Skip to main content
SpringerLink
Log in

The FX iron–sulfur cluster serves as the terminal bound electron acceptor in heliobacterial reaction centers

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Phototrophs of the family Heliobacteriaceae contain the simplest known Type I reaction center (RC), consisting of a homodimeric (PshA)2 core devoid of bound cytochromes and antenna proteins. Unlike plant and cyanobacterial Photosystem I in which the FA/FB protein, PsaC, is tightly bound to P700–FX cores, the RCs of Heliobacterium modesticaldum contain two FA/FB proteins, PshBI and PshBII, which are loosely bound to P800–FX cores. These two 2[4Fe–4S] ferredoxins have been proposed to function as mobile redox proteins, reducing downstream metabolic partners much in the same manner as does [2Fe–2S] ferredoxin or flavodoxin (Fld) in PS I. Using P800–FX cores devoid of PshBI and PshBII, we show that iron–sulfur cluster FX directly reduces Fld without the involvement of FA or FB (Fld is used as a proxy for soluble redox proteins even though a gene encoding Fld is not identified in the H. modesticaldum genome). The reduction of Fld is suppressed by the addition of PshBI or PshBII, an effect explained by competition for the electron on FX. In contrast, P700–FX cores require the presence of the PsaC, and hence, the FA/FB clusters for Fld (or ferredoxin) reduction. Thus, in H. modesticaldum, the interpolypeptide FX cluster serves as the terminal bound electron acceptor. This finding implies that the homodimeric (PshA)2 cores should be capable of donating electrons to a wide variety of yet-to-be characterized soluble redox partners.

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

Similar content being viewed by others

References

  • Amesz J (1995) The heliobacteria, a new group of photosynthetic bacteria. J Photochem Photobiol B 30(2–3):89–96

    Article  CAS  Google Scholar 

  • Azai C, Tsukatani Y, Itoh S, Oh-oka H (2010) C-type cytochromes in the photosynthetic electron transfer pathways in green sulfur bacteria and heliobacteria. Photosynth Res 104:189–199

    Article  PubMed  CAS  Google Scholar 

  • Brettel K, Leibl W, Liebl U (1998) Electron transfer in the heliobacterial reaction center: evidence against a quinone-type electron acceptor functioning analogous to A1 in photosystem I. Biochim Biophys Acta 1363(3):175–181

    Article  PubMed  CAS  Google Scholar 

  • Brockmann H, Lipinski A (1983) Bacteriochlorophyll-g a new bacteriochlorophyll from Heliobacterium chlorum. Arch Microbiol 136(1):17–19

    Article  CAS  Google Scholar 

  • Fillat MF, Sandmann G, Gomez-Moreno C (1988) Flavodoxin from the nitrogen-fixing cyanobacterium Anabaena PCC 7119. Arch Microbiol 150:160–164

    Article  CAS  Google Scholar 

  • Gest H, Favinger JL (1983) Heliobacterium chlorum, an anoxygenic brownish-green photosynthetic bacterium containing a new form of bacteriochlorophyll. Arch Microbiol 136(1):11–16

    Article  CAS  Google Scholar 

  • Heinnickel M, Golbeck JH (2007) Heliobacterial photosynthesis. Photosynth Res 92(1):35–53

    Article  PubMed  CAS  Google Scholar 

  • Heinnickel M, Shen G, Agalarov R, Golbeck JH (2005) Resolution and reconstitution of a bound Fe–S protein from the photosynthetic reaction center of Heliobacterium modesticaldum. Biochemistry 44(29):9950–9960

    Article  PubMed  CAS  Google Scholar 

  • Heinnickel M, Agalarov R, Svensen N, Krebs C, Golbeck JH (2006) Identification of FX in the heliobacterial reaction center as a [4Fe–4S] cluster with an S = 3/2 ground spin state. Biochemistry 45(21):6756–6764

    Article  PubMed  CAS  Google Scholar 

  • Heinnickel M, Shen G, Golbeck JH (2007) Identification and characterization of PshB, the dicluster ferredoxin that harbors the terminal electron acceptors FA and FB in Heliobacterium modesticaldum. Biochemistry 46(9):2530–2536

    Article  PubMed  CAS  Google Scholar 

  • Jagannathan B, Golbeck JH (2008) Unifying principles in homodimeric type I photosynthetic reaction centers: properties of PscB and the FA, FB and FX iron–sulfur clusters in green sulfur bacteria. Biochim Biophys Acta 1777(12):1535–1544

    Article  PubMed  CAS  Google Scholar 

  • Jagannathan B, Shen G, Golbeck J (2011) Evolution of Photosystem I. In: Burnap R, Vermaas W (eds) Functional genomics and evolution of photosynthetic systems. Springer, Dordrecht

