Advertisement

BioMetals

, Volume 32, Issue 1, pp 171–184 | Cite as

Determination of iron species, including biomineralized jarosite, in the iron-hyperaccumulator moss Scopelophila ligulata by Mössbauer, X-ray diffraction, and elemental analyses

  • Hiromitsu NakajimaEmail author
  • Atsushi Okazawa
  • Shiro Kubuki
  • Qing Shen
  • Kiminori Itoh
Article
  • 132 Downloads

Abstract

Scopelophila ligulata is an Fe-hyperaccumulator moss growing in acidic environments, but the mechanism of Fe accumulation remains unknown. To understand the mechanism, we determined Fe species in S. ligulata samples. The moss samples were collected from four sites in Japan. The concentrations of Fe, P, S, Cl, and K in them were measured by induced coupled plasma mass spectrometry. Fe species in some of them were determined by Mössbauer spectroscopy and were confirmed by X-ray diffraction analysis. Fe species in S. ligulata samples were determined to be jarosite, ferritin, high-spin Fe(II) species, and akaganeite. To our knowledge, this is the first report on the biomineralization of jarosite in mosses. This result, combined with the fact that bacteria, a fungus, and a grass mineralize jarosite, suggests that its biomineralization is a common characteristic in a wide variety of living organisms. These findings indicate that the biomineralization of jarosite occurs not only in the region-specific species but in species adapted to a low-pH and metal-contaminated environment in different regions, provide a better understanding of the mechanism of Fe accumulation in the Fe-hyperaccumulator moss S. ligulata, and offer new insights into the biomineralization of jarosite.

Keywords

Scopelophila ligulata Iron Hyperaccumulation Biomineralization Jarosite Akaganeite 

Notes

Acknowledgements

We thank Prof. Yoshio Kobayashi and Prof. Kiyoshi Nomura for helpful comments. This study was partly supported by JSPS KAKENHI Grant No. 26340045.

