Skip to main content
SpringerLink
Log in

Cobalt binding in the photosynthetic bacterium R. sphaeroides by X-ray absorption spectroscopy

  • Published:
BioMetals Aims and scope Submit manuscript

Abstract

Cobalt is an important oligoelement required for bacteria; if present in high concentration, exhibits toxic effects that, depending on the microorganism under investigation, may even result in growth inhibition. The photosynthetic bacterium Rhodobacter (R.) sphaeroides tolerates high cobalt concentration and bioaccumulates Co2+ ion, mostly on the cellular surface. Very little is known on the chemical fate of the bioaccumulated cobalt, thus an X-ray absorption spectroscopy investigation was conducted on R. sphaeroides cells to gain structural insights into the Co2+ binding to cellular components. X-ray absorption near-edge spectroscopy and extended X-ray absorption fine structure measurements were performed on R. sphaeroides samples containing whole cells and cell-free fractions obtained from cultures exposed to 5 mM Co2+. An octahedral coordination geometry was found for the cobalt ion, with six oxygen-ligand atoms in the first shell. In the soluble portion of the cell, cobalt was found bound to carboxylate groups, while a mixed pattern containing equivalent amount of two sulfur and two carbon atoms was found in the cell envelope fraction, suggesting the presence of carboxylate and sulfonate metal-binding functional groups, the latter arising from sulfolipids of the cell envelope.

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Albering H, van Leusen S, Moonen E, Hoogewerff J, Kleinjans J (1999) Human health risk assessment: a case study involving heavy metal soil contamination after the flooding of the river Meuse during the winter of 1993–1994. Environ Health Perspect 107(1):37–43

    Article  PubMed  CAS  Google Scholar 

  • Barceloux DG (1999) Cobalt. J Toxicol Clin Toxicol 37(2):201–206

    Article  PubMed  CAS  Google Scholar 

  • Barton MR, Zhang Y, Atwood JD (2002) Mono-sulfonated derivatives of triphenylphosphine, [NH4]TPPMS and M(TPPMS)2 (TPPMS = P(Ph)2(m-C6H4SO3 −); M = Mn2+, Fe2+, Co2+ and Ni2+). Crystal structure determinations for [NH4]TPPMS*½ H2O, [Fe(H2O)5(TPPMS)TPPMS], [Co(H2O)5TPPMS]TPPMS and [Ni(H2O)6](TPPMS)4*H2O. J Coord Chem 55(8):969–983

    Article  CAS  Google Scholar 

  • Bebien M, Chauvin JP, Adriano JM, Grosse S, Vermeglio A (2001) Effect of selenite on growth and protein synthesis in the phototrophic bacterium Rhodobacter sphaeroides. Appl Environ Microbiol 67(10):4440–4447

    Article  PubMed  CAS  Google Scholar 

  • Benning C, Beatty JT, Prince RC, Somerville CR (1993) The sulfolipid sulfoquinovosyldiacylglycerol is not required for photosynthetic electron transport in Rhodobacter sphaeroides but enhances growth under phosphate limitation. Proc Natl Acad Sci USA 90(4):1561–1565

    Article  PubMed  CAS  Google Scholar 

  • Boyanov MI, Kelly SD, Kemner KM, Bunker BA, Fein JB, Fowle DA (2003) Adsorption of cadmium to Bacillus subtilis bacterial cell walls: a pH-dependent X-ray absorption fine structure spectroscopy study. Geochimica et Cosmochimica Acta 67(18):3299–3311. doi:http://dx.doi.org/10.1016/S0016-7037(02)01343-1

    Google Scholar 

  • Brink C, Hodgkin DC, Lindsey J, Pickworth J, Robertson JH, White JG (1954) Structure of vitamin B12: X-ray crystallographic evidence on the structure of vitamin B12. Nature 174(4443):1169–1171

    Article  PubMed  CAS  Google Scholar 

  • Bruins MR, Kapil S, Oehme FW (2000) Microbial resistance to metals in the environment. Ecotoxicol Environ Saf 45(3):198–207

    Article  PubMed  CAS  Google Scholar 

  • Buccolieri A, Italiano F, Dell’Atti A, Buccolieri G, Giotta L, Agostiano A, Milano F, Trotta M (2006) Testing the photosynthetic bacterium Rhodobacter sphaeroides as heavy metal removal tool. Ann Chim 96(3–4):195–203

