Skip to main content

Advertisement

SpringerLink
Log in

Upregulation of Hox-hydrogenase gene expression by nutrient adjustment in the filamentous non-heterocystous cyanobacterium Arthrospira sp. PCC 8005

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Arthrospira sp. PCC 8005 is potentially able to produce hydrogen catalysed by hox gene–encoded bidirectional hydrogenase with the aid of hyp gene–encoded accessory proteins. In the present study, we investigated the physiological factors affecting the hoxE, hoxY, hoxH, and hypF transcription in Arthrospira sp. PCC 8005. About a 4-fold increase of biomass and chlorophyll-a content was observed in cells grown for 7 days in Zarrouk’s medium supplemented with Fe2+. Cells grown in N-deprived medium with added Ni2+ had increased H2 production and hydrogenase activity with a maximal value of 7.24 ± 0.25 μmol H2 mg−1 Chla h−1 and 0.61 ± 0.03 μmol H2 mg−1 Chla h−1, respectively. RT-PCR analysis revealed that cells grown in the N-deprived medium supplemented with Fe2+ or Ni2+ increased hoxE, hoxY, and hoxH transcripts. However, the highest increase of the hoxE, hoxY, hoxH, and hypF transcripts was observed in cells grown in the S-deprived medium supplemented with a combination of Fe2+ and β-mercaptoethanol. These results indicated that the increased expression of hox genes in Arthrospira sp. PCC 8005 can be achieved by proper adjustment of the nutrients in the growth medium. Phylogenetic analysis revealed that the small hydrogenase subunit, HoxY sequence, from Arthrospira sp. PCC 8005 was clustered together along with other cyanobacterial HoxY which is highly related to Arthrospira platensis NIES46.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Agervald Å, Stensjö K, Holmqvist M, Lindblad P (2008) Transcription of the extended hyp-operon in Nostoc sp. strain PCC 7120. BMC Microbiol 8:69

    PubMed  PubMed Central  Google Scholar 

  • Ainas M, Hasnaoui S, Bouarab R, Abdi N, Drouiche N, Mameri N (2017) Hydrogen production with the cyanobacterium Spirulina platensis. Int J Hydrogen Energy 42:4902–4907

    CAS  Google Scholar 

  • Antal TK, Lindblad P (2005) Production of H2 by sulphur-deprived cells of the unicellular cyanobacteria Gloeocapsa alpicola and Synechocystis sp. PCC 6803 during dark incubation with methane or at various extracellular pH. J Appl Microbiol 98:114–120

    CAS  PubMed  Google Scholar 

  • Antal TK, Oliveira P, Lindblad P (2006) The bidirectional hydrogenase in the cyanobacterium Synechocystis sp. strain PCC 6803. Int J Hydrogen Energy 31:1439–1444

    CAS  Google Scholar 

  • Axelsson R, Lindblad P (2002) Transcriptional regulation of Nostoc hydrogenases: effects of oxygen, hydrogen, and nickel. Appl Environ Microbiol 68:444–447

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baebprasert W, Lindblad P, Incharoensakdi A (2010) Response of H2 production and Hox-hydrogenase activity to external factors in the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. Int J Hydrogen Energy 35:6611–6616

    CAS  Google Scholar 

  • Barz M, Beimgraben C, Staller T, Germer F, Opitz F, Marquardt C, Schwarz C, Gutekunst K, Vanselow KH, Schmitz R, LaRoche J, Schulz R, Appel J (2010) Distribution analysis of hydrogenases in surface waters of marine and freshwater environments. PLoS One 5:e13846

    PubMed  PubMed Central  Google Scholar 

  • Beimgraben C, Gutekunst K, Opitz F, Appel J (2014) HypD as a marker for [NiFe]-hydrogenases in microbial communities of surface waters. Appl Environ Microbiol 80:3776–3782

    PubMed  PubMed Central  Google Scholar 

  • Böck A, King PW, Blokesch M, Posewitz MC (2006) Maturation of hydrogenases. Adv Microb Physiol 51:1–71

    PubMed  Google Scholar 

  • Boison G, Bothe H, Schmitz O (2000) Transcriptional analysis of hydrogenase genes in the cyanobacteria Anacystis nidulans and Anabaena variabilis monitored by RT-PCR. Curr Microbiol 40:315–321

    CAS  PubMed  Google Scholar 

  • Bolatkhan K, Kossalbayev BD, Zayadan BK, Tomo T, Veziroglu TN, Allakhverdiev SI (2019) Hydrogen production from phototrophic microorganisms: reality and perspectives. Int J Hydrogen Energy 44:5799–5811

