Skip to main content

Recent Advances in the Nitrogen Metabolism in Haloarchaea and Its Biotechnological Applications

  • Chapter
  • First Online:
Biotechnology of Extremophiles:

Abstract

Halophilic archaea belong to the third domain of life, which live and survive in a highly salty environment. Nitrate assimilation is one of the main processes of the N-cycle, allowing the use of NO3 , NO2 and/or NH4 + as N source for growth. This pathway in general termed “Assimilatory nitrate pathway or assimilatory nitrate reduction” includes not only assimilatory nitrate reduction but also the assimilation of nitrite and ammonium. In the assimilatory nitrate reduction, NO3 is finally reduced to NH4 + by two sequential reactions catalysed by a ferredoxin-dependent nitrate reductase (Nas; EC 1.6.6.2) and a ferredoxin-dependent nitrite reductase (Nir; EC 1.7.7.1). The glutamine synthetase/glutamate synthase pathway (GS-GOGAT; EC 6.3.1.2, EC 1.4.7.1, respectively) or l-glutamate dehydrogenase (GDH; EC 1.4.1.2) are responsible for incorporating NH4 + into carbon skeletons. This chapter reviews current knowledge on nitrogen metabolism in haloarchaea with emphasis on assimilatory nitrate reduction, proteins involved and its regulation.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
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

  • Adul Rahman RN, Jongsareejit B, Fujiwara S, Imanaka T (1997) Characterization of recombinant glutamine synthetase from the hyperthermophilic archaeon Pyrococcus sp. strain KOD1. Appl Environ Microbiol 63:2472–2476

    CAS  PubMed  PubMed Central  Google Scholar 

  • Alcántara-Hernández RJ, Valenzuela-Encinas C, Zavala-Díaz de la Serna FJ, Rodriguez-Revilla J, Dendooven L, Marsch R (2009) Haloarchaeal assimilatory nitrate-reducing communities from a saline alkaline soil. FEMS Microbiol Lett 298(1):56–66

    Article  PubMed  Google Scholar 

  • Andrade SL, Einsle O (2007) The Amt/Mep/Rh family of ammonium transport proteins. Mol Membr Biol 24:357–365

    Article  CAS  PubMed  Google Scholar 

  • Andrade SL, Dickmanns A, Ficner R, Einsle O (2005) Crystal structure of the archaeal ammonium transporter Amt-1 from Archaeoglobus fulgidus. Proc Natl Acad Sci U S A 102:14994–14999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Asker D, Ohta Y (2002) Production of canthaxanthin by Haloferax alexandrines under non-aseptic conditions and a simple, rapid method for its extraction. Appl Microbiol Biotechnol 58:743–750

    Article  CAS  PubMed  Google Scholar 

  • Bauernfeind JC (1981) Natural food colors. In: Bauernfeind JC, Stewart GF, Schweigert BS, Hawthorn J (eds) Carotenoids as colorants and vitamin A precursors. Technological and nutritional applications. Academic Press, New York, pp 1–45. ISBN:978-0-12-082850-0

    Google Scholar 

  • Beckers G, Nolden L, Burkovski A (2001) Glutamate synthase of Corynebacterium glutamicum is not essential for glutamate synthesis and is regulated by the nitrogen status. Microbiology 147(11):2961–2970

    Article  CAS  PubMed  Google Scholar 

  • Beinert H (2000) Iron–sulfur proteins: ancient structures, still full of surprises. J Biol Inorg Chem 5:2–15

    Article  CAS  PubMed  Google Scholar 

  • Belitsky BR, Wray LV, Fisher SH, Bohannon DE, Sonenshein AL (2000) Role of TnrA in nitrogen source-dependent repression of bacillus subtilis glutamate synthase gene expression. J Bacteriol 182(21):5939–5947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonete MJ, Camacho ML, Cadenas E (1986) Purification and some properties of NAD + -dependent glutamate dehydrogenase from Halobacterium halobium. Int J Biochem 18:785–789

    Article  CAS  Google Scholar 

  • Bonete MJ, Camacho ML, Cadenas E (1987) A new glutamate dehydrogenase from Halobacterium halobium with different coenzyme specificity. Int J Biochem 19:1149–1155

    Article  CAS  Google Scholar 

  • Bonete MJ, Perez-Pomares F, Ferrer J, Camacho ML (1996) NAD-glutamate dehydrogenase from Halobacterium halobium: inhibition and activation by TCA intermediates and amino acids. Biochim Biophys Acta 1289(1):14–24

