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Modulation of fluorescence in Heliobacterium modesticaldum cells

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Abstract

In what appears to be a common theme for all phototrophs, heliobacteria exhibit complex modulations of fluorescence yield when illuminated with actinic light and probed on a time scale of μs to minutes. The fluorescence yield from cells of Heliobacterium modesticaldum remained nearly constant for the first 10–100 ms of illumination and then rose to a maximum level with one or two inflections over the course of many seconds. Fluorescence then declined to a steady-state value within about one minute. In this analysis, the origins of the fluorescence induction in whole cells of heliobacteria are investigated by treating cells with a combination of electron accepters, donors, and inhibitors of the photosynthetic electron transport, as well as varying the temperature. We conclude that fluorescence modulation in H. modesticaldum results from acceptor-side limitation in the reaction center (RC), possibly due to charge recombination between P800 + and A0 .

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Abbreviations

RC:

Reaction center

[4Fe–4S]:

4-Iron–4-sulfur

PMS:

Phenazine methosulfate

BChl:

Bacteriochlorophyll

PS1:

Photosystem 1

A0 :

Primary acceptor in the RC

F0 :

Basal fluorescence level

Fv :

Variable fluorescence

References

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

    Article  CAS  Google Scholar 

  • Amesz J, Fork DC (1967) Quenching of chlorophyll fluorescence by quinones in algae and chloroplasts. Biochim Biophys Acta 143:97–107

    Article  CAS  PubMed  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 1363:175–181

    Article  CAS  PubMed  Google Scholar 

  • Bryant DA, Costas AMG, Maresca JA, Chew AGM, Klatt CG, Bateson MM, Tallon LJ, Hostetler J, Nelson WC, Heidelberg JF, Ward DM (2007) Candidatus Chloracidobacterium thermophilum: an aerobic phototrophic acidobacterium. Science 317:523–526

    Article  CAS  PubMed  Google Scholar 

  • Deinum G, Kramer H, Aartsma TJ, Kleinherenbrink FAM, Amesz J (1991) Fluorescence quenching in Heliobacterium chlorum by reaction centers in the charge separated state. Biochim Biophys Acta 1058:339–344

    Article  CAS  Google Scholar 

  • Duysens LNM, Sweers HE (1963) Mechanism of two photochemical reactions in algae as studied by means of fluorescence. In: JSoP Physiologists (ed) Studies on microalgae and photosynthetic bacteria, pp 353–371. University of Tokyo Press, Japan

    Google Scholar 

  • Francke C, Otte SCM, van der Heiden JC, Amesz J (1994) Spurious circular dichroism signals with intact cells of heliobacteria. Biochim Biophys Acta 1186:75–80

    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 136:11–16

    Article  CAS  Google Scholar 

  • Govindjee (1995) Sixty-three years since Kautsky: chlorophyll a fluorescence. Aust J Plant Physiol 22:131–160

    Article  CAS  Google Scholar 

  • Govindjee, Papageorgiou G (2004) Chlorophyll a fluorescence: a signature of photosynthesis. Springer, Dordrecht

    Google Scholar 

  • Heathcote P, Jones MR, Fyfe PK (2003) Type I photosynthetic reaction centres: structure and function. Phil Trans: Biol Sci 358:231–243

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  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 44:9950–9960

    Article  CAS  PubMed  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 45:6756–6764

    Article  CAS  PubMed  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 46:2530–2536

    Article  CAS  PubMed  Google Scholar 

  • Hiraishi A (1989) Occurrence of menaquinone as the sole isoprenoid quinone in the photosynthetic bacterium Heliobacterium chlorum. Arch Microbiol 151:378–379

    Article  CAS  Google Scholar 

  • Hohmann-Marriott MF, Blankenship RE (2007) Variable fluorescence in green sulfur bacteria. Biochim Biophys Acta 1767:106–113

    Article  CAS  PubMed  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 1777:1535–1544

    Article  CAS  PubMed  Google Scholar 

  • Jagannathan B, Golbeck JH (2009) Understanding of the binding interface between PsaC and the PsaA/PsaB heterodimer in photosystem I. Biochemistry 48:5405–5416

    Article  CAS  PubMed  Google Scholar 

  • Kautsky H, Hirsch A (1931) Neue Versuche zur Kohlensäureassimilation. Naturwissenschaften 19:964

    Article  CAS  Google Scholar 

  • Kimble LK, Madigan MT (1992) Nitrogen fixation and nitrogen metabolism in heliobacteria. Arch Microbiol 158:155–161

    Article  CAS  Google Scholar 

  • Kimble LK, Mandelco L, Woese CR, Madigan MT (1995) Heliobacterium modesticaldum, sp. nov., a thermophilic heliobacterium of hot springs and volcanic soils. Arch Microbiol 163:259–267

    Article  CAS  Google Scholar 

  • Kleinherenbrink FAM, Aartsma TJ, Amesz J (1991) Charge separation and formation of bacteriochlorophyll triplets in Heliobacterium chlorum. Biochim Biophys Acta 1057:346–352

