scholar]
  102. Liu T, Li Y, Wang X, Ye Q, Li H. 102.  et al. 2015. Transcriptional regulator–mediated activation of adaptation genes triggers CRISPR de novo spacer acquisition. Nucleic Acids Res 43:1044–55 [Google Scholar]
  103. Lu Q, Han J, Zhou L, Coker JA, DasSarma P. 103.  et al. 2008. Dissection of the regulatory mechanism of a heat-shock responsive promoter in Haloarchaea: a new paradigm for general transcription factor directed archaeal gene regulation. Nucleic Acids Res 36:3031–42 [Google Scholar]
  104. Lundgren M, Bernander R. 104.  2007. Genome-wide transcription map of an archaeal cell cycle. PNAS 104:2939–44 [Google Scholar]
  105. Ma HW, Kumar B, Ditges U, Gunzer F, Buer J, Zeng AP. 105.  2004. An extended transcriptional regulatory network of Escherichia coli and analysis of its hierarchical structure and network motifs. Nucleic Acids Res 32:6643–49 [Google Scholar]
  106. Macneil LT, Walhout AJ. 106.  2011. Gene regulatory networks and the role of robustness and stochasticity in the control of gene expression. Genome Res 21:645–57 [Google Scholar]
  107. Maeder DL, Anderson I, Brettin TS, Bruce DC, Gilna P. 107.  et al. 2006. The Methanosarcina barkeri genome: comparative analysis with Methanosarcina acetivorans and Methanosarcina mazei reveals extensive rearrangement within methanosarcinal genomes. J. Bacteriol. 188:7922–31 [Google Scholar]
  108. Maeder DL, Weiss RB, Dunn DM, Cherry JL, Gonzalez JM. 108.  et al. 1999. Divergence of the hyperthermophilic archaea Pyrococcus furiosus and P. horikoshii inferred from complete genomic sequences. Genetics 152:1299–305 [Google Scholar]
  109. Makarova KS, Wolf YI, Koonin EV. 109.  2015. Archaeal clusters of orthologous genes (arCOGs): an update and application for analysis of shared features between Thermococcales, Methanococcales, and Methanobacteriales. Life 5:818–40 [Google Scholar]
  110. Marbach D, Costello JC, Kuffner R, Vega NM, Prill RJ. 110.  et al. 2012. Wisdom of crowds for robust gene network inference. Nat. Methods 9:796–804 [Google Scholar]
  111. Martinez-Pastor M, Lancaster WA, Tonner PD, Adams MWW, Schmid AK. 111.  2017. A transcription network of interlocking positive feedback loops maintains intracellular iron balance in archaea. Nucleic Acids Res 45:9990–10001 [Google Scholar]
  112. Milo R, Shen-Orr S, Itzkovitz S, Kashtan N, Chklovskii D, Alon U. 112.  2002. Network motifs: simple building blocks of complex networks. Science 298:824–27 [Google Scholar]
  113. Müller JA, DasSarma S. 113.  2005. Genomic analysis of anaerobic respiration in the archaeon Halobacterium sp. strain NRC-1: dimethyl sulfoxide and trimethylamine N-oxide as terminal electron acceptors. J. Bacteriol. 187:1659–67 [Google Scholar]
  114. Nagy J, Grohmann D, Cheung ACM, Schulz S, Smollett K. 114.  et al. 2015. Complete architecture of the archaeal RNA polymerase open complex from single-molecule FRET and NPS. Nature Commun 6:6161 [Google Scholar]
  115. Naor A, Lapierre P, Mevarech M, Papke RT, Gophna U. 115.  2012. Low species barriers in halophilic archaea and the formation of recombinant hybrids. Curr. Biol. 22:1444–48 [Google Scholar]
  116. Ng WV, Kennedy SP, Mahairas GG, Berquist B, Pan M. 116.  et al. 2000. Genome sequence of Halobacterium species NRC-1. PNAS 97:12176–81 [Google Scholar]
  117. Nguyen-Duc T, Peeters E, Muyldermans S, Charlier D, Hassanzadeh-Ghassabeh G. 117.  2013a. Nanobody®-based chromatin immunoprecipitation/micro-array analysis for genome-wide identification of transcription factor DNA binding sites. Nucleic Acids Res 41:e59 [Google Scholar]