    Article  PubMed  Google Scholar 

  • Bonete MJ, Martínez-Espinosa RM, Pire C, Zafrilla B, Richardson DJ (2008) Nitrogen metabolism in haloarchaea. Saline Syst 4:9. doi:10.1186/1746-1448-4-9

    Article  PubMed  PubMed Central  Google Scholar 

  • Bowsher CG, Lacey AE, Hanke GT, Clarkson DT, Saker LR, Stulen I, Emes MJ (2007) The effect of Glc6P uptake and its subsequent oxidation within pea root plastids on nitrite reduction and glutamate synthesis. J Exp Bot 58(5):1109–1118

    Article  CAS  PubMed  Google Scholar 

  • Brown JR, Masuchi Y, Robb FT, Doolittle WF (1994) Evolutionary relationships of bacterial and archaeal glutamine synthetase genes. J Mol Evol 38(6):566–576

    Article  CAS  PubMed  Google Scholar 

  • Campbell WH, Kinghorn JR (1990) Functional domains of assimilatory nitrate reductase and nitrite reductases. Trends Biochem Sci 15:315–319

    Article  CAS  PubMed  Google Scholar 

  • Carpenter KLH, van der Veen C, Hird R, Dennis IF, Ding T, Mitchinson MJ (1997) The carotenoids: β-carotene, canthaxanthin and zeaxanthin inhibit macrophage-mediated LDL oxidation. FEBS Lett 401:262–266

    Article  CAS  PubMed  Google Scholar 

  • Chai W, Stewart V (1998) NasR, a novel RNA-binding protein, mediates nitrate-responsive transcription antitermination of the Klebsiella oxytoca M5al nasF operon leader in vitro. J Mol Biol 283:339–351

    Article  CAS  PubMed  Google Scholar 

  • Chávez S, Lucena JM, Reyes JC, Florencio FJ, Candau P (1999) The presence of glutamate dehydrogenase is a selective advantage for the cyanobacterium Synechocystis sp. strain PCC 6803 under nonexponential growth conditions. J Bacteriol 181(3):808–813

    PubMed  PubMed Central  Google Scholar 

  • Chew BP, Park JS, Wong MW, Wong TSA (1999) Comparison of the anticancer activities of dietary β-carotene, canthaxanthin and astaxanthin in mice in vivo. Anticancer Res 19:1849–1853

    CAS  PubMed  Google Scholar 

  • Díaz S, Pérez-Pomares F, Pire C, Ferrer J, Bonete MJ (2006) Gene cloning, heterologous overexpression and optimized refolding of the NAD-glutamate dehydrogenase from Haloferax mediterranei. Extremophiles 10(2):105–115

    Article  PubMed  Google Scholar 

  • Dixon R, Kahn D (2004) Genetic regulation of biological nitrogen fixation. Nat Rev Microbiol 2(8):621–631

    Article  CAS  PubMed  Google Scholar 

  • Edge R, McGarvey DJ, Truscott TG (1997) The carotenoids as antioxidants – a review. J Photochem Photobiol B Biol 41:189–200

    Article  CAS  Google Scholar 

  • Ehlers C, Grabbe R, Veit K, Schmitz RA (2002) Characterization of GlnK1 from Methanosarcina mazei Strain Gö1: complementation of an Escherichia coli glnK Mutant Strain by GlnK1. J Bacteriol 184:1028–1040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ehlers C, Weidenbach K, Veit K, Forchhammer K, Schmitz RA (2005) Unique mechanistic features of post-translational regulation of glutamine synthetase activity in Methanosarcina mazei strain Gö1 in response to nitrogen availability. Mol Microbiol 55:1841–1854

    Article  CAS  PubMed  Google Scholar 

  • Esclapez J, Bravo-Barrales G, Bautista V, Pire C, Camacho M, Bonete MJ (2014) Effects of nitrogen sources on the nitrate assimilation in Haloferax mediterranei: growth kinetics and transcriptomic analysis. FEMS Microbiol Lett 350:168–174

    Article  CAS  PubMed  Google Scholar 

  • Esclapez J, Pire C, Camacho M, Bautista V, Martínez-Espinosa RM, Zafrilla B, Vegara A, Alcaraz LA, Bonete MJ (2015) Transcriptional profiles of Haloferax mediterranei based on nitrogen availability. J Biotechnol 193:100–107