References

  1. Aikawa Y, Nagano I, Sakamoto S, Nishiyama M, Matsumoto S (1999) Contents of heavy metal elements in copper mosses: Scopelophila ligulata, Scopelophila cataractae, and Mielichhoferia japonica and their substrates. Soil Sci Plant Nutr 45:835–842CrossRefGoogle Scholar
  2. Ambe S (1989) Mössbauer study of iron in the tomato plant. Int J Radiat Appl Instrum Part A 40:671–675CrossRefGoogle Scholar
  3. Ambe S, Ambe F, Nozaki T (1987) Mössbauer study of iron in soybean seeds. J Agric Food Chem 35:292–296CrossRefGoogle Scholar
  4. Amils R, de la Fuente V, Rodríguez N, Zuluaga J, Menéndez N, Tornero J (2007) Composition, speciation and distribution of iron minerals in Imperata cylindrica. Plant Physiol Biochem 45:335–340CrossRefGoogle Scholar
  5. Ancuceanu R, Dinu M, Hovaneţ MV, Anghel AI, Popescu CV, Negreş S (2015) A survey of plant iron content: a semi-systematic review. Nutrients 7:10320–10351CrossRefGoogle Scholar
  6. Baron D, Palmer CD (1996) Solubility of jarosite at 4–35 °C. Geochim Cosmochim Acta 60:185–195CrossRefGoogle Scholar
  7. Barrero CA, García KE, Morales AL, Kodjikian S, Greneche JM (2006) New analysis of the Mössbauer spectra of akaganeite. J Phys 18:6827–6840Google Scholar
  8. Bauminger ER, Cohen SG, Dickson DPE, Levy A, Ofer S, Yariv J (1980) Mössbauer spectroscopy of Escherichia coli and its iron-storage protein. Biochim Biophys Acta 623:237–242CrossRefGoogle Scholar
  9. Bell SH, Weir MP, Dickson DPE, Gibson JF, Sharp GA, Peters TJ (1984) Mössbauer spectroscopic studies of human haemosiderin and ferritin. Biochim Biophys Acta 787:227–236CrossRefGoogle Scholar
  10. Bibi I, Singh B, Silvester E (2001) Akaganéite (β-FeOOH) precipitation in inland acid sulfate soils of south-western New South Wales (NSW), Australia. Geochim Cosmochim Acta 75:6429–6438CrossRefGoogle Scholar
  11. Bigham JM, Carlson L, Murad E (1994) Schwertmannite, a new iron oxyhydroxysulphate from Pyhäsalmi, Finland, and other localities. Miner Mag 58:641–648CrossRefGoogle Scholar
  12. Böhnke R, Matzanke BF (1995) The mobile ferrous iron pool in Escherichia coli is bound to a phosphorylated sugar derivative. Biometals 8:223–230CrossRefGoogle Scholar
  13. Bou-Abdallah F (2010) The iron redox and hydrolysis chemistry of the ferritins. Biochim Biophys Acta 1800:719–731CrossRefGoogle Scholar
  14. Buchanan BB, Gruissem W, Jones RL (2015) Biochemistry and molecular biology of plants, 2nd edn. Wiley, West SussexGoogle Scholar
  15. Casas C, Brugues M, Cros RM, Sergio C (2006) Handbook of mosses of the Iberian Peninsula and the Balearic Islands. Institut d’Estudis Catalans, BarcelonaGoogle Scholar
  16. Chambaere D, de Grave E (1984) On the Neel temperature of β-FeOOH: structural dependence and its applications. J Magn Magn Mater 42:263–268CrossRefGoogle Scholar
  17. Chasteen ND, Harrison PM (1999) Mineralization in ferritin: an efficient means of iron strage. J Struct Biol 126:182–194CrossRefGoogle Scholar
  18. Cornell RM, Schwertmann U (2003) The iron oxides. Wiley-VCH, WeinheimCrossRefGoogle Scholar
  19. de Grave E, Vandenberghe RE (1986) 57Fe Mössbuaer effect study of well-crystallized goethite (α-FeOOH). Hyperfine Interact 28:643–646CrossRefGoogle Scholar
  20. Franco A, Rufo L, Fuente V (2015) Fe absorption and distribution of Imperata cylindrica (L.) P. Beauv. under controlled conditions. Environ Anal Toxicol 2:1.  https://doi.org/10.4172/21610525.1000335 Google Scholar
  21. Frankel RB, Papaefthymiou GC (1987) Binding of Fe2+ by Mammalian Ferritin. Hyperfine Interact 33:233–240CrossRefGoogle Scholar