  118. Nguyen-Duc T, van Oeffelen L, Song N, Hassanzadeh-Ghassabeh G, Muyldermans S. 118.  et al. 2013b. The genome-wide binding profile of the Sulfolobus solfataricus transcription factor Ss-LrpB shows binding events beyond direct transcription regulation. BMC Genom 14:828 [Google Scholar]
  119. Nitzan M, Fechter P, Peer A, Altuvia Y, Bronesky D. 119.  et al. 2015. A defense–offense multi-layered regulatory switch in a pathogenic bacterium. Nucleic Acids Res 43:1357–69 [Google Scholar]
  120. Offre P, Spang A, Schleper C. 120.  2013. Archaea in biogeochemical cycles. Annu. Rev. Microbiol. 67:437–57 [Google Scholar]
  121. Okamura H, Yokoyama K, Koike H, Yamada M, Shimowasa A. 121.  et al. 2007. A structural code for discriminating between transcription signals revealed by the feast/famine regulatory protein DM1 in complex with ligands. Structure 15:1325–38 [Google Scholar]
  122. Oren A. 122.  2008. Microbial life at high salt concentrations: phylogenetic and metabolic diversity. Saline Syst 4:2 [Google Scholar]
  123. Oren A. 123.  2014. Halophilic archaea on Earth and in space: growth and survival under extreme conditions. Philos. Trans. R. Soc. A 372:20140194 [Google Scholar]
  124. Ouhammouch M, Dewhurst RE, Hausner W, Thomm M, Geiduschek EP. 124.  2003. Activation of archaeal transcription by recruitment of the TATA-binding protein. PNAS 100:5097–102 [Google Scholar]
  125. Ouhammouch M, Geiduschek EP. 125.  2005. An expanding family of archaeal transcriptional activators. PNAS 102:15423–28 [Google Scholar]
  126. Peeters E, Albers SV, Vassart A, Driessen AJ, Charlier D. 126.  2009. Ss-LrpB, a transcriptional regulator from Sulfolobus solfataricus, regulates a gene cluster with a pyruvate ferredoxin oxidoreductase–encoding operon and permease genes. Mol. Microbiol. 71:972–88 [Google Scholar]
  127. Peeters E, Charlier D. 127.  2010. The Lrp family of transcription regulators in archaea. Archaea 2010:750457 [Google Scholar]
  128. Peeters E, Peixeiro N, Sezonov G. 128.  2013. Cis-regulatory logic in archaeal transcription. Biochem. Soc. Trans. 41:326–31 [Google Scholar]
  129. Peeters E, Thia-Toong TL, Gigot D, Maes D, Charlier D. 129.  2004. Ss-LrpB, a novel Lrp-like regulator of Sulfolobus solfataricus P2, binds cooperatively to three conserved targets in its own control region. Mol. Microbiol. 54:321–36 [Google Scholar]
  130. Peng N, Xia Q, Chen Z, Liang YX, She Q. 130.  2009. An upstream activation element exerting differential transcriptional activation on an archaeal promoter. Mol. Microbiol. 74:928–39 [Google Scholar]
  131. Perez JC, Groisman EA. 131.  2009. Evolution of transcriptional regulatory circuits in bacteria. Cell 138:233–44 [Google Scholar]
  132. Perez-Rueda E, Janga SC. 132.  2010. Identification and genomic analysis of transcription factors in archaeal genomes exemplifies their functional architecture and evolutionary origin. Mol. Biol. Evol. 27:1449–59 [Google Scholar]
  133. Peters JM, Colavin A, Shi H, Czarny TL, Larson MH. 133.  et al. 2016. A comprehensive, CRISPR-based functional analysis of essential genes in bacteria. Cell 165:1493–506 [Google Scholar]
  134. Peterson JR, Labhsetwar P, Ellermeier JR, Kohler PR, Jain A. 134.  et al. 2014. Towards a computational model of a methane producing archaeum. Archaea 2014:898453 [Google Scholar]
  135. Pfeifer F, Blaseio U. 135.  1990. Transposition burst of the ISH27 insertion element family in Halobacterium halobium. Nucleic Acids Res 18:6921–25 [Google Scholar]
