, Volume 121, Issue 3, pp 505–517 | Cite as

Spectroscopic (XANES/XRF) characterization of contaminant manganese cycling in a temperate watershed

  • Elizabeth M. HerndonEmail author
  • Carmen E. Martínez
  • Susan L. Brantley


Many soils around the globe are contaminated with metals due to inputs from anthropogenic activities; however, the long-term processes that retain these metals in soils or flush them into river systems remain unclear. Soils at the Susquehanna/Shale Hills Critical Zone Observatory, a headwater catchment in central Pennsylvania, USA, are enriched in manganese due to past atmospheric deposition from industrial sources. To investigate how Mn is retained in the catchment, we evaluated the spatial distribution and speciation of Mn in the soil–plant system using X-ray fluorescence and X-ray Absorption Near Edge Structure spectroscopies. Weathered soils near the land surface were enriched in both amorphous and crystalline Mn(III/IV)-oxides, presumably derived from biogenic precipitation and atmospheric deposition, respectively. In contrast, mineral soils near the soil–bedrock interface contained Mn(II) in clays and crystalline Mn(III/IV)-oxides that formed as Mn(II) was leached from the parent shale and oxidized. Roots, stems, and foliar tissue were dominated by organic-bound and aqueous Mn(II); however, a small portion of foliar Mn was concentrated as organic-bound Mn(III) in dark spots that denote Mn toxicity. During decomposition of leaves and roots, soluble Mn(II) stored in vegetation was rapidly oxidized and immobilized as mixed-valence Mn-oxides. We propose that considerable uptake of Mn by certain plant species combined with rapid oxidation of Mn during organic matter decomposition contributes to long-term retention in soils and may slow removal of Mn contamination from watersheds.


Manganese Spectroscopy Critical zone Soil geochemistry Metal contamination 



This study was supported by National Science Foundation grant EAR #1052614 to SLB, the NSF Susquehanna Shale Hills Critical Zone Observatory grant EAR #0725019 to C. Duffy (Penn State), and NSF grant CHE #0431328 to SLB. The authors particularly acknowledge the help of Matthew Newville (GSECARS) and Dale Brewe (PNC/XSD) at APS and Timothy Fischer for scientific support at the beamlines, and Katie Gaines, Jim Savage, and Jane Wubbels for leaf collection at SSHCZO. Portions of this work (µXRF and µXANES) were performed at GeoSoilEnviroCARS (Sector 13), Advanced Photon Source (APS), Argonne National Laboratory. GeoSoilEnviroCARS is supported by the NSF—Earth Sciences (EAR-1128799) and DOE—Geosciences (DE-FG02-94ER14466). Use of the APS was supported by the U. S. Department of Energy Office of Science, Office of Basic Energy Sciences, under Contract No. DE-AC02-06CH11357. Other portions of this work (bulk XANES) were performed at PNC/XSD facilities. PNC/XSD facilities at the APS, and research at these facilities, are supported by the US DOE—Basic Energy Sciences, a Major Resources Support grant from NSERC, the University of Washington, Simon Fraser University and the Advanced Photon Source. Use of the Advanced Photon Source, an Office of Science User Facility operated for the U.S. DOE Office of Science by Argonne National Laboratory, was supported by the U.S. DOE under Contract No. DE-AC02-06CH11357.

Supplementary material

10533_2014_18_MOESM1_ESM.pdf (1.5 mb)
Supplementary material 1 (PDF 1549 kb)