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kleinherenbrink F, Chiou H-C, LoBrutto R, Blankenship R (1994a) Spectroscopic evidence for the presence of an iron-sulfur center similar to Fx of photosystem I in Heliobacillus mobilis. Photosynth Res 41:115–123

    Article  CAS  PubMed  Google Scholar 

  • Kleinherenbrink FAM, Hastings G, Wittmershaus BP, Blankenship RE (1994b) Delayed fluorescence from Fe–S type photosynthetic reaction centers at low redox potential. Biochemistry 33:3096–3105

    Article  CAS  PubMed  Google Scholar 

  • Klerk HD, Govindjee, Kamen MD, Lavorel J (1969) Age and fluorescence characteristics in some species of athiorhodaceae. Proc Nat Acad Sci USA 62:972–978

  • 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. Biochim Biophys Acta 1057:89–96

    Article  CAS  Google Scholar 

  • Kramer DM, Schoepp B, Liebl U, Nitschke W (1997) Cyclic electron transfer in Heliobacillus mobilis involving a menaquinol-oxidizing cytochrome bc complex and an RCI-type reaction center. Biochemistry 36:4203–4211

    Article  CAS  PubMed  Google Scholar 

  • Liebl U, Mockensturm-Wilson 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 Nat Acad Sci USA 90:7124–7128

    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 45:6306–6316

    Article  CAS  PubMed  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 47:4386–4393

    Article  CAS  PubMed  Google Scholar 

  • Mizoguchi T, Oh-oka H, Tamiaki H (2005) Determination of stereochemistry of bacteriochlorophyll g and 81-hydroxy-chlorophyll a from Heliobacterium modesticaldum. Photochem Photobiol 81:666–673

    Article  CAS  PubMed  Google Scholar 

  • Muhiuddin IP, Rigby SEJ, Evans MCW, 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 38:7159–7167

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Oh-oka H, Iwaki M, Itoh S (2002) Electron donation from membrane-bound cytochrome c to the photosynthetic reaction center in whole cells and isolated membranes of Heliobacterium gestii. Photosynth Res 71:137–147

    Article  CAS  PubMed  Google Scholar 

  • Papageorgiou G, Tsimilli-Michael M, Stamatakis K (2007) The fast and slow kinetics of chlorophyll a fluorescence induction in plants, algae and cyanobacteria: a viewpoint. Photosynth Res 94:275–290

    Article  CAS  PubMed  Google Scholar 

  • Redding K, MacMillan F, Leibl W, Brettel K, Hanley J, Rutherford AW, Breton J, Rochaix J-D (1998) A systematic survey of conserved histidines in the core subunits of photosystem I by site-directed mutagenesis reveals the likely axial ligands of P700. EMBO J 17:50–60

    Article  CAS  PubMed  Google Scholar 

  • Roy E, Rohmer T, Gast P, Jeschke G, Alia A, Jr Matysik (2008) Characterization of the primary radical pair in reaction centers of Heliobacillus mobilis by 13C photo-CIDNP MAS NMR. Biochemistry 47:4629–4635

    Article  CAS  PubMed  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 190:4687–4696

    Article  CAS  PubMed  Google Scholar 

  • Schansker G, Tóth SZ, Strasser RJ (2005) Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. Biochim Biophys Acta 1706:250–261

    Article  CAS  PubMed  Google Scholar 

  • Schmidt KA, Trissl H-W (1998) Combined fluorescence and photovoltage studies on chlorosome containing bacteria. Photosynth Res 58:43–55

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Trost JT, Brune DC, Blankenship RE (1992) Protein sequences and redox titrations indicate that the electron acceptors in reaction centers from heliobacteria are similar to photosystem I. Photosynth Res 32:11–22

    Article  CAS  PubMed  Google Scholar 

  • van de Meent EJ, Kobayashi M, Erkelens C, van Veelen PA, Amesz J, Watanabe T (1991) Identification of 81-hydroxychlorophyll a as a functional reaction center pigment in heliobacteria. Biochim Biophys Acta 1058:356–362

    Article  Google Scholar 

  • Vasil’ev S, Wiebe S, Bruce D (1998) Non-photochemical quenching of chlorophyll fluorescence in photosynthesis. 5-hydroxy-1,4-naphthoquinone in spinach thylakoids as a model for antenna based quenching mechanisms. Biochim Biophys Acta 1363:147–156

    Article  PubMed  Google Scholar 

  • Webber AN, Lubitz W (2001) P700: the primary electron donor of photosystem I. Biochim Biophys Acta 1507:61–79

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We would like to thank Dr. Michael Madigan for kindly providing cells of Heliobacterium modesticaldum. This study was supported by grant #NNX08AP62G from the Exobiology program of NASA to R. E. Blankenship, and a CAREER award from the NSF (MCB-0347935) and Fulbright Research grant to KR. KR also acknowledges support from the CNRS while on sabbatical at the IBPC.

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Correspondence to Robert E. Blankenship.

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Collins, A.M., Redding, K.E. & Blankenship, R.E. Modulation of fluorescence in Heliobacterium modesticaldum cells. Photosynth Res 104, 283–292 (2010). https://doi.org/10.1007/s11120-010-9554-8

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