  136. Pfeiffer F, Broicher A, Gillich T, Klee K, Mejia J. 136.  et al. 2008a. Genome information management and integrated data analysis with HaloLex. Arch. Microbiol. 190:281–99 [Google Scholar]
  137. Pfeiffer F, Schuster SC, Broicher A, Falb M, Palm P. 137.  et al. 2008b. Evolution in the laboratory: the genome of Halobacterium salinarum strain R1 compared to that of strain NRC-1. Genomics 91:335–46 [Google Scholar]
  138. Plaisier CL, Lo FY, Ashworth J, Brooks AN, Beer KD. 138.  et al. 2014. Evolution of context dependent regulation by expansion of feast/famine regulatory proteins. BMC Syst. Biol. 8:122 [Google Scholar]
  139. Prasse D, Förstner KU, Jäger D, Backofen R, Schmitz RA. 139.  2017. sRNA154 a newly identified regulator of nitrogen fixation in Methanosarcina mazei strain Gö1. RNA Biol 15:1–5 [Google Scholar]
  140. Price MN, Dehal PS, Arkin AP. 140.  2008. Horizontal gene transfer and the evolution of transcriptional regulation in Escherichia coli. Genome Biol 9:R4 [Google Scholar]
  141. Ptashne M, Gann A. 141.  2002. Genes and Signals Cold Spring Harbor, NY: Cold Spring Harb. Lab. [Google Scholar]
  142. Qi Q, Ito Y, Yoshimatsu K, Fujiwara T. 142.  2016. Transcriptional regulation of dimethyl sulfoxide respiration in a haloarchaeon, Haloferax volcanii. Extremophiles 20:27–36 [Google Scholar]
  143. Raymann K, Brochier-Armanet C, Gribaldo S. 143.  2015. The two-domain tree of life is linked to a new root for the Archaea. PNAS 112:6670–75 [Google Scholar]
  144. Reichelt R, Gindner A, Thomm M, Hausner W. 144.  2016. Genome-wide binding analysis of the transcriptional regulator TrmBL1 in Pyrococcus furiosus. BMC Genom 17:40 [Google Scholar]
  145. Reichlen MJ, Murakami KS, Ferry JG. 145.  2010. Functional analysis of the three TATA binding protein homologs in Methanosarcina acetivorans. J. Bacteriol. 192:1511–17 [Google Scholar]
  146. Reichlen MJ, Vepachedu VR, Murakami KS, Ferry JG. 146.  2012. MreA functions in the global regulation of methanogenic pathways in Methanosarcina acetivorans. mBio 3:e00189–12 [Google Scholar]
  147. Reiss DJ, Baliga NS, Bonneau R. 147.  2006. Integrated biclustering of heterogeneous genome-wide datasets for the inference of global regulatory networks. BMC Bioinform 7:280 [Google Scholar]
  148. Reiss DJ, Plaisier CL, Wu WJ, Baliga NS. 148.  2015. cMonkey2: automated, systematic, integrated detection of co-regulated gene modules for any organism. Nucleic Acids Res 43:e87 [Google Scholar]
  149. Renfrow MB, Naryshkin N, Lewis LM, Chen HT, Ebright RH, Scott RA. 149.  2004. Transcription factor B contacts promoter DNA near the transcription start site of the archaeal transcription initiation complex. J. Biol. Chem. 279:2825–31 [Google Scholar]
  150. Rodionov DA, Leyn SA, Li X, Rodionova IA. 150.  2017. A novel transcriptional regulator related to thiamine phosphate synthase controls thiamine metabolism genes in Archaea. J. Bacteriol. 199:e00743–16 [Google Scholar]
  151. Rodionova IA, Vetting MW, Li X, Almo SC, Osterman AL, Rodionov DA. 151.  2017. A novel bifunctional transcriptional regulator of riboflavin metabolism in Archaea. Nucleic Acids Res 45:3785–99 [Google Scholar]
  152. Rutherford JC, Jaron S, Winge DR. 152.  2003. Aft1p and Aft2p mediate iron-responsive gene expression in yeast through related promoter elements. J. Biol. Chem. 278:27636–43 [Google Scholar]
  153. Sapienza C, Rose MR, Doolittle WF. 153.  1982. High-frequency genomic rearrangements involving archaebacterial repeat sequence elements. Nature 299:182–85 [Google Scholar]