  1. Andrews DM, Lin H, Zhu Q, Jin L, Brantley SL (2011) Hot spot and hot moments of dissolved organic carbon export and soil organic carbon storage in the Shale Hills catchment. Vadose Zone J 10:943–954Google Scholar
  2. Archibald FS, Fridovich I (1982) The scavenging of superoxide radical by manganous complexes: in vitro. Arch Biochem Biophys 214(2):452–463CrossRefGoogle Scholar
  3. Bargar JR, Webb SM, Tebo BM (2005) EXAFS, XANES and In-Situ SR-XRD characterization of biogenic manganese oxides produced in sea water. Phys Scr T115:888–890CrossRefGoogle Scholar
  4. Berg B, Steffen KT, McClaugherty C (2007) Litter decomposition rate is dependent on litter Mn concentrations. Biogeochemistry 82:29–39CrossRefGoogle Scholar
  5. Blamey FPC, Joyce DC, Edwards DG, Asher CJ (1986) Role of trichomes in sunflower tolerance to manganese toxicity. Plant Soil 91:171–180CrossRefGoogle Scholar
  6. Brantley SL, Lebedeva M (2011) Learning to read the chemistry of the regolith to understand the Critical Zone. Ann Rev Earth Planet Sci 39:387–416Google Scholar
  7. Broadhurst CL, Tappero RV, Maugel TK, Erbe EF, Sparks DL, Chaney RL (2009) Interaction of nickel and manganese in accumulation and localization in leaves of the Ni hyperaccumulators Alyssum murale and Alyssum corsicum. Plant Soil 314:35–48CrossRefGoogle Scholar
  8. Bunker G (2010) Introduction to XAFS: a practical guide to X-ray absorption fine structure spectroscopy, 1st edn. Cambrige University Press, Cambrige, MACrossRefGoogle Scholar
  9. Cui H, Liu F, Feng X, Tan W, Wang MK (2010) Aging promotes todorokite formation from layered manganese oxide at near-surface conditions. J Soils Sediments 10:1540–1547Google Scholar
  10. Duckworth OW, Sposito G (2005) Siderophore-manganese(III) interactions II. Manganite dissolution promoted by desferrioxamine B. Environ Sci Technol 39:6045–6051CrossRefGoogle Scholar
  11. Eickhorst T, Tippkötter R (2008) Detection of microorganisms in undisturbed soil by combining fluorescence in situ hybridization (FISH) and micropedological methods. Soil Biol Biochem 40:1284–1293CrossRefGoogle Scholar
  12. Fernando DR, Mizuno T, Woodrow IE, Baker AJM, Collins RN (2010) Characterization of foliar manganese (Mn) in Mn (hyper)accumulators using X-ray absorption spectroscopy. New Phytol 188:1014–1027CrossRefGoogle Scholar
  13. Gonzalez A, Lynch JP (1999) Subcellular and tissue Mn compartmentation in bean leaves under Mn toxicity stress. Aust J Plant Physiol 26:811–822CrossRefGoogle Scholar
  14. Gonzalez A, Steffen K, Lynch J (1998) Light and excess manganese. Implications for oxidative stress in common bean. Plant Physiol 118:493–504CrossRefGoogle Scholar
  15. Harrington JM, Parker DL, Bargar JR, Jarzecki AA, Tebo BM, Sposito G, Duckworth O (2012a) Structural dependence of Mn complexation by siderophores: donor group dependence on complex stability and reactivity. Geochim Cosmochim Acta 88:106–119CrossRefGoogle Scholar
  16. Harrington JM, Bargar JR, Jarzecki AA, Roberts JG, Sombers LA, Duckworth OW (2012b) Trace metal complexation by the triscatecholate siderophore protochelin: structure and stability. Biometals 25:393–412CrossRefGoogle Scholar
  17. Herndon EM (2012) Biogeochemistry of manganese contamination in a temperate forested watershed. PhD Dissertation, The Pennsylvania State UniversityGoogle Scholar
  18. Herndon EM, Brantley SL (2011) Movement of manganese contamination through the critical zone. Appl Geochem 26:S40–S43CrossRefGoogle Scholar
  19. Herndon EM, Jin L, Brantley SL (2011) Soils reveal widespread manganese enrichment from industrial inputs. Environ Sci Technol 45:241–247CrossRefGoogle Scholar