    Article  CAS  PubMed  Google Scholar 

  • Fang CJ, Ku KL, Lee MH, Su NW (2010) Influence of nutritive factors on C50 carotenoids production by Haloferax mediterranei ATCC 33500 with two-stage cultivation. Bioresour Technol 101(16):6487–6493

    Article  CAS  PubMed  Google Scholar 

  • Feng J, Liu B, Zhang Z, Ren Y, Li Y, Gan F, Huang Y, Chen X, Shen P, Wang L, Tang B, Tang XF (2012) The complete genome sequence of Natrinema sp. J7-2, a haloarchaeon capable of growth on synthetic media without amino acid supplements. PLoS One 7(7), e41621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernández E, Galvan A, Quesada A (1998) Nitrogen assimilation and its regulation. In: The molecular biology of chloroplast and mitochondria in Chlamydomonas. Kluwer Academic Publishers, The Netherlands, pp 637–659

    Google Scholar 

  • Ferrer J, Pérez-Pomares F, Bonete MJ (1996) NADP-glutamate dehydrogenase from the halophilic archaeon Haloferax mediterranei: enzyme purification, N-terminal sequence and stability. FEMS Microbiol Lett 141(1):59–63

    Article  CAS  PubMed  Google Scholar 

  • Forchhammer K (2008) P(II) signal transducers: novel functional and structural insights. Trends Microbiol 16(2):65–72

    Article  CAS  PubMed  Google Scholar 

  • Forchhammer K (2010) The network of PII signalling protein interactions in unicellular cyanobacteria. Adv Exp Med Biol 675:71–90. Chap 5. doi:10.1007/978-1-4419-1528-3_5

    Google Scholar 

  • Forde BG, Lea PJ (2007) Glutamate in plants: metabolism, regulation, and signalling. J Exp Bot 58(9):2339–2358

    Article  CAS  PubMed  Google Scholar 

  • Frolow F, Harel M, Sussman JL, Mevarech M, Shoham M (1996) Insights into protein adaptation to a saturated salt environment from the crystal structure of a halophilic 2Fe-2S ferredoxin. Nat Struct Biol 3(5):452–458

    Article  CAS  PubMed  Google Scholar 

  • Geiger B, Mevarech M, Werber MM (1978) Immunochemical characterization of ferredoxin from Halobacterium of the Dead Sea. Eur J Biochem 84(2):449–455

    Article  CAS  PubMed  Google Scholar 

  • Heinrich A, Maheswaran M, Ruppert U, Forchhammer K (2004) The Synechococcus elongates PII signal transduction protein controls arginine synthesis by complex formation with N-acetyl-l-glutamate kinase. Mol Microbiol 52:1303–1314

    Article  CAS  PubMed  Google Scholar 

  • Helfmann S, Lü W, Litz C, Andrade SLA (2010) Cooperative binding of MgATP and MgADP in the trimeric PII protein GlnK2 from Archaeoglobus fulgidus. J Mol Biol 402:165–177

    Article  CAS  PubMed  Google Scholar 

  • Helling RB (1994) Why does Escherichia coli have two primary pathways for synthesis of glutamate? J Bacteriol 176:4664–4668

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hochman A, Nissany A, Amizur M (1988) Nitrate reduction and assimilation by a moderately halophilic, halotolerant bacterium Ba1. Biochim Biophys Acta 965(1):82–89

    Article  CAS  Google Scholar 

  • Ingoldsby LM, Geoghegan KF, Hayden BM, Engel PC (2005) The discovery of four distinct glutamate dehydrogenase genes in a strain of Halobacterium salinarum. Gene 349:237–244

    Article  CAS  PubMed  Google Scholar 

  • Javelle A, Severi E, Thornton J, Merrick M (2004) Ammonium sensing in Escherichia coli. Role of the ammonium transporter AmtB and AmtB–GlnK complex formation. J Biol Chem 279:8530–8538

    Article  CAS  PubMed  Google Scholar 

  • Jiang P, Mayo AE, Ninfa AJ (2007) Escherichia coli glutamine synthetase adenylyltransferase (ATase, EC 2.7.7.49): kinetic characterization of regulation by PII, PII-UMP, glutamine, and α-ketoglutarate. Biochemistry 46:4133–4146

    Article  CAS  PubMed  Google Scholar 

  • Kameya M, Ikeda T, Nakamura M, Arai H, Ishii M, Igarashi Y (2007) A novel ferredoxin-dependent glutamate synthase from the hydrogen-oxidizing chemoautotrophic bacterium Hydrogenobacter thermophilus TK-6. J Bacteriol 189(7):2805–2812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khademi S, Stroud RM (2006) The Amt/MEP/Rh family: structure of AmtB and the mechanism of ammonia gas conduction. Physiology (Bethesda) 21:419–429