  22. Fuente V, Rufo L, Juárez BH, Menéndez N, García-Hernández M, Salas-Colera E, Espinosa A (2016) Formation of biomineral iron oxides compounds in a Fe hyperaccumulator plant: Imperata cylindrica (L.) P. Beauv. J Struct Biol 193:23–32CrossRefGoogle Scholar
  23. Gao X, Schulze DG (2010) Precipitation and transformation of secondary Fe oxyhydroxides in a histosol impacted by runoff from lead smelter. Clays Clay Miner 58:377–387CrossRefGoogle Scholar
  24. Goodman BA, DeKock PC (1982) Mössbauer studies of plant materials. I. Duckweed, stocks, soyabean and pea. J Plant Nutr 5:345–353CrossRefGoogle Scholar
  25. Hájek M, Plesková Z, Syrovátka V, Peterka T, Laburdová J, Kintrová K, Martin Jiroušek M, Hájek T (2014) Patterns in moss element concentrations in fens across species, habitats, and regions. Perspect Plant Ecol Evol Syst 16:203–218CrossRefGoogle Scholar
  26. Harmens H, Norris D, Mills G, and the participants of the moss survey (2013) Heavy metals and nitrogen in mosses: spatial patterns in 2010/2011 and long-term temporal trends in Europe. ICP Vegetation Programme Coordination Centre, Centre for Ecology and Hydrology, Bangor, p 63Google Scholar
  27. Harmens H, Norris DA, Steinnes E, Kubin E, Piispanen J, Alber R, Aleksiayenak Y, Blum O, Coşkun M, Dam M, De Temmerman L, Fernández JA, Frolova M, Frontasyeva M, González-Miqueo L, Grodzińska K, Jeran Z, Korzekwa S, Krmar M, Kvietkus K, Leblond S, Liiv S, Magnússon SH, Maňkovská B, Pesch R, Rühling Å, Santamaria JM, Schröder W, Spiric Z, Suchara I, Thöni L, Urumov V, Yurukova L, Zechmeister HG (2010) Mosses as biomonitors of atmospheric heavy metal deposition: spatial patterns and temporal trends in Europe. Environ Pollut 158:3144–3156CrossRefGoogle Scholar
  28. Harmens H, Norris DA, Sharps K, Mills G, Alber R, Aleksiayenak Y, Blum O, Cucu-Man SM, Dam M, De Temmerman L, Ene A, Fernández JA, Martinez-Abaigar J, Frontasyeva M, Godzik B, Jeran Z, Lazo P, Leblond S, Liiv S, Magnússon SH, Maňkovská B, Pihl Karlsson G, Piispanen J, Poikolainen J, Santamaria JM, Skudnik M, Spiric Z, Stafilov T, Steinnes E, Stihi C, Suchara I, Thöni L, Torodan R, Yurukova L, Zechmeister HG (2015) Heavy metal and nitrogen concentrations in mosses are declining across Europe whilst some “hotspots” remain in 2010. Environ Pollut 200:93–104CrossRefGoogle Scholar
  29. Herbert RB Jr (1997) Properties of goethite and jarosite precipitated from acidic groundwater, Dalarna, Sweden. Clays Clay Miner 45:261–273CrossRefGoogle Scholar
  30. Itouga M, Komatsu-Kato Y, Yamaguchi I, Ono Y, Sakakibara H (2006) Phytoremediation using bryophytes, 2. Bryo-filtration of copper in water using two species of Scopelophila. Hikobia 14:413–418Google Scholar
  31. Itouga M, Komatsu-Kato Y, Kiguchi H, Ono Y, Sakakibara H (2007) Iron analysis of sporophyte in Scopelophila ligulata using X-ray fluorescence micro-analyzer. Hikobia 15:105–108Google Scholar
  32. Itouga M, Hayatsu M, Sato M, Tsuboi Y, Kato Y, Toyooka K, Suzuki S, Nakatsuka S, Kawakami S, Kikuchi J, Sakakibara H (2017) Protonema of the moss Funaria hygrometrica can function as a lead (Pb) adsorbent. PLoS ONE 12:e0189726CrossRefGoogle Scholar
  33. Johnson CE (1969) Antiferromagnetic of γ-FeOOH: a Mössbuaer effect study. J Phys C 2:1996–2002CrossRefGoogle Scholar
  34. Jones B, Renaut RW (2007) Selective mineralization of microbes in Fe-rich precipitates (jarosite, hydrous ferric oxides) from acid hot springs in the Waiotapu geothermal area, North Island, New Zealand. Sediment Geol 194:77–98CrossRefGoogle Scholar
  35. Kilcoyne SH, Bentley PM, Thongbai P, Gordon DC, Goodman BA (2000) The application of 57Fe Mössbauer spectroscopy in the investigation of iron uptake and translocation in plants. Nucl Instrum Meth Phys Res B 160:157–166CrossRefGoogle Scholar