    Article  PubMed  CAS  Google Scholar 

  • Coucouvanis D, Reynolds RA, Dunham WR (1995) Synthesis and characterization of a new class of asymmetric aqua-acetate bridged dimers. Solid state molecular structures of the [M2(.mu.-H2O)(.mu.-OAc)2(OAc)3(Py)2]-anions (M = Mn(II), Fe(II), Co(II)). A structural model for the Fe2 site in methane monooxygenase. J Am Chem Soc 117(28):7570–7571. doi:10.1021/ja00133a041

    Article  CAS  Google Scholar 

  • D’Amici GM, Rinalducci S, Murgiano L, Italiano F, Zolla L (2010) Oligomeric characterization of the photosynthetic apparatus of Rhodobacter sphaeroides R26.1 by nondenaturing electrophoresis methods. J Proteome Res 9(1):192–203

    Article  PubMed  Google Scholar 

  • Drews G, Golcki JR (1995) Structure, molecular organization and biosynthesis of membranes of purple bacteria. In: Blankenship RE, Madiga MT, Bauer CE (eds) Anoxygenic photosyntetic bacteria. Advances in photosynthesis, vol 2. Kluwer, Dordrecht, pp 231–257

    Chapter  Google Scholar 

  • Fang J, Barcelona MJ, Semrau JD (2000) Characterization of methanotrophic bacteria on the basis of intact phospholipid profiles. FEMS Microbiol Lett 189(1):67–72

    Article  PubMed  CAS  Google Scholar 

  • Forstner U, Wittmann GTW (1983) Metal pollution in the aquatic environment. Springer, Berlin

    Google Scholar 

  • Frenkel AI, Korshin GV (1999) A study of non-uniformity of metal binding sites in humic substances by X-ray absorption spectroscopy. Royal Society of Chemistry, Cambridge

    Google Scholar 

  • Gault N, Sandre C, Poncy JL, Moulin C, Lefaix JL, Bresson C (2010) Cobalt toxicity: chemical and radiological combined effects on HaCaT keratinocyte cell line. Toxicol In Vitro 24(1):92–98. doi:10.1016/j.tiv.2009.08.027

    Article  PubMed  CAS  Google Scholar 

  • Ghabbour EA, Scheinost AC, Davies G (2007) XAFS studies of cobalt(II) binding by solid peat and soil-derived humic acids and plant-derived humic acid-like substances. Chemosphere 67(2):285–291. doi:http://dx.doi.org/10.1016/j.chemosphere.2006.09.094

  • Giotta L, Agostiano A, Italiano F, Milano F, Trotta M (2006) Heavy metal ion influence on the photosynthetic growth of Rhodobacter sphaeroides. Chemosphere 62(9):1490–1499

    Article  PubMed  CAS  Google Scholar 

  • Giotta L, Italiano F, Pisani F, Ceci LLR, De Leo F (2007) Cobalt effect on the bacteriochlorophyll biosynthesis pathway and magnesium metabolism in Rhodobacter sphaeroides strain R26.1. Photosynth Res 91(2–3):302–303

    Google Scholar 

  • Giotta L, Italiano F, Buccolieri A, Agostiano A, Milano F, Trotta M (2008) Magnesium chemical rescue to cobalt-poisoned cells from Rhodobacter sphaeroides. In: Allen JF, Gantt E, Golbeck JH, Osmond B (eds) Photosynthesis. Energy from the sun: 14th international congress on photosynthesis, vol 1. Springer, Dordrecht, pp 1455–1458

    Chapter  Google Scholar 

  • Giotta L, Mastrogiacomo D, Italiano F, Milano F, Agostiano A, Nagy K, Valli L, Trotta M (2011) Reversible binding of metal ions onto bacterial layers revealed by protonation-induced ATR–FTIR difference spectroscopy. Langmuir 27(7):3762–3773. doi:10.1021/la104868m

    Article  PubMed  CAS  Google Scholar 

  • Guengerich FP (2012) Thematic Minireview series: metals in biology 2012. J Biol Chem 287(17):13508–13509. doi:10.1074/jbc.R112.355933

    Article  PubMed  CAS  Google Scholar 

  • Han L-J, Yang S-P, Fu L–L, Gao H-L (2011) Hexaaquacobalt(II) bis(5-acetyl-2-hydroxybenzoate) dihydrate. Acta Crystallogr E 67(12):m1733. doi:10.1107/S1600536811046678