    Article  CAS  Google Scholar 

  • Kumada Y, Benson DR, Hillemann D, Hosted TJ, Rochefort DA, Thompson CJ, Wohlleben W, Tateno Y (1993) Evolution of the glutamine synthetase gene, one of the oldest existing and functioning genes. Proc Natl Acad Sci USA 90:3009–3013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Labboun S, Tercé-Laforgue T, Roscher A, Bedu M, Restivo FM, Velanis CN et al (2009) Resolving the role of plant glutamate dehydrogenase. I. In vivo real time nuclear magnetic resonance spectroscopy experiments. Plant Cell Physiol 50:1761–1773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leigh JA, Dodsworth JA (2007) Nitrogen regulation in bacteria and archaea. Annu Rev Microbiol 61:349–377

    Article  CAS  PubMed  Google Scholar 

  • Lin JT, Stewart V (1998) Nitrate assimilation by bacteria. Adv Microb Physiol 39:330–379

    CAS  Google Scholar 

  • Litz C, Helfmann S, Gerhardt S, Andrade SLA (2011) Structure of GlnK1, a signaling protein from Archaeoglobus fulgidus. Acta Crystallogr 67:178–181

    CAS  Google Scholar 

  • Lledó B, Marhuenda-Egea FC, Martínez-Espinosa RM, Bonete MJ (2005) Identification and transcriptional analysis of nitrate assimilation genes in the halophilic archaeon Haloferax mediterranei. Gene 361:80–88

    Article  PubMed  Google Scholar 

  • Luque-Almagro VM, Gates AJ, Moreno-Vivián C, Ferguson SJ, Richardson DJ, Roldán MD (2011) Bacterial nitrate assimilation: gene distribution and regulation. Biochem Soc Trans 39:1838–1843

    Article  CAS  PubMed  Google Scholar 

  • Manitz B, Holldorf AW (1993) Purification and properties of glutamine synthetase from the archaebacterium Halobacterium salinarium. Arch Microbiol 159:90–97

    Article  CAS  Google Scholar 

  • Martínez-Espinosa RM, Marhuenda-Egea FC, Bonete MJ (2001a) Assimilatory nitrate reductase from the haloarchaeon Haloferax mediterranei: purification and characterisation. FEMS Microbiol Lett 204(2):381–385

    Article  PubMed  Google Scholar 

  • Martínez-Espinosa RM, Marhuenda-Egea FC, Bonete MJ (2001b) Purification and characterisation of a possible assimilatory nitrite reductase from the halophile archaeon Haloferax mediterranei. FEMS Microbiol Lett 196(2):113–118

    Article  PubMed  Google Scholar 

  • Martínez-Espinosa RM, Marhuenda-Egea FC, Donaire A, Bonete MJ (2003) NMR studies of a ferredoxin from Haloferax mediterranei and its physiological role in nitrate assimilatory pathway. Biochim Biophys Acta 1623(1):47–51

    Article  PubMed  Google Scholar 

  • Martínez-Espinosa RM, Esclapez J, Bautista V, Bonete MJ (2006) An octameric prokaryotic glutamine synthetase from the haloarchaeon Haloferax mediterranei. FEMS Microbiol Lett 264(1):110–116

    Article  PubMed  Google Scholar 

  • Martínez-Espinosa RM, Lledó B, Marhuenda-Egea FC, Bonete MJ (2007) The effect of ammonium on assimilatory nitrate reduction in the haloarchaeon Haloferax mediterranei. Extremophiles 11(6):759–767

    Article  PubMed  Google Scholar 

  • Martínez-Espinosa RM, Lledó B, Marhuenda-Egea FC, Díaz S, Bonete MJ (2009) NO3 /NO2 assimilation in halophilic archaea: physiological analysis, nasA and nasD expressions. Extremophiles 13:785–792

    Article  PubMed  Google Scholar 

  • McCarty GW, Bremner J (1992) Regulation of assimilatory nitrate reductase activity in soil by microbial assimilation of ammonium. Proc Natl Acad Sci USA 89:453–456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mehta BJ, Obraztsova IN, Cerda-Olmedo E (2003) Mutants and intersexual heterokaryons of Blakeslea trispora for production of beta-carotene and lycopene. Appl Environ Microbiol 69:4043–4048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miflin BJ (2002) The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops. J Exp Bot 53(370):979–987