  36. Kim SA, Guerinot ML (2007) Mining iron: iron uptake and transport in plants. FEBS Lett 581:2273–2280CrossRefGoogle Scholar
  37. Klencsár Z, Kuzmann E, Vértes A (1996) User-freidnly software for Mössbuaer spectrum analysis. J Radioanal Nucl Chem 210:105–118CrossRefGoogle Scholar
  38. Klingelhöfer G, Morris RV, Bernhardt B, Schröder C, Rodionov DS, Souza PA Jr, Yen A, Gellert R, Evlanov EN, Zubkov B, Foh J, Bonnes U, Kankeleit E, Gütlich P, Ming DW, Renz F, Wdowiak T, Squyres SW, Arvidson RE (2004) Jarosite and hematite at Meridiani Planum from Opportunity’s Mössbauer spectrometer. Science 306:1740–1745CrossRefGoogle Scholar
  39. Leclerc A (1980) Room temperature Mössbauer analysis of jarosite-type compounds. Phys Chem Miner 6:327–334CrossRefGoogle Scholar
  40. Lenton TM, Dahl TW, Daines SJ, Mills BJW, Ozaki K, Saltzman MR, Porada P (2016) Earliest land plants created modern levels of atmospheric oxygen. Proc Natl Acad Sci USA 113:9704–9709CrossRefGoogle Scholar
  41. Lo JC, Tsednee M, Lo YC, Yang SC, Hu JM, Ishizaki K, Kohchi T, Lee DC, Yeh KC (2016) Evolutionary analysis of iron (Fe) acquisition system in Marchantia polymorpha. New Phytol 211:569–583CrossRefGoogle Scholar
  42. Luna C, Ilyn M, Vega V, Prida VM, Gonzalez J, Mendoza-Resendez R (2014) Size distribution and frustrated antiferromagnetic coupling effects on the magnetic behavior of ultrafine akaganéite (β-FeOOH) aanoparticles. J Phys Chem C 118:21128–21139CrossRefGoogle Scholar
  43. Madden MEE, Bodnar RJ, Rimstidt JD (2004) Jarosite as an indicator of water-limited chemical weathering on Mars. Nature 431:821–823CrossRefGoogle Scholar
  44. Matzanke BF, Bill E, Müller GI, Winkelmann G, Trautwein AX (1989) In vivo Mössbauer spectroscopy of iron uptake and ferrometabolism in Escherichia coli. Hyperfine Interact 47:311–327CrossRefGoogle Scholar
  45. Matzanke BF, Bill E, Trautwein AX (1992) Main components of iron metabolism in microbial systems—analyzed by in vivo Mössbauer spectroscopy. Hyperfine Interact 71:1259–1262CrossRefGoogle Scholar
  46. Murad E (1979) Mössbauer and X-ray data on β-FeOOH (akaganéite). Clay Miner 14:273–283CrossRefGoogle Scholar
  47. Murad E, Schwertmann U (1984) The influence of crystallinity on the Mössbuaer spectrum of lepidocrocite. Miner Mag 48:507–511CrossRefGoogle Scholar
  48. Nakajima H, Itoh K (2017) Relationship between metal and pigment concentrations in the Fe-hyperaccumulator moss Scopelophila ligulata. J Plant Res 130:135–141CrossRefGoogle Scholar
  49. Nakajima H, Itoh K, Otake H, Fujimoto K (2010) Photoabsorption study of pigments in mosses: scopelophila ligulata has an abnormally high formation rate of pheophytin. Chem Lett 39:284–285CrossRefGoogle Scholar
  50. Noguchi A (1988) Illustrated Moss Flora of Japan, Part 2. Hattori Botanical Laboratory, Hiroshima, p 328Google Scholar
  51. Oggerin M, Rodríguez N, del Moral C, Amils R (2014) Fungal jarosite biomineralization in Río Tinto. Res Microbiol 165:719–725CrossRefGoogle Scholar
  52. Onianwa PC (2001) Monitoring atmospheric metal pollution: a review of the use of mosses as indicators. Environ Monit Assess 71:13–50CrossRefGoogle Scholar
  53. Oue K, Ohsawa S, Yusa Y (2002) Change in color of the hot spring deposits at the Chinoike-Jigoku hot pool. Beppu geothermal field. Geothermics 31:361–380CrossRefGoogle Scholar
  54. Post JE, Buchwald VF (1991) Crystal structure refinement of akaganéite. Am Miner 76:272–277Google Scholar
  55. Proctor MCF (2009) Physiological ecology. In: Goffinet B, Shaw AJ (eds) Bryophyte biology, 2nd edn. Cambridge University Press, New York, pp 237–268Google Scholar