  154. Sarmiento F, Mrazek J, Whitman WB. 154.  2013. Genome-scale analysis of gene function in the hydrogenotrophic methanogenic archaeon Methanococcus maripaludis. PNAS 110:4726–31 [Google Scholar]
  155. Schmid AK, Pan M, Sharma K, Baliga NS. 155.  2011. Two transcription factors are necessary for iron homeostasis in a salt-dwelling archaeon. Nucleic Acids Res 39:2519–33 [Google Scholar]
  156. Schmid AK, Reiss DJ, Kaur A, Pan M, King N. 156.  et al. 2007. The anatomy of microbial cell state transitions in response to oxygen. Genome Res 17:1399–413 [Google Scholar]
  157. Schmid AK, Reiss DJ, Pan M, Koide T, Baliga NS. 157.  2009. A single transcription factor regulates evolutionarily diverse but functionally linked metabolic pathways in response to nutrient availability. Mol. Syst. Biol. 5:282 [Google Scholar]
  158. Schulz S, Gietl A, Smollett K, Tinnefeld P, Werner F, Grohmann D. 158.  2016. TFE and Spt4/5 open and close the RNA polymerase clamp during the transcription cycle. PNAS 113:E1816–25 [Google Scholar]
  159. Schut GJ, Brehm SD, Datta S, Adams MW. 159.  2003. Whole-genome DNA microarray analysis of a hyperthermophile and an archaeon: Pyrococcus furiosus grown on carbohydrates or peptides. J. Bacteriol. 185:3935–47 [Google Scholar]
  160. Schwaiger R, Schwarz C, Furtwangler K, Tarasov V, Wende A, Oesterhelt D. 160.  2010. Transcriptional control by two leucine-responsive regulatory proteins in Halobacterium salinarum R1. BMC Mol. Biol. 11:40 [Google Scholar]
  161. Seckbach J. 161.  2013. Polyextremophiles: Life Under Multiple Forms of Stress Dordrecht, Neth./New York: Springer [Google Scholar]
  162. Seitzer P, Wilbanks EG, Larsen DJ, Facciotti MT. 162.  2012. A Monte Carlo–based framework enhances the discovery and interpretation of regulatory sequence motifs. BMC Bioinform 13:317 [Google Scholar]
  163. Sharma K, Gillum N, Boyd JL, Schmid A. 163.  2012. The RosR transcription factor is required for gene expression dynamics in response to extreme oxidative stress in a hypersaline-adapted archaeon. BMC Genom 13:351 [Google Scholar]
  164. She Q, Singh RK, Confalonieri F, Zivanovic Y, Allard G. 164.  et al. 2001. The complete genome of the crenarchaeon Sulfolobus solfataricus P2. PNAS 98:7835–40 [Google Scholar]
  165. Shen-Orr SS, Milo R, Mangan S, Alon U. 165.  2002. Network motifs in the transcriptional regulation network of Escherichia coli. Nat. Genet. 31:64–68 [Google Scholar]
  166. Smollett K, Blombach F, Reichelt R, Thomm M, Werner F. 166.  2017. A global analysis of transcription reveals two modes of Spt4/5 recruitment to archaeal RNA polymerase. Nature Microbiol 2:17021 [Google Scholar]
  167. Song N, Nguyen Duc T, van Oeffelen L, Muyldermans S, Peeters E, Charlier D. 167.  2013. Expanded target and cofactor repertoire for the transcriptional activator LysM from Sulfolobus. Nucleic Acids Res 41:2932–49 [Google Scholar]
  168. Sorrells TR, Johnson AD. 168.  2015. Making sense of transcription networks. Cell 161:714–23 [Google Scholar]
  169. Spang A, Saw JH, Jørgensen SL, Zaremba-Niedzwiedzka K, Martijn J. 169.  et al. 2015. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521:173–79 [Google Scholar]
  170. Stachler AE, Marchfelder A. 170.  2016. Gene repression in haloarchaea using the CRISPR (clustered regularly interspaced short palindromic repeats)-Cas I-B system. J. Biol. Chem. 291:15226–42 [Google Scholar]
