Skip to main content

Advertisement

SpringerLink
Log in

Transcriptome analysis of Rhodobacter capsulatus grown on different nitrogen sources

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

This study investigated the effect of different nitrogen sources, namely, ammonium chloride and glutamate, on photoheterotrophic metabolism of Rhodobacter capsulatus grown on acetate as the carbon source. Genes that were significantly differentially expressed according to Affymetrix microarray data were categorized into Clusters of Orthologous Groups functional categories and those in acetate assimilation, hydrogen production, and photosynthetic electron transport pathways were analyzed in detail. Genes related to hydrogen production metabolism were significantly downregulated in cultures grown on ammonium chloride when compared to those grown on glutamate. In contrast, photosynthetic electron transport and acetate assimilation pathway genes were upregulated. In detail, aceA encoding isocitrate lyase, a unique enzyme of the glyoxylate cycle and ccrA encoding the rate limiting crotonyl-CoA carboxylase/reductase enzyme of ethylmalonyl-coA pathway were significantly upregulated. Our findings indicate for the first time that R. capsulatus can operate both glyoxylate and ethylmalonyl-coA cycles for acetate assimilation.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adessi A, Concato M, Sanchini A, Rossi F, De Philippis R (2016) Hydrogen production under salt stress conditions by a freshwater Rhodopseudomonas palustris strain. Appl Microbiol Biotechnol 100:2917–2926

    Article  CAS  PubMed  Google Scholar 

  • Afşar N (2012) A global approach to the hydrogen production, carbon assimilation and nitrogen metabolism of Rhodobacter capsulatus by physiological and microarray analysis. Dissertation, Middle East Technical University

  • Akköse S, Gündüz U, Yücel M, Eroglu I (2009) Effects of ammonium ion, acetate and aerobic conditions on hydrogen production and expression levels of nitrogenase genes in Rhodobacter sphaeroides O.U.001. Int J Hydrog Energy 24:8818–8827

    Article  CAS  Google Scholar 

  • Alber BE (2011) Biotechnological potential of the ethylmalonyl-CoA pathway. Appl Microbial Biotechnol 89:17–25

    Article  CAS  Google Scholar 

  • Alber BE, Spanheimer R, Ebenau-Jehle C, Fuchs G (2006) Study of an alternate glyoxylate cycle for acetate assimilation by Rhodobacter sphaeroides. Mol Microbiol 61:297–309

    Article  CAS  PubMed  Google Scholar 

  • Albers H, Gottschalk G (1976) Acetate metabolism in Rhodopseudomonas gelatinosa and several other Rhodospirillaceae. Arch Microbiol 111:45–49

    Article  CAS  PubMed  Google Scholar 

  • Androga D, Özgür E, Eroglu I, Gündüz U, Yücel M (2011) Significance of carbon to nitrogen ratio on the long-term stability of continuous photofermentative hydrogen production. Int J Hydrog Energy 36:15583–15594

    Article  CAS  Google Scholar 

  • Basak N, Das D (2007) The prospect of purple non-sulfur (PNS) photosynthetic bacteria for hydrogen production: the present state of the art. World J Microbiol Biotechnol 23:31–42

    Article  CAS  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate—a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300

    Google Scholar 

  • Biebl H, Pfennig N (1981) Isolation of members of the family Rhodosprillaceae. In: Starr MP, Stolp H, Trüper HG, Balows A, Schlegel HG (eds) The prokaryotes, vol 1. Springer, New York, pp 267–273

    Chapter  Google Scholar 

  • Boran E, Özgür E, Van der Burg J, Yücel M, Gündüz U, Eroglu I (2010) Biological hydrogen production by Rhodobacter capsulatus in solar tubular photo bioreactor. J Clean Prod 18:29–35

    Article  CAS  Google Scholar 

  • Brandt U (2006) Energy converting NADH:quinone oxidoreductase (complex I). Annu Rev Biochem 75:69–92