    CAS  Google Scholar 

  • Burow LC, Woebken D, Bebout BM, McMurdie PJ, Singer SW, Pett-Ridge J, Prufert-Bebout L, Spormann AM, Weber PK, Hoehler TM (2012) Hydrogen production in photosynthetic microbial mats in the Elkhorn Slough estuary, Monterey Bay. ISME J 6:863–874

    CAS  PubMed  Google Scholar 

  • Carrieri D, Ananyev G, Dismukes GC (2008) Renewable hydrogen production by cyanobacteria: nickel requirements for optimal hydrogenase activity. Int J Hydrogen Energy 33:2014–2022

    CAS  Google Scholar 

  • Chang Y, Wu Z, Bian L, Feng D, Leung DYC (2013) Cultivation of Spirulina platensis for biomass production and nutrient removal from synthetic human urine. Appl Energ 102:427–431

    CAS  Google Scholar 

  • Facey JA, Apte SC, Mitrovic SM (2019) A review of the effect of trace metals on freshwater cyanobacterial growth and toxin production. Toxins 11:643

    CAS  PubMed Central  Google Scholar 

  • Ferreira D, Leitão E, Sjöholm J, Oliveira P, Lindblad P, Moradas-Ferreira P, Tamagnini P (2007) Transcription and regulation of the hydrogenase(s) accessory genes, hypFCDEAB, in the cyanobacterium Lyngbya majuscula CCAP 1446/4. Arch Microbiol 188:609–617

    CAS  PubMed  Google Scholar 

  • Ferreira D, Pinto F, Moradas-Ferreira P, Mendes MV, Tamagnini P (2009) Transcription profiles of hydrogenases related genes in the cyanobacterium Lyngbya majuscula CCAP 1446/4. BMC Microbiol 9:67

    PubMed  PubMed Central  Google Scholar 

  • Guindon S, Delsuc F, Dufayard J-F, Gascuel O (2009) Estimating maximum likelihood phylogenies with PhyML. Methods Mol Biol 537:113–137

    CAS  PubMed  Google Scholar 

  • Gutekunst K, Chen X, Schreiber K, Kaspar U, Makam S, Appel J (2014) The bidirectional NiFe-hydrogenase in Synechocystis sp. PCC 6803 is reduced by flavodoxin and ferredoxin and is essential under mixotrophic, nitrate-limiting conditions. J Biolumin Chemilumin 289:1930–1937

    CAS  Google Scholar 

  • Gutekunst K, Hoffmann D, Lommer M, Egert M, Suzuki I, Schulz-Friedrich R, Appel J (2006) Metal dependence and intracellular regulation of the bidirectional NiFe-hydrogenase in Synechocystis sp. PCC 6803. Int J Hydrogen Energy 3:1452–1459

    Google Scholar 

  • Gutthann F, Egert M, Marques A, Appel J (2007) Inhibition of respiration and nitrate assimilation enhances photohydrogen evolution under low oxygen concentrations in Synechocystis sp. PCC 6803. Biochim Biophys Acta 1767:161–169

    CAS  PubMed  Google Scholar 

  • Hoffmann D, Gutekunst K, Klissenbauer M, Schluz-Friedrich R, Appel J (2006) Mutagenesis of hydrogenase accessory genes of Synechocystis sp. PCC 6803. Additional homologues of hypA and hypB are not active in hydrogenase maturation. FEBS J 273:4516–4527

    CAS  PubMed  Google Scholar 

  • Hoffmann D, Maldonado J, Wojciechowski MF, Garcia-Pichel F (2015) Hydrogen export from intertidal cyanobacterial mats: sources, fluxes and the influence of community composition. Environ Microbiol 17:3738–3753

    CAS  PubMed  Google Scholar 

  • Holmqvist M, Lindberg P, Agervald Å, Stensjö K, Lindblad P (2011) Transcript analysis of the extended hyp-operon in the cyanobacteria Nostoc sp. strain PCC 7120 and Nostoc punctiforme ATCC 29133. BMC Res Notes 4:186

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ismaiel MMS, El-Ayouty YM, Loewen PC, Piercey-Normore MD (2014) Characterization of the iron-containing superoxide dismutase and its response to stress in cyanobacterium Spirulina (Arthrospira) platensis. J Appl Phycol 26:1649–1658