    Article  CAS  Google Scholar 

  • Head IM (1998) Bioremediation: towards a credible technology. Microbiology 144:599–608

    Article  CAS  Google Scholar 

  • Hebes SE, Schwall IR (1978) Microbial degradation of polycyclic aromatic hydrocarbons in pristine and petroleum contaminated sediments. Appl Environ Microb 35:306–316

    Google Scholar 

  • Imhoff JF, Bias-Imhoff U (1995) Lipids, quinines and fatty acids of anoxygenic phototropic bacteria. In: Blankenship RE, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer, Dordrecht, pp 179–205

    Google Scholar 

  • Italiano F, De Leo F, Pisani F, Ceci L, Gallerani R, Zolla L, Rinalducci S, Gio L (2007) Effect of cobalt ions on the soluble proteome of Rhodobacter sphaeroides carotenoidless mutant. Photosynth Res 91(2–3):303

    Google Scholar 

  • Italiano F, Pisani F, De Leo F, Ceci L, Gallerani R, Zolla L, Rinalducci S, Giotta L, Milano F, Agostiano A, Trotta M (2008) Effect of cobalt ions on the soluble proteome of a Rhodobacter sphaeroides carotenoidless mutant. In: Allen JF, Gantt E, Goldbeck J, Osmond B (eds) Photosynthesis. Energy from the sun: 14th international congress on photosynthesis, vol 1. Springer, Dordrecht, pp 1479–1484

    Chapter  Google Scholar 

  • Italiano F, Buccolieri A, Giotta L, Agostiano A, Valli L, Milano F, Trotta M (2009) Response of the carotenoidless mutant Rhodobacter sphaeroides growing cells to cobalt and nickel exposure. Int Biodeterior Biodegrad 63:948–957

    Article  CAS  Google Scholar 

  • Italiano F, D’Amici GM, Rinalducci S, De Leo F, Zolla L, Gallerani R, Trotta M, Ceci LR (2011) The photosynthetic membrane proteome of Rhodobacter sphaeroides R-26.1 exposed to cobalt. Res Microbiol 162(5):520–527

    Article  PubMed  CAS  Google Scholar 

  • Italiano F, Rinalducci S, Agostiano A, Zolla L, De Leo F, Ceci LR, Trotta M (2012) Changes in morphology, cell wall composition and soluble proteome in Rhodobacter sphaeroides cells exposed to chromate. Biometals 25(5):939–949. doi:10.1007/s10534-012-9561-7

    Article  PubMed  CAS  Google Scholar 

  • Jacobs G, Patterson PM, Zhang Y, Das T, Li J, Davis BH (2002) Fischer–Tropsch synthesis: deactivation of noble metal-promoted Co/Al2O3 catalysts. Appl Catal A 233(1–2):215–226. doi:http://dx.doi.org/10.1016/S0926-860X(02)00147-3

  • Jennette KW (1981) The role of metals in carcinogenesis: biochemistry and metabolism. Environ Health Perspect 40:233–252

    Article  PubMed  CAS  Google Scholar 

  • Juhin A, de Groot F, Vankó G, Calandra M, Brouder C (2010) Angular dependence of core hole screening in LiCoO2: a DFT+U calculation of the oxygen and cobalt K-edge X-ray absorption spectra. Phys Rev B 81(11):115115

    Article  Google Scholar 

  • Kantar C, Demiray H, Dogan NM, Dodge CJ (2011) Role of microbial exopolymeric substances (EPS) on chromium sorption and transport in heterogeneous subsurface soils: I. Cr(III) complexation with EPS in aqueous solution. Chemosphere 82(10):1489–1495. doi:http://dx.doi.org/10.1016/j.chemosphere.2011.01.009

    Google Scholar 

  • Kasprzak K (1991) The role of oxidative damage in metal carcinogenicity. Chem Res Toxicol 4(6):604–615

    Article  PubMed  CAS  Google Scholar 

  • Kiley PJ, Kaplan S (1988) Molecular genetics of photosynthetic membrane biosynthesis in Rhodobacter sphaeroides. Microbiol Rev 52(1):50–69