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Dupuis A, Chevallet M, Darrouzet E, Duborjal H, Lunardi J, Issartel JP (1998) The complex I from Rhodobacter capsulatus. Biochim Biophys Acta 1364:147–165

    Article  CAS  PubMed  Google Scholar 

  • Erb TJ, Frerichs-Revermann L, Fuchs G, Alber BE (2010) The apparent malate synthase activity of Rhodobacter sphaeroides is due to two paralogous enzymes, (3S)-malyl-CoA/β -methylmalyl-CoA lyase and (3S)-malyl-CoA thioesteraseş. J Bacteriol 192:1249–1258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eroglu E, Melis A (2011) Photobiological hydrogen production: recent advances and state of the art. Bioresour Technol 102:8403–8413

    Article  CAS  PubMed  Google Scholar 

  • Golomysova A, Gomelsky M, Ivanov PS (2010) Flux balance analysis of photoheterotrophic growth of purple nonsulfur bacteria relevant to biohydrogen production. Int J Hydrog Energy 35:12751–12760

    Article  CAS  Google Scholar 

  • Gürgan M, Erkal AN, Özgür E, Gündüz U, Eroglu I, Yücel M (2015) Transcriptional profiling of hydrogen production metabolism of Rhodobacter capsulatus under temperature stress by microarray analysis. Int J Mol Sci 16(6):13781–13797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hadicke O, Grammel H, Klamt S (2011) Metabolic network modeling of redox balancing and biohydrogen production in purple nonsulfur bacteria. BMC Syst Biol 5:150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hallenbeck PC, Liu Y (2016) Recent advances in hydrogen production by photosynthetic bacteria. Int J Hydrog Energy 41:4446–4454

    Article  CAS  Google Scholar 

  • Herter SM, Kortluke CM, Drews G (1998) Complex I of Rhodobacter capsulatus and its role in reverted electron transport. Arch Microbiol 169:98–105

    Article  CAS  PubMed  Google Scholar 

  • Hoekema S, Douma RD, Janssen M, Tramper J, Wijffels RH (2006) Controlling light-use by Rhodobacter capsulatus continuous cultures in a flat-panel photobioreactor. Biotechnol Bioeng 95:613–626

    Article  CAS  PubMed  Google Scholar 

  • Imhoff JF (2006) The phototrophic alpha-proteobacteria. Prokaryotes 5:41–64

    Article  Google Scholar 

  • Keskin T, Abo-Hashesh M, Hallenbeck PC (2011) Photofermentative hydrogen production from wastes. Bioresour Technol 102:8557–8568

    Article  CAS  PubMed  Google Scholar 

  • Koku H, Eroglu I, Gunduz U, Yucel M, Turker L (2002) Aspects of the metabolism of hydrogen production by Rhodobacter sphaeroides. Int J Hydrog Energy 27:1315–1329

    Article  CAS  Google Scholar 

  • Kontur WS, Ziegelhoffer EC, Spero MA, Imam S, Noguera DR, Donohue TJ (2011) Pathways involved in reductant distribution during photobiological H2 production by Rhodobacter sphaeroides. Appl Environ Microbiol 77:7425–7429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kornberg HL, Krebs HA (1957) Synthesis of cell constituents from C2-units by a modified tricarboxylic acid cycle. Nature 179:988–991

    Article  CAS  PubMed  Google Scholar 

  • Kornberg HL, Lascelles J (1960) The formation of isocitratase by the athiorhodaceae. J Gen Microbiol 23:511–517

    Article  CAS  PubMed  Google Scholar 

  • Laguna R, Tabita FR, Alber BE (2011) Acetate-dependent photoheterotrophic growth and the differential requirement for the Calvin–Benson–Bassham reductive pentose phosphate cycle in Rhodobacter sphaeroides and Rhodopseudomonas palustris. Arch Microbiol 193:151–154