  171. Storz G, Altuvia S, Wassarman KM. 171.  2005. An abundance of RNA regulators. Annu. Rev. Biochem. 74:199–217 [Google Scholar]
  172. Sun J, Klein A. 172.  2004. A lysR-type regulator is involved in the negative regulation of genes encoding selenium-free hydrogenases in the archaeon Methanococcus voltae. Mol. Microbiol. 52:563–71 [Google Scholar]
  173. Tapias A, Leplat C, Confalonieri F. 173.  2009. Recovery of ionizing-radiation damage after high doses of γ ray in the hyperthermophilic archaeon Thermococcus gammatolerans. Extremophiles 13:333–43 [Google Scholar]
  174. Tebbe A, Schmidt A, Konstantinidis K, Falb M, Bisle B. 174.  et al. 2009. Life-style changes of a halophilic archaeon analyzed by quantitative proteomics. Proteomics 9:3843–55 [Google Scholar]
  175. Todor H, Dulmage K, Gillum N, Bain JR, Muehlbauer MJ, Schmid AK. 175.  2014. A transcription factor links growth rate and metabolism in the hypersaline adapted archaeon Halobacterium salinarum. Mol. Microbiol. 93:1172–82 [Google Scholar]
  176. Todor H, Gooding J, Ilkayeva OR, Schmid AK. 176.  2015. Dynamic metabolite profiling in an archaeon connects transcriptional regulation to metabolic consequences. PLOS ONE 10:e0135693 [Google Scholar]
  177. Todor H, Sharma K, Pittman AM, Schmid AK. 177.  2013. Protein–DNA binding dynamics predict transcriptional response to nutrients in archaea. Nucleic Acids Res 41:8546–58 [Google Scholar]
  178. Tonner PD, Darnell CL, Engelhardt BE, Schmid AK. 178.  2017. Detecting differential growth of microbial populations with Gaussian process regression. Genome Res 27:320–33 [Google Scholar]
  179. Tonner PD, Pittman AM, Gulli JG, Sharma K, Schmid AK. 179.  2015. A regulatory hierarchy controls the dynamic transcriptional response to extreme oxidative stress in archaea. PLOS Genet 11:e1004912 [Google Scholar]
  180. Turkarslan S, Reiss DJ, Gibbins G, Su WL, Pan M. 180.  et al. 2011. Niche adaptation by expansion and reprogramming of general transcription factors. Mol. Syst. Biol. 7:554 [Google Scholar]
  181. Van PT, Schmid AK, King NL, Kaur A, Pan M. 181.  et al. 2008. Halobacterium salinarum NRC-1 PeptideAtlas: toward strategies for targeted proteomics and improved proteome coverage. J. Proteome Res. 7:3755–64 [Google Scholar]
  182. van de Werken HJ, Verhees CH, Akerboom J, de Vos WM, van der Oost J. 182.  2006. Identification of a glycolytic regulon in the archaea Pyrococcus and Thermococcus. FEMS Microbiol. Lett. 260:69–76 [Google Scholar]
  183. van Wageningen S, Kemmeren P, Lijnzaad P, Margaritis T, Benschop JJ. 183.  et al. 2010. Functional overlap and regulatory links shape genetic interactions between signaling pathways. Cell 143:991–1004 [Google Scholar]
  184. Veit K, Ehlers C, Ehrenreich A, Salmon K, Hovey R. 184.  et al. 2006. Global transcriptional analysis of Methanosarcina mazei strain Gö1 under different nitrogen availabilities. Mol. Genet. Genom. 276:41–55 [Google Scholar]
  185. Wagner M, Wagner A, Ma X, Kort JC, Ghosh A. 185.  et al. 2014. Investigation of the malE promoter and MalR, a positive regulator of the maltose regulon, for an improved expression system in Sulfolobus acidocaldarius. Appl. Environ. Microbiol. 80:1072–81 [Google Scholar]
  186. Weidenbach K, Ehlers C, Kock J, Ehrenreich A, Schmitz RA. 186.  2008a. Insights into the NrpR regulon in Methanosarcina mazei Gö1. Arch. Microbiol. 190:319–32 [Google Scholar]
  187. Weidenbach K, Ehlers C, Kock J, Schmitz RA. 187.  2010. NrpRII mediates contacts between NrpRI and general transcription factors in the archaeon Methanosarcina mazei Gö1. FEBS J 277:4398–411 [Google Scholar]