  56. Rodríguez N, Menéndez N, Tornero J, Amils R, de la Fuente V (2005) Internal iron biomineralization in Imperata cylindrica, a perennial grass: chemical composition, speciation and plant localization. New Phytol 165:781–789CrossRefGoogle Scholar
  57. Ron E, Estébanez B, Alfayate C, Marfil R, Cortella A (1999) Mineral deposits in cells of Hookeria lucens. J Bryol 21:281–288CrossRefGoogle Scholar
  58. Shaw AJ (1990) Metal tolerance in bryophytes. In: Shaw AJ (ed) Heavy metal tolerance in plants: evolutionary aspects. CRC Press, Boca Raton, pp 133–152Google Scholar
  59. Shaw J, Antonovics J, Anderson LE (1987) Inter- and intraspecific variation of mosses in tolerance to copper and zinc. Evolution 41:1312–1325CrossRefGoogle Scholar
  60. Sperotto RA, Ricachenevsky FK, Stein RJ, Waldow VA, Fett JP (2010) Iron stress in plants: dealing with deprivation and overload. Plant Stress 4:57–69Google Scholar
  61. St Pierre TG, Bell SH, Dickson DPE, Mann S, Webb J, Moore GR, Williams RJP (1986) Mössbauer spectroscopic studies of the cores of human, limpet and bacterial ferritins. Biochim Biophys Acta 870:127–134CrossRefGoogle Scholar
  62. St Pierre TG, Carson KC, Webb J, Glenn AR, Dilworth MJ (1999) Evidence for polynuclear iron(III) clusters in the root nodule bacterium, Rhizobium leguminosarum bv. Viciae WSM710. Biometals 12:73–76CrossRefGoogle Scholar
  63. Stein RJ, Duarte GL, Spohr MG, Lopes SIG, Fett JP (2009) Distinct physiological responses of two rice cultivars subjected to iron toxicity under field conditions. Ann Appl Biol 154:269–277CrossRefGoogle Scholar
  64. Takano M, Shinjo T, Takada T (1971) On the spin arrangement in “Kagome” lattice of antiferromagnetic KFe3(OH)6(SO4)2. J Phys Soc Jpn 30:1049–1053CrossRefGoogle Scholar
  65. Townsend MG, Longworth G, Roudaut E (1986) Triangular-spin, kagome plane in jarosites. Phys Rev B 33:4919–4926CrossRefGoogle Scholar
  66. Tyler G (1990) Bryophytes and heavy metals: a literature review. Bot J Linnean Soc 104:231–253CrossRefGoogle Scholar
  67. Urtizberea A, Luis F, Millan A, Natividad E, Palacio F, Kampert E, Zeitler U (2011) Thermoinduced magnetic moment in akaganeite nanoparticles. Phys Rev B 83:214426–214427CrossRefGoogle Scholar
  68. Wade VJ, Treffry A, Laulhère J-P, Bauminger ER, Cleton MI, Mann S, Briat J-F, Harrison PM (1993) Structure and composition of ferritin cores from pea seed (Pisum sativum). Biochim Biophys Acta 1161:91–96CrossRefGoogle Scholar
  69. Yang CY, Bryan AM, Theil EC, Sayers DE, Bowen LH (1986) Structural variations in soluble iron complexes of models for ferritin: an X-ray absorption and mössbauer spectroscopy comparison of horse spleen ferritin to blutal (iron-chondroitin sulfate) and imferon (iron-dextran). J Inorg Biochem 28:393–405CrossRefGoogle Scholar
  70. Ziegler S, Ackermann S, Majzlan J, Gescher J (2009) Matrix composition and community structure analysis of a novel bacterial pyrite leaching community. Environ Microbiol 11:2329–2338CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Hiromitsu Nakajima
    • 1
    • 2
    Email author
  • Atsushi Okazawa
    • 3
  • Shiro Kubuki
    • 4
  • Qing Shen
    • 1
  • Kiminori Itoh
    • 2
  1. 1.Faculty of Informatics and EngineeringThe University of Electro-CommunicationsChofuJapan
  2. 2.Graduate School of Environment and Information SciencesYokohama National UniversityYokohamaJapan
  3. 3.Department of Basic Science, Graduate School of Arts and SciencesThe University of TokyoTokyoJapan
  4. 4.Graduate School of Science and EngineeringTokyo Metropolitan UniversityHachiojiJapan

Personalised recommendations