    Article  CAS  PubMed  Google Scholar 

  • Lanciano P, Lee DW, Yang H, Darrouzet E, Daldal F (2011) Intermonomer electron transfer between the low-potential b hemes of cytochrome bc1. Biochemistry 50:1651–1663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leroy B, De Meur Q, Moulin C, Wegria G, Wattiez R (2015) New insight into the photoheterotrophic growth of the isocytrate lyase-lacking purple bacterium Rhodospirillum rubrum on acetate. Microbiology 161:1061–1072

    Article  CAS  PubMed  Google Scholar 

  • Madigan MT, Jung DO (2009) An overview of purple bacteria: systematic, physiology and habitats. In: Hunter CD, Daldal F, Thurnauer MC, Beatty JT (eds) Advances in photosynthesis and respiration. The purple phototrophic bacteria, vol 28. Springer, Dordrecht, pp 1–15

    Chapter  Google Scholar 

  • Masepohl B, Hallenbeck PC (2010) Nitrogen and molybdenum control of nitrogen fixation in the phototrophic bacterium Rhodobacter capsulatus. In: Hallenbeck PC (ed) Recent Advances in phototrophic prokaryotes. Advances in experimental medicine and biology, vol 675. Springer, New York, pp 49–70

    Chapter  Google Scholar 

  • Masepohl B, Kranz RG (2009) Regulation of nitrogen fixation. In: Hunter CN, Daldal F, Thurnauer MC, Beatty JT (eds) The purple phototrophic bacteria. Springer, Dordrecht, pp 759–775

    Chapter  Google Scholar 

  • Masepohl B, Drepper T, Paschen SG, Pawlowski A, Riedel K, Klipp W (2002) Regulation of nitrogen fixation in the phototrophic purple bacterium Rhodobacter capsulatus. J Mol Microbiol Biotechnol 4:243–248

    CAS  PubMed  Google Scholar 

  • Masepohl B, Drepper T, Klipp W (2004) Nitrogen fixation in the phototrophic purple bacterium Rhodobacter capsulatus. In: Klipp W, Masepohl B, Gallon JR, Newton WE (eds) Genetics and regulation of nitrogen fixation in free-living bacteria. Kluwer Academic Publisher, Dordrecht, pp 141–173

    Google Scholar 

  • McEwan AG (1994) Photosynthetic electron transport and anaerobic metabolism in purple non-sulfur photosynthetic bacteria. Antonie Leeuwenhoek 66:151–164

    Article  CAS  PubMed  Google Scholar 

  • McKinlay JB, Harwood CS (2010) Photobiological production of hydrogen gas as a biofuel. Curr Opin Biotechnol 21:244–251

    Article  CAS  PubMed  Google Scholar 

  • Meister M, Saum S, Alber BE, Fuchs G (2005) L-Malyl-coenzyme A/β- methylmalyl-coenzyme A lyase is involved in acetate assimilation of the isocitrate lyase-negative bacterium Rhodobacter capsulatus. J Bacteriol 187:1415–1425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Melis A, Melnicki M (2006) Integrated biological hydrogen production. Int J Hydrog Energy 31:1563–1573

    Article  CAS  Google Scholar 

  • Özgür E, Uyar B, Öztürk Y, Yücel M, Gündüz U, Eroglu I (2010) Biohydrogen production by R. capsulatus on acetate at fluctuating temperatures. Resour Conserv Recycl 54:310–314

    Article  Google Scholar 

  • Öztürk Y, Yücel M, Daldal F, Mandacı S, Gündüz U, Türker L, Eroğlu E (2006) Hydrogen production by using Rhodobacter capsulatus mutants with genetically modified electron transfer chains. Int J Hydrog Energy 31:1545–1552

    Article  Google Scholar 

  • Redwood MD, Paterson-Beedle M, Macaskie LE (2009) Integrating dark and light bio-hydrogen production strategies: towards the hydrogen economy. Rev Environ Sci Bio/Technol 8:149–185