    Google Scholar 

  • Kleinherenbrink FA, Amesz J (1993) Stoichiometries and rates of electron transfer and charge recombination in Heliobacterium chlorum. Biochem Biophys Acta 1143:77–83

    Article  CAS  Google Scholar 

  • Kleinherenbrink FA, Ikegami I, Hirashi A, Otte SCM, Amesz J (1993) Electron transfer in menaquinone-depleted membranes of Heliobacterium chlorum. Biochem Biophys Acta 1142:69–73

    Article  CAS  Google Scholar 

  • Kleinherenbrink FA, Chiou HC, LoBrutto R, Blankenship RE (1994) Spectroscopic evidence for the presence of an iron–sulfur center similar to Fx of Photosystem I in Heliobacillus mobilis. Photosynth Res 41(1):115–123

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi M, van de Meent EJ, Erkelens C, Amesz J, Ikegami I, Watanabe T (1991) Bacteriochlorophyll g epimer as a possible reaction center component of heliobacteria. Biochem Biophys Acta 1057:89–96

    Article  CAS  Google Scholar 

  • Liebl U, Mockensturmwilson M, Trost JT, Brune DC, Blankenship RE, Vermaas W (1993) Single core polypeptide in the reaction center of the photosynthetic bacterium Heliobacillus mobilis—structural implications and relations to other photosystems. Proc Natl Acad Sci USA 90(15):7124–7128

    Article  PubMed  CAS  Google Scholar 

  • Lin S, Chiou HC, Kleinherenbrink FA, Blankenship RE (1994) Time-resolved spectroscopy of energy and electron transfer processes in the photosynthetic bacterium Heliobacillus mobilis. Biophys J 66(2 Pt 1):437–445

    Article  PubMed  CAS  Google Scholar 

  • Medina M, Hervas M, Navarro JA, De la Rosa MA, Gomez-Moreno C, Tollin G (1992) A laser flash absorption spectroscopy study of Anabaena sp. PCC 7119 flavodoxin photoreduction by photosystem I particles from spinach. FEBS Lett 313(3):239–242

    Article  PubMed  CAS  Google Scholar 

  • Meimberg K, Muhlenhoff U (1999) Laser-flash absorption spectroscopy study of the competition between ferredoxin and flavodoxin photoreduction by Photosystem I in Synechococcus sp. PCC 7002: evidence for a strong preference for ferredoxin. Photosynth Res 61:253–2677

    Article  CAS  Google Scholar 

  • Meimberg K, Fischer N, Rochaix JD, Muhlenhoff U (1999) Lys35 of PsaC is required for the efficient photoreduction of flavodoxin by photosystem I from Chlamydomonas reinhardtii. Eur J Biochem 263(1):137–144

    Article  PubMed  CAS  Google Scholar 

  • Miyamoto R, Iwaki M, Mino H, Harada J, Itoh S, Oh-Oka H (2006) ESR signal of the iron–sulfur center FX and its function in the homodimeric reaction center of Heliobacterium modesticaldum. Biochemistry 45(20):6306–6316

    Article  PubMed  CAS  Google Scholar 

  • Miyamoto R, Mino H, Kondo T, Itoh S, Oh-Oka H (2008) An electron spin-polarized signal of the P800+ A1(Q)− state in the homodimeric reaction center core complex of Heliobacterium modesticaldum. Biochemistry 47(15):4386–4393

    Article  PubMed  CAS  Google Scholar 

  • Muh F, Glockner C, Hellmich J, Zouni A (2012) Light-induced quinone reduction in photosystem II. Biochim Biophys Acta 1817(1):44–65

    Article  PubMed  Google Scholar 

  • Muhiuddin IP, Rigby SE, Evans MC, Amesz J, Heathcote P (1999) ENDOR and special TRIPLE resonance spectroscopy of photoaccumulated semiquinone electron acceptors in the reaction centers of green sulfur bacteria and heliobacteria. Biochemistry 38(22):7159–7167

    Article  PubMed  CAS  Google Scholar 

  • Naver H, Scott MP, Golbeck JH, Olsen CE, Scheller HV (1998) The eight-amino acid internal loop of PSI-C mediates association of low molecular mass iron–sulfur proteins with the P700–FX core in photosystem I. J Biol Chem 273(30):18778–18783

    Article  PubMed  CAS  Google Scholar 

  • Neerken S, Amesz J (2001) The antenna reaction center complex of heliobacteria: composition, energy conversion and electron transfer. Biochim Biophys Acta 1507(1–3):278–290