    PubMed  CAS  Google Scholar 

  • Kobayashi M, Shimizu S (1999) Cobalt proteins. Eur J Biochem 261(1):1–9

    Article  PubMed  CAS  Google Scholar 

  • Leonard SM, Gannett P, Rojanasakul Y, Schwegler-Berry D, Castranova V, Vallyathan V, Shi X (1998) Cobalt-mediated generation of reactive oxygen species and its possible mechanism. J Inorg Biochem 70(3–4):239–244

    Article  PubMed  CAS  Google Scholar 

  • Losurdo L, Italiano F, Trotta M, Gallerani R, Luigi RC, De Leo F (2011) Assessment of an internal reference gene in Rhodobacter sphaeroides grown under cobalt exposure. J Basic Microbiol 50(3):302–305

    Article  Google Scholar 

  • Martinezluque M, Dobao MM, Castillo F (1991) Characterization of the assimilatory and dissimilatory nitrate-reducing systems in Rhodobacter: a comparative-study. FEMS Microbiol Lett 83(3):329–334. doi:10.1111/j.1574-6968.1991.tb04485.x

    CAS  Google Scholar 

  • Mishra A, Malik A (2013) Recent advances in microbial metal bioaccumulation. Crit Rev Environ Sci Technol 43(11):1162–1222. doi:10.1080/10934529.2011.627044

    Article  CAS  Google Scholar 

  • Mishra B, Boyanov MI, Bunker BA, Kelly SD, Kemner KM, Nerenberg R, Read-Daily BL, Fein JB (2009) An X-ray absorption spectroscopy study of Cd binding onto bacterial consortia. Geochim Cosmochim Acta 73(15):4311–4325. doi:http://dx.doi.org/10.1016/j.gca.2008.11.032

    Google Scholar 

  • Moen A, Nicholson DG, Rnning M, Lamble GM, Lee J-F, Emerich H (1997) X-Ray absorption spectroscopic study at the cobalt K-edge on the calcination and reduction of the microporous cobalt silicoaluminophosphate catalyst CoSAPO-34. J Chem Soc Faraday Trans 93(22):4071–4077

    Article  CAS  Google Scholar 

  • Moore MD, Kaplan S (1992) Identification of intrinsic high-level resistance to rare-earth oxides and oxyanions in members of the class Proteobacteria: characterization of tellurite, selenite, and rhodium sesquioxide reduction in Rhodobacter sphaeroides. J Bacteriol 174(5):1505–1514

    PubMed  CAS  Google Scholar 

  • Murtaza S, Ruetz M, Gruber K, Kräutler B (2010) Isovitamin B12: a vitamin B12 derivative that flips its tail. Chem Euro J 16(36):10984–10988. doi:10.1002/chem.201001616

    Article  CAS  Google Scholar 

  • Myllykallio H, Zannoni D, Daldal F (1999) The membrane-attached electron carrier cytochrome c(y) from Rhodobacter sphaeroides is functional in respiratory but not in photosynthetic electron transfer. Proc Natl Acad Sci USA 96(8):4348–4353. doi:10.1073/pnas.96.8.4348

    Article  PubMed  CAS  Google Scholar 

  • Nevin R (2000) How lead exposure relates to temporal changes in IQ, violent crime, and unwed pregnancy. Environ Res 83(1):1–22. doi:http://dx.doi.org/10.1006/enrs.1999.4045

    Google Scholar 

  • Newville M, Līviņš P, Yacoby Y, Rehr JJ, Stern EA (1993) Near-edge X-ray-absorption fine structure of Pb: a comparison of theory and experiment. Phys Rev B 47(21):14126–14131

    Article  CAS  Google Scholar 

  • Okamoto S, Eltis LD (2011) The biological occurrence and trafficking of cobalt. Metallomics 3(10):963–970. doi:10.1039/c1mt00056j

    Article  PubMed  CAS  Google Scholar 

  • Pisani F, Italiano F, de Leo F, Gallerani R, Rinalducci S, Zolla L, Agostiano A, Ceci LR, Trotta M (2009) Soluble proteome investigation of cobalt effect on the carotenoidless mutant of Rhodobacter sphaeroides. J Appl Microbiol 106(1):338–349

    Article  PubMed  CAS  Google Scholar 

  • Ravel B, Newville M (2005) ATHENA, ARTEMIS, HEPHAESTUS: data analysis for X-ray absorption spectroscopy using IFEFFIT. J Synchrotron Radiat 12(4):537–541. doi:10.1107/S0909049505012719