    CAS  Google Scholar 

  • Janssen PJ, Morin N, Mergeay M, Leroy B, Wattiez R, Vallaeys T, Waleron K, Waleron M, Wilmotte A, Quillardet P, Tandeau De Marsac N, Talla E, Zhang CC, Leys N (2010) Genome sequence of the edible cyanobacterium Arthrospira sp. PCC 8005. J Bacteriol 192:2465–2466

    CAS  PubMed  PubMed Central  Google Scholar 

  • Khetkorn W, Khanna N, Incharoensakdi A, Lindblad P (2013) Metabolic and genetic engineering of cyanobacteria for enhanced hydrogen production. Biofuels 4:535–561

    CAS  Google Scholar 

  • Kiss E, Kós PB, Vass I (2009) Transcriptional regulation of the bidirectional hydrogenase in the cyanobacterium Synechocystis 6803. J Biotechnol 142:31–37

    CAS  PubMed  Google Scholar 

  • Maneeruttanarungroj C, Lindblad P, Incharoensakdi A (2010) A newly isolated green alga, Tetraspora sp. CU2551, from Thailand with efficient hydrogen production. Int J Hydrogen Energy 35:13193–13199

    CAS  Google Scholar 

  • Marques AE, Barbosa AT, Jotta J, Coelho MC, Tamagnini P, Gouveia L (2011) Biohydrogen production by Anabaena sp. PCC 7120 wild-type and mutants under different conditions: light, nickel, propane, carbon dioxide and nitrogen. Biomass Bioenergy 35:4426–4434

    CAS  Google Scholar 

  • Márquez-Reyes LA, Sánchez-Saavedra MDP, Valdez-Vazquez I (2015) Improvement of hydrogen production by reduction of the photosynthetic oxygen in microalgae cultures of Chlamydomonas gloeopara and Scenedesmus obliquus. Int J Hydrogen Energy 40:7291–7300

    Google Scholar 

  • Melis A, Zhang L, Forestier M, Ghirardi ML, Seibert M (2000) Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii. Plant Physiol 122:127–135

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nagy V, Vidal-Meireles A, Podmaniczki A, Szentmihályi K, Rákhely G, Zsigmond L, Kovács L, Tóth SZ (2018) The mechanism of photosystem-II inactivation during sulphur deprivation-induced H2 production in Chlamydomonas reinhardtii. Plant J 94:548–561

    CAS  PubMed  Google Scholar 

  • Oliveira P, Lindblad P (2009) Transcriptional regulation of the cyanobacterial bidirectional Hox-hydrogenase. Dalton Trans 45:9990–9996

    Google Scholar 

  • Puggioni V, Tempel S, Latifi A (2016) Distribution of hydrogenases in cyanobacteria: a phylum-wide genomic survey. Front Genet 7:223

    PubMed  PubMed Central  Google Scholar 

  • Quintana N, Van der Kooy F, Van de Rhee MD, Voshol GP, Verpoorte R (2011) Renewable energy from cyanobacteria: energy production optimization by metabolic pathway engineering. Appl Microbiol Biotechnol 91:471–490

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raksajit W, Satchasataporn K, Lehto K, Mäenpää P, Incharoensakdi A (2012) Enhancement of hydrogen production by the filamentous non-heterocystous cyanobacterium Arthrospira sp. PCC8005. Int J Hydrogen Energy 37:8791–18797

    Google Scholar 

  • Rout NP, Khandual S, Gutierrez-Mora A, Ibarra-Montoya JL, Vega-Valero G (2015) Divergence in three newly identified Arthrospira species from Mexico. World J Microbiol Biotechnol 31:1157–1165

    PubMed  Google Scholar 

  • Sakurai H, Masukawa H, Kitashima M, Inoue K (2013) Photobiological hydrogen production: bioenergetics and challenges for its practical application. J Photochem Photobiol, C 17:1–25

    CAS  Google Scholar 

  • Sánchez-Bayo A, Morales V, Rodríguez R, Vicente G, Bautista LF (2020) Cultivation of microalgae and cyanobacteria: effect of operating conditions on growth and biomass composition. Molecules 25:2834

    PubMed Central  Google Scholar 

  • Schmitz O, Boison G, Salzmann H, Bothe H, Schütz K, Wang S-H, Happe T (2002) HoxE-a subunit specific for the pentameric bidirectional hydrogenase complex (HoxEFUYH) of cyanobacteria. Biochim Biophys Acta, Bioenerg 1554:66–74

    CAS  Google Scholar 

  • Sheremetieva ME, Troshina OY, Serebryakova LT, Lindblad P (2002) Identification of hox genes and analysis of their transcription in the unicellular cyanobacterium Gloeocapsa alpicola CALU 743 growing under nitrate-limiting conditions. FEMS Microbiol Lett 214:229–233