    Article  CAS  PubMed  Google Scholar 

  • Miller A, Fan X, Shen Q, Smith SJ (2008) Amino acids and nitrate as signals for the regulation of nitrogen acquisition. J Exp Bot 59:111–119

    Article  CAS  PubMed  Google Scholar 

  • Moir W, Wood NJ (2001) Nitrate and nitrite transport in bacteria. Cell Mol Life Sci 58:215–224

    Article  CAS  PubMed  Google Scholar 

  • Moreno-Vivián C, Flores E (2007) Nitrate assimilation in Bacteria. In: Bothe H, Ferguson SF, Newton WE (eds) Biology of the nitrogen cycle. Elsevier BV, Amsterdam, pp 263–282

    Google Scholar 

  • Nesbo CL, L’Haridon S, Stetter KO, Doolittle WF (2001) Phylogenetic analyses of two ‘archaeal’ genes in thermotoga maritima reveal multiple transfers between archaea and bacteria. Mol Biol Evol 18(3):362–375

    Article  CAS  PubMed  Google Scholar 

  • Ninfa AJ, Jiang P (2005) PII signal transduction proteins: sensors of [alpha]-ketoglutarate that regulate nitrogen metabolism. Curr Opin Microbiol 8:168–173

    Article  CAS  PubMed  Google Scholar 

  • Olaizola M (2000) Commercial production of astaxanthin from Haematococcus pluvialis using 25,000-liter outdoor photobioreactors. J Appl Phycol 12:499–506

    Article  CAS  Google Scholar 

  • Palanca C, Pedro-Roig L, Llácer JL, Camacho M, Bonete MJ, Rubio V (2014) The structure of a PII signaling protein from a halophilic archaeon reveals novel traits and high-salt adaptations. FEBS J 281:3299–3314

    Article  CAS  PubMed  Google Scholar 

  • Palozza P, Maggiano N, Calviello G, Lanza P, Piccioni E, Ranelletti FO, Bartoli GM (1998) Canthaxanthin induces apoptosis in human cancer cell lines. Carcinogenesis 19:373–376

    Article  CAS  PubMed  Google Scholar 

  • Pantoja O (2012) High affinity ammonium transporters: molecular mechanism of action. Front Plant Sci 3:34. doi:10.3389/fpls.2012.00034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pedro-Roig L, Camacho M, Bonete MJ (2011) In vitro proof of direct regulation of glutamine synthetase by GlnK proteins in the extreme halophilic archaeon Haloferax mediterranei. Biochem Soc Trans 39:259–262

    Article  CAS  PubMed  Google Scholar 

  • Pedro-Roig L, Camacho M, Bonete MJ (2013a) Haloferax mediterranei GlnK proteins are post-translationally modified by uridylylation. Proteomics 13:1371–1374

    Article  CAS  PubMed  Google Scholar 

  • Pedro-Roig L, Camacho M, Bonete MJ (2013b) Regulation of ammonium assimilation in Haloferax mediterranei: Interaction between glutamine synthetase and two GlnK proteins. Biochim Biophys Acta 1834:16–23

    Article  CAS  PubMed  Google Scholar 

  • Pedro-Roig L, Lange C, Bonete MJ, Soppa J, Maupin-Furlow J (2013c) Nitrogen regulation of protein-protein interactions and transcript levels of GlnK PII regulator and AmtB ammonium transporter homologs in archaea. Microbiologyopen 2(5):826–840

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pérez-Pomares F, Ferrer J, Camacho M, Pire C, Llorca F, Bonete MJ (1999) Amino acid residues implied in the catalytic mechanism of NAD-dependent glutamate dehydrogenase from Halobacterium salinarum. Biochim Biophys Acta 1426:513–525

    Article  PubMed  Google Scholar 

  • Pire C, Martínez-Espinosa RM, Pérez-Pomares F, Esclapez J, Bonete MJ (2014) Ferredoxin-dependent glutamate synthase: involvement in ammonium assimilation in Haloferax mediterranei. Extremophiles 18(1):147–159

    Article  CAS  PubMed  Google Scholar 

  • Radin JW (1977) Amino acid interactions in the regulation of nitrate reductase induction in cotton root tips. Plant Physiol 60:467–469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raja R, Hemaiswarya S, Rengasamy R (2007) Exploitation of Dunaliella for betacarotene production. Appl Microbiol Biotechnol 74:517–523