    PubMed  CAS  Google Scholar 

  • Nitschke W, Setif P, Liebl U, Feiler U, Rutherford AW (1990) Reaction center photochemistry of Heliobacterium chlorum. Biochemistry 29(50):11079–11088

    Article  PubMed  CAS  Google Scholar 

  • Nuijs AM, van Dorssen RJ, Duysens LNM, Amesz J (1985) Excited states and primary photochemical reactions in the photosynthetic bacterium Heliobacerium chlorum. Proc Natl Acad Sci USA 82:6865–6868

    Article  PubMed  CAS  Google Scholar 

  • Oh-oka H (2007) Type 1 reaction center of photosynthetic heliobacteria. Photochem Photobiol 83(1):177–186

    Article  PubMed  CAS  Google Scholar 

  • Romberger SP, Golbeck JH (2010) The bound iron–sulfur clusters of type-I homodimeric reaction centers. Photosynth Res 104(2–3):333–346

    Article  PubMed  CAS  Google Scholar 

  • Romberger SP, Castro C, Sun Y, Golbeck JH (2010) Identification and characterization of PshBII, a second FA/FB-containing polypeptide in the photosynthetic reaction center of Heliobacterium modesticaldum. Photosynth Res 104(2–3):293–303

    Article  PubMed  CAS  Google Scholar 

  • Sattley WM, Madigan MT, Swingley WD, Cheung PC, Clocksin KM, Conrad AL, Dejesa LC, Honchak BM, Jung DO, Karbach LE, Kurdoglu A, Lahiri S, Mastrian SD, Page LE, Taylor HL, Wang ZT, Raymond J, Chen M, Blankenship RE, Touchman JW (2008) The genome of Heliobacterium modesticaldum, a phototrophic representative of the Firmicutes containing the simplest photosynthetic apparatus. J Bacteriol 190(13):4687–4696

    Article  PubMed  CAS  Google Scholar 

  • Stevenson AK, Kimble LK, Woese CR, Madigan MT (1997) Characterization of new phototrophic heliobacteria and their habitats. Photosynth Res 53:1–12

    Article  CAS  Google Scholar 

  • Trost JT, Blankenship RE (1989) Isolation of a photoactive photosynthetic reaction center-core antenna complex from Heliobacillus mobilis. Biochemistry 28(26):9898–9904

    Article  PubMed  CAS  Google Scholar 

  • van de Meent EJ, Kobayashi M, Erkelens C, van Veelen PA, Amesz J, Watanabe T (1991) Identification of 8-hydroxychlorophyll a as a function reaction center pigment in heliobacteria. Biochem Biophys Acta 1058:356–362

    Article  Google Scholar 

  • van der Est A, Hager-Braun C, Leibl W, Hauska G, Stehlik D (1998) Transient electron paramagnetic resonance spectroscopy on green-sulfur bacteria and heliobacteria at two microwave frequencies. Biochim Biophys Acta 1409(2):87–98

    Article  PubMed  Google Scholar 

  • Vermaas WFJ (1994) Evolution of heliobacteria—implications for photosynthetic reaction-center complexes. Photosynth Res 41(1):285–294

    Article  PubMed  CAS  Google Scholar 

  • Woese CR, Debrunnervossbrinck BA, Oyaizu H, Stackebrandt E, Ludwig W (1985) Gram-positive bacteria—possible photosynthetic ancestry. Science 229(4715):762–765

    Article  PubMed  CAS  Google Scholar 

  • Xu Q, Jung YS, Chitnis VP, Guikema JA, Golbeck JH, Chitnis PR (1994) Mutational analysis of photosystem I polypeptides in Synechocystis sp. PCC 6803. Subunit requirements for reduction of NADP+ mediated by ferredoxin and flavodoxin. J Biol Chem 269(34):21512–21518

    PubMed  CAS  Google Scholar 

  • Zhao J, Li R, Bryant DA (1998) Measurement of photosystem I activity with photoreduction of recombinant flavodoxin. Anal Biochem 264(2):263–270

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

This study is supported by a grant from the U.S. Department of Energy Chemical Sciences, Geosciences, & Biosciences Division (DE-FG02-98ER20314).

Author information

Authors and Affiliations

  1. Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, PA, 16802, USA

    Steven P. Romberger & John H. Golbeck

  2. Department of Chemistry, The Pennsylvania State University, University Park, PA, 16802, USA

    John H. Golbeck

Authors
  1. Steven P. Romberger
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. John H. Golbeck
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John H. Golbeck.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Romberger, S.P., Golbeck, J.H. The FX iron–sulfur cluster serves as the terminal bound electron acceptor in heliobacterial reaction centers. Photosynth Res 111, 285–290 (2012). https://doi.org/10.1007/s11120-012-9723-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-012-9723-z

Keywords

Search

Navigation