    Article  PubMed  CAS  Google Scholar 

  • Sardaro A, Castagnolo M, Trotta M, Italiano F, Milano F, Cosma P, Agostiano A, Fini P (2013) Isothermal microcalorimetry of the metabolically versatile bacterium Rhodobacter sphaeroides. J Therm Anal Calorim 112(1):505–511. doi:10.1007/s10973-012-2895-0

    Article  CAS  Google Scholar 

  • Schultz JE, Weaver PF (1982) Fermentation and anaerobic respiration by Rhodospirillum rubrum and Rhodopseudomonas capsulata. J Bacteriol 149(1):181–190

    PubMed  CAS  Google Scholar 

  • Sobolev AN, Miminoshvili EB, Miminoshvili KE, Sakvarelidze TN (2003) Cobalt diacetate tetrahydrate. Acta Crystallogr E 59(10):m836–m837. doi:10.1107/S1600536803019093

    Article  CAS  Google Scholar 

  • Valls M, de Lorenzo V (2002) Exploiting the genetic and biochemical capacities of bacteria for the remediation of heavy metal pollution. FEMS Microbiol Rev 26(4):327–338

    PubMed  CAS  Google Scholar 

  • Wang H, Gao S, Ng SW (2011) Hexaaquacobalt(II) bis(2,2′-sulfanediyldiacetato-[kappa]3O, S, O’)cobaltate(II) tetrahydrate. Acta Crystallogr E 67(11):m1521. doi:10.1107/S1600536811040979

    Article  CAS  Google Scholar 

  • Weckesser J, Mayer H, Schultz G (1995) Anoxygenic phototrophic bacteria: model organisms for studies on cell wall macromolecules. In: Blankenship RE, Madiga MT, Bauer CE (eds) Anoxygenic photosyntetic bacteria. Advances in photosynthesis, vol 2. Kluwer, Dordrecht, pp 207–230

    Chapter  Google Scholar 

  • Xia K, Bleam W, Helmke PA (1997) Studies of the nature of binding sites of first row transition elements bound to aquatic and soil humic substances using X-ray absorption spectroscopy. Geochim Cosmochim Acta 61(11):2223–2235. doi:http://dx.doi.org/10.1016/S0016-7037(97)00080-X

  • Zabinsky SI, Rehr JJ, Ankudinov A, Albers RC, Eller MJ (1995) Multiple-scattering calculations of X-ray-absorption spectra. Phys Rev B 52(4):2995–3009

    Article  CAS  Google Scholar 

  • Zhang X-L, Ng SW (2005) Hexaaquacobalt(II) bis(6-hydroxypyridine-3-carboxylate). Acta Crystallogr E 61(6):m1140–m1141. doi:10.1107/S1600536805014911

    Article  CAS  Google Scholar 

  • Zhang L-W, Gao S, Ng SW (2011) Hexaaquacobalt(II) bis[4-(pyridin-2-ylmethoxy)benzoate] dihydrate. Acta Crystallogr E 67(11):m1519. doi:10.1107/S1600536811040931

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Ralph Steininger and Joerg Goettlicher at SUL-X beamline at ANKA are greatly acknowledged (Project ENV-219). Support for this work was obtained by the Italian Ministry of Research Education and Education (PRIN 2009) and by COST Action CM0902 Molecular machinery for ion translocation across the membrane.

Author information

Authors and Affiliations

  1. Istituto di Cristallografia, Consiglio Nazionale delle Ricerche, Via Amendola 122/O, 70126, Bari, Italy

    Benny D. Belviso, Rocco Caliandro & Benedetta Carrozzini

  2. Istituto per i Processi Chimico Fisici, Consiglio Nazionale delle Ricerche, Via Orabona 4, 70126, Bari, Italy

    Francesca Italiano & Massimo Trotta

  3. Dipartimento di Biologia, Università Aldo Moro di Bari, Via Orabona 4, 70126, Bari, Italy

    Alessandra Costanza

Authors
  1. Benny D. Belviso
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Francesca Italiano
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rocco Caliandro
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Benedetta Carrozzini
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alessandra Costanza
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Massimo Trotta
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Francesca Italiano.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Belviso, B.D., Italiano, F., Caliandro, R. et al. Cobalt binding in the photosynthetic bacterium R. sphaeroides by X-ray absorption spectroscopy. Biometals 26, 693–703 (2013). https://doi.org/10.1007/s10534-013-9641-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10534-013-9641-3

Keywords

Search

Navigation