  20. Hocking PJ (1980) The Composition of phloem exudate and xylem sap from tree tobacco (Nicotiana glauca Grah.). Ann Bot 45:633–643Google Scholar
  21. Hofrichter M (2002) Review: lignin conversion by manganese peroxidase (MnP). Enzym Microb Technol 30:454–466CrossRefGoogle Scholar
  22. Horiguchi T (1987) Mechanism of manganese toxicity and tolerance of plants. Soil Sci Plant Nutr 33:595–606CrossRefGoogle Scholar
  23. Horsley SB, Long RR, Bailey SW, Hallett RA, Hall TJ (2000) Factors associated with the decline disease of sugar maple on the Allegheny Plateau. Can J For Res 30:1365–1378CrossRefGoogle Scholar
  24. Huggins FE, Srikantapura S, Parekh BK, Blanchard L, Robertson JD (1997) XANES spectroscopic characterization of selected elements in deep-cleaned fractions of kentucky No. 9 Coal. Energy Fuels 11:691–701CrossRefGoogle Scholar
  25. Jin L, Ravella R, Ketchum B, Bierman PR, Heaney P, White T, Brantley SL (2010) Mineral weathering and elemental transport during hillslope evolution at the Susquehanna/Shale Hills Critical Zone Observatory. Geochim Cosmochim Acta 74:3669–3691CrossRefGoogle Scholar
  26. Jobbagy EG, Jackson RB (2004) The uplift of soil nutrients by plants: biogeochemical consequences across scales. Ecology 85:2380–2389Google Scholar
  27. Kabata-Pendias A, Pendias H (2001) Trace elements in soils and plants, 3rd edn. CRC Press LLC, Boca RatonGoogle Scholar
  28. Kogelmann WJ, Sharpe WE (2006) Soil acidity and manganese in declining and nondeclining sugar maple stands in Pennsylvania. J Environ Qual 35:433–441CrossRefGoogle Scholar
  29. Learman DR, Wankel SD, Webb SM, Martinez N, Madden AS, Hansel CM (2011a) Coupled biotic–abiotic Mn(II) oxidation pathway mediates the formation and structural evolution of biogenic Mn oxides. Geochim Cosmochiam Acta 75:6048–6063CrossRefGoogle Scholar
  30. Learman DR, Voelker BM, Vazquez-Rodriguez AI, Hansel CM (2011b) Formation of manganese oxides by bacterially generated superoxide. Nat Geosci 4:95–98CrossRefGoogle Scholar
  31. Learman DR, Voelker BM, Madden AS, Hansel CM (2013) Constraints on superoxide mediated formation of manganese oxides. Front Microbiol 4:262Google Scholar
  32. Ma L, Chabaux F, Pelt E, Blaes E, Jin L, Brantley SL (2010) Regolith production rates calculated with uranium-series isotopes at Susquehanna/Shale Hills Critical Zone Observatory. Earth Planet Sci Lett 297:211–225CrossRefGoogle Scholar
  33. Madison AS, Tebo Bradley M, Luther GW (2011) Simultaneous determination of soluble manganese(III), manganese(II) and total manganese in natural (pore)waters. Talanta 84:374–381CrossRefGoogle Scholar
  34. Manceau A, Marcus MA, Grangeon S (2012) Determination of Mn valence states in mixed-valence manganates by XANES spectroscopy. Am Mineral 97:816–827CrossRefGoogle Scholar
  35. McKeown D, Post J (2001) Characterization of manganese oxide mineralogy in rock varnish and dendrites using X-ray absorption spectroscopy. Am Mineral 86:701–713Google Scholar
  36. McNear DH, Kupper JV (2014) Mechanisms of trichome-specific Mn accumulation and toxicity in the Ni hyperaccumulator Alyssum murale. Plant Soil 377:407–422Google Scholar
  37. McNear DH, Peltier E, Everhart J, Chaney RL, Sutton S, Newville M, Rivers M, Sparks DL (2005) Application of quantitative fluorescence and absorption-edge computed microtomography to image metal compartmentalization in Alyssum murale. Environ Sci Technol 39:2210–2218CrossRefGoogle Scholar
  38. Miyata N, Tani Y, Maruo K, Tsuno H, Sakata M, Iwahori K (2006) Manganese(IV) oxide production by Acremonium sp. strain KR21-2 and extracellular Mn(II) oxidase activity. Appl Environ Microbiol 72:6467–6473CrossRefGoogle Scholar
  39. Newville M (2001) EXAFS analysis using FEFF and FEFFIT. J Synchrotron Radiat 