    Article  CAS  PubMed  Google Scholar 

  • Reitzer L (2003) Nitrogen assimilation and global regulation in Escherichia coli. Annu Rev Microbiol 57:155–176

    Article  CAS  PubMed  Google Scholar 

  • Reyes JC, Florencio FJ (1994) A mutant lacking the glutamine synthetase gene (glnA) is impaired in the regulation of the nitrate assimilation system in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 176:7516–7523

    CAS  PubMed  PubMed Central  Google Scholar 

  • Richardson DJ, Berks BC, Russell DA, Spiro S, Taylor CJ (2001) Functional, biochemical and genetic diversity of prokaryotic nitrate reductases. Cell Mol Life Sci 58(2):165–178

    Article  CAS  PubMed  Google Scholar 

  • Robertson DL, Alberte RS (1996) Isolation and characterization of glutamine synthetase from the marine diatom Skeletonema costatum. Plant Physiol 111(4):1169–1175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santero E, Hervás AB, Canosa I, Govantes F (2012) Glutamate dehydrogenases: enzymology, physiological role and biotechnological relevance; Chapter 12. In: Canuto RA (ed) Dehydrogenases. InTech, under CC BY 3.0 license. doi:10.5772/2903. ISBN 978-953-307-019-3

    Google Scholar 

  • Schulz AA, Collett HJ, Reid SJ (2001) Nitrogen and carbon regulation of glutamine synthetase and glutamate synthase in Corynebacterium glutamicum ATCC 13032. FEMS Microbiol Lett 205(2):361–367

    Article  CAS  PubMed  Google Scholar 

  • Shapiro BM (1969) The glutamine synthetase deadenylylating enzyme system from Escherichia coli. Resolution into two components, specific nucleotide stimulation, and cofactor requirements. Biochemistry 8(2):659–670

    Article  CAS  PubMed  Google Scholar 

  • Smith EL, Austen BM, Blumenthal KM, Nyc JF (1975) Glutamate dehydrogenase. In: Boyer PD (ed) The enzymes, vol 11, 3rd edn. Academic Press, New York, pp 293–367

    Google Scholar 

  • Sugimori D, Ichimata T, Ikeda A, Nakamura S (2000) Purification and characterization of a ferredoxin from Haloarcula japonica strain TR-1. Biometals 13(1):23–28

    Article  CAS  PubMed  Google Scholar 

  • Tomita T, Miyazaki T, Miyazaki J, Kuzuyama T, Nishiyama M (2010) Hetero-oligomeric glutamate dehydrogenase from Thermus thermophilus. Microbiology 156:3801–3813

    Article  CAS  PubMed  Google Scholar 

  • Tomita T, Kuzuyama T, Nishiyama M (2011) Structural basis for leucine-induced allosteric activation of glutamate dehydrogenase. J Biol Chem 286:37406–37413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vanoni MA, Curti B (1999) Glutamate synthase: a complex iron-sulfur flavoprotein. Cell Mol Life Sci 55:617–638

    Article  CAS  PubMed  Google Scholar 

  • Vanoni MA, Curti B (2005) Structure and function studies on the ironsulfur flavoenzyme glutamate synthase: an unexpectedly complex self-regulated enzyme. Arch Biochem Biophys 433(1):193–211

    Article  CAS  PubMed  Google Scholar 

  • Wanner C, Soppa J (1999) Genetic Identification of three ABC transporters as essential elements for nitrate respiration in Haloferax volcanii. Genetics 152(4):1417–1428

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wood NJ, Alizadeh T, Richardson DJ, Ferguson SJ, Moir JW (2002) Two domains of a dual-function NarK protein are required for nitrate uptake, the first step of denitrification in Paracoccus pantotrophus. Mol Microbiol 44(1):157–170

    Article  CAS  PubMed  Google Scholar 

  • Zafrilla B, Martínez-Espinosa RM, Bonete MJ, Butt JN, Richardson DJ, Gates AJ (2011) A haloarchaeal ferredoxin electron donor that plays an essential role in nitrate assimilation. Biochem Soc Trans 39(6):1844–1848

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to María José Bonete .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Esclapez, J. et al. (2016). Recent Advances in the Nitrogen Metabolism in Haloarchaea and Its Biotechnological Applications. In: Rampelotto, P. (eds) Biotechnology of Extremophiles:. Grand Challenges in Biology and Biotechnology, vol 1. Springer, Cham. https://doi.org/10.1007/978-3-319-13521-2_9

Download citation

Publish with us

Policies and ethics