    CAS  PubMed  Google Scholar 

  • Shomura Y, Higuchi Y (2012) Structural basis for the reaction mechanism of S-carbamoylation of HypE by HypF in the maturation of [NiFe]-hydrogenases. J Biolumin Chemilumin 287:28409–28419

    CAS  Google Scholar 

  • Sjöholm J, Oliveira P, Lindblad P (2007) Transcription and regulation of the bidirectional hydrogenase in the cyanobacterium Nostoc sp. strain PCC 7120. Appl Environ Microbiol 73:5435–5446

    PubMed  PubMed Central  Google Scholar 

  • Sukrachan T, Incharoensakdi A (2020) Enhanced hydrogen production by Nostoc sp. CU2561 immobilized in a novel agar bead. J Appl Phycol 32:1103–1115

    CAS  Google Scholar 

  • Taikhao S, Junyapoon S, Incharoensakdi A, Phunpruch S (2013) Factors affecting biohydrogen production by unicellular halotolerant cyanobacterium Aphanothece halophytica. J Appl Phycol 25:575–585

    CAS  Google Scholar 

  • Taikhao S, Phunpruch S (2017) Effect of metal cofactors of key enzymes on biohydrogen production by nitrogen fixing cyanobacterium Anabaena siamensis TISIR 8012. Energy Procedia 138:360–365

    CAS  Google Scholar 

  • Tamagnini P, Leitao E, Oliveira P, Ferreira D, Pinto F, Harris DJ, Heidorn T, Lindblad P (2007) Cyanobacterial hydrogenase: diversity, regulation and applications. FEMS Microbiol Rev 31:692–720

    CAS  PubMed  Google Scholar 

  • Xu T, Qin S, Hu Y, Song Z, Ying J, Li P, Dong W, Zhao F, Yang H, Bao Q (2016) Whole genomic DNA sequencing and comparative genomic analysis of Arthrospira platensis: high genome plasticity and genetic diversity. DNA Res 23:325–338

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Zhang X, Shiraiwa Y, Mao Y, Sui Z, Liu J (2005) Cloning and characterization of hoxH genes from Arthrospira and Spirulina and application in phylogenetic study. Mar Biotechnol 7:287–296

    CAS  Google Scholar 

  • Zhang Z, Pendse ND, Phillips KN, Cotner JB, Khodursky A (2008) Gene expression patterns of sulfur starvation in Synechocystis sp. PCC 6803. BMC Genomics 9:344

    PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by the Kasetsart University Research and Development Institute (KURDI) (M-W9.53) to W. Raksajit, the Thailand Research Fund and Commission on Higher Education (TRF-CHE) (MRG5300825), the Chulalongkorn University Ratchadaphiseksomphot Endowment Fund (IRG 5780008) to A. Incharoensakdi, and the Erasmus+ International Credit Mobility fellowship to W. Raksajit and P. Mäenpää.

Author information

Authors and Affiliations

  1. Department of Veterinary Technology, Faculty of Veterinary Technology, Kasetsart University, Bangkok, 10900, Thailand

    Wuttinun Raksajit

  2. Department of Biology, Faculty of Science, King Mongkut’s Institute of Technology Ladkrabang, Ladkrabang, Bangkok, 10520, Thailand

    Cherdsak Maneeruttanarungroj

  3. Department of Biochemistry, Faculty of Science and Engineering, University of Turku, FI20014, Turku, Finland

    Pirkko Mäenpää & Kirsi Lehto

  4. Department of Biochemistry, Laboratory of Cyanobacterial Biotechnology, Faculty of Science, Chulalongkorn University, Bangkok, 10330, Thailand

    Aran Incharoensakdi

  5. Academy of Science, Royal Society of Thailand, Bangkok, 10300, Thailand

    Aran Incharoensakdi

Authors
  1. Wuttinun Raksajit
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cherdsak Maneeruttanarungroj
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pirkko Mäenpää
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kirsi Lehto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Aran Incharoensakdi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aran Incharoensakdi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Raksajit, W., Maneeruttanarungroj, C., Mäenpää, P. et al. Upregulation of Hox-hydrogenase gene expression by nutrient adjustment in the filamentous non-heterocystous cyanobacterium Arthrospira sp. PCC 8005. J Appl Phycol 32, 3799–3807 (2020). https://doi.org/10.1007/s10811-020-02217-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-020-02217-x

Keywords

Search

Navigation