    Article  CAS  Google Scholar 

  • Sağır E, Yucel M, Hallenbeck PC (2018) Demonstration and optimization of sequential microaerobic dark- and photo-fermentation biohydrogen production by immobilized Rhodobacter capsulatus JP91. Bioresour Technol 250:43–52

    Article  CAS  PubMed  Google Scholar 

  • Selao TT, Nordlund S, Noren A (2008) Comparative proteomic studies in Rhodospirillum rubum grown under different nitrogen conditions. J Proteome 7:3267–3275

    Article  CAS  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 8:659–670

    Article  CAS  PubMed  Google Scholar 

  • Smyth GK (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3(1):1–25

    Article  Google Scholar 

  • Strnad H, Lapidus A, Paces J, Ulbrich P, Vlcek C, Paces V, Haselkorn R (2010) Complete genome sequence of the photosynthetic purple nonsulfur bacterium Rhodobacter capsulatus SB 1003. J Bacteriol 192:3545–3546

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uyar B, Eroglu I, Yücel M, Gündüz U, Türker L (2007) Effect of light intensity, wavelength and illumination protocol on hydrogen production in photobioreactors. Int J Hydrog Energy 32:4670–4677

    Article  CAS  Google Scholar 

  • Uyar B, Kars G, Eroglu I, Yücel M, Gündüz U (2012) Hydrogen production via photofermentation. In: Levin D, Azbar N (eds) State of the art and progress in production of biohydrogen. Bentham Science Publishers, Danvers, pp 54–77

    Chapter  Google Scholar 

  • Willison JC (1988) Pyruvate and acetate metabolism in the photosynthetic bacterium Rhodobacter capsulatus. J Gen Microbiol 134:2429–2439

    CAS  Google Scholar 

  • Zarzycki J, Schlichting A, Strychalsky N, Müller M, Alber BE, Fuchs G (2008) Mesaconyl-coenzyme A hydratase, a new enzyme of two central carbon metabolic pathways in bacteria. J Bacteriol 190:1366–1374

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The raw microarray data used in this article were obtained using custom-designed Affymetrix GeneChip® (TR_RCH2a520699F) and derived from the PhD work of Nilufer Afsar Erkal ‘A global approach to the hydrogen production, carbon assimilation and nitrogen metabolism of Rhodobacter capsulatus by physiological and microarray analysis’ (Dissertation, Middle East Technical University). This research was supported by TUBITAK 1001 Project 108T455 and the EU 6th Framework Integrated Project 019825 (HYVOLUTION). Microarray experiments were carried out at METU Central Laboratory, Molecular Biology and Biotechnology R&D Center (Ankara, Turkey).

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Middle East Technical University, 06800, Ankara, Turkey

    Nilüfer Afsar Erkal, Ufuk Gündüz & Meral Yücel

  2. Mikro Biyositemler Inc, 06530, Ankara, Turkey

    Nilüfer Afsar Erkal & Ebru Özgür

  3. Department of Biology, Namık Kemal University, 59030, Tekirdağ, Turkey

    Muazzez Gürgan Eser

  4. Department of Chemical Engineering, Middle East Technical University, 06800, Ankara, Turkey

    Ebru Özgür & Inci Eroglu

Authors
  1. Nilüfer Afsar Erkal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Muazzez Gürgan Eser
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ebru Özgür
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ufuk Gündüz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Inci Eroglu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Meral Yücel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Meral Yücel.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Shuang-Jiang Liu.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 30 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Erkal, N.A., Eser, M.G., Özgür, E. et al. Transcriptome analysis of Rhodobacter capsulatus grown on different nitrogen sources. Arch Microbiol 201, 661–671 (2019). https://doi.org/10.1007/s00203-019-01635-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-019-01635-x

Keywords

Search

Navigation