  188. Weidenbach K, Ehlers C, Schmitz RA. 188.  2014. The transcriptional activator NrpA is crucial for inducing nitrogen fixation in Methanosarcina mazei Gö1 under nitrogen-limited conditions. FEBS J 281:3507–22 [Google Scholar]
  189. Weidenbach K, Gloer J, Ehlers C, Sandman K, Reeve JN, Schmitz RA. 189.  2008b. Deletion of the archaeal histone in Methanosarcina mazei Gö1 results in reduced growth and genomic transcription. Mol. Microbiol. 67:662–71 [Google Scholar]
  190. Werner F, Grohmann D. 190.  2011. Evolution of multisubunit RNA polymerases in the three domains of life. Nat. Rev. Microbiol. 9:85–98 [Google Scholar]
  191. Whitehead K, Kish A, Pan M, Kaur A, Reiss DJ. 191.  et al. 2006. An integrated systems approach for understanding cellular responses to γ radiation. Mol. Syst. Biol. 2:47 [Google Scholar]
  192. Wilbanks EG, Larsen DJ, Neches RY, Yao AI, Wu CY. 192.  et al. 2012. A workflow for genome-wide mapping of archaeal transcription factors with ChIP-seq. Nucleic Acids Res 40:e74 [Google Scholar]
  193. Williams E, Lowe TM, Savas J, DiRuggiero J. 193.  2007. Microarray analysis of the hyperthermophilic archaeon Pyrococcus furiosus exposed to γ irradiation. Extremophiles 11:19–29 [Google Scholar]
  194. Wohlbach DJ, Thompson DA, Gasch AP, Regev A. 194.  2009. From elements to modules: regulatory evolution in Ascomycota fungi. Curr. Opin. Genet. Dev. 19:571–78 [Google Scholar]
  195. Wurtzel O, Sapra R, Chen F, Zhu Y, Simmons BA, Sorek R. 195.  2010. A single-base resolution map of an archaeal transcriptome. Genome Res 20:133–41 [Google Scholar]
  196. Xia Q, Hendrickson EL, Zhang Y, Wang T, Taub F. 196.  et al. 2006. Quantitative proteomics of the archaeon Methanococcus maripaludis validated by microarray analysis and real time PCR. Mol. Cell Proteom. 5:868–81 [Google Scholar]
  197. Yoon SH, Reiss DJ, Bare JC, Tenenbaum D, Pan M. 197.  et al. 2011. Parallel evolution of transcriptome architecture during genome reorganization. Genome Res 21:1892–904 [Google Scholar]
  198. Yoon SH, Turkarslan S, Reiss DJ, Pan M, Burn JA. 198.  et al. 2013. A systems level predictive model for global gene regulation of methanogenesis in a hydrogenotrophic methanogen. Genome Res 23:1839–51 [Google Scholar]
  199. Yu H, Gerstein M. 199.  2006. Genomic analysis of the hierarchical structure of regulatory networks. PNAS 103:14724–31 [Google Scholar]
  200. Zaigler A, Schuster SC, Soppa J. 200.  2003. Construction and usage of a onefold-coverage shotgun DNA microarray to characterize the metabolism of the archaeon Haloferax volcanii. Mol. Microbiol. 48:1089–105 [Google Scholar]
  201. Zaremba-Niedzwiedzka K, Caceres EF, Saw JH, Backstrom D, Juzokaite L. 201.  et al. 2017. Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541:353–58 [Google Scholar]
  202. Zebec Z, Manica A, Zhang J, White MF, Schleper C. 202.  2014. CRISPR-mediated targeted mRNA degradation in the archaeon Sulfolobus solfataricus. Nucleic Acids Res 42:5280–88 [Google Scholar]
  203. Zhao B, Yan Y, Chen S. 203.  2014. How could haloalkaliphilic microorganisms contribute to biotechnology?. Can. J. Microbiol. 60:717–27 [Google Scholar]
  204. Zhu Y, Kumar S, Menon AL, Scott RA, Adams MW. 204.  2013. Regulation of iron metabolism by Pyrococcus furiosus. J. Bacteriol. 195:2400–7 [Google Scholar]
/content/journals/10.1146/annurev-genet-120116-023413
Loading
/content/journals/10.1146/annurev-genet-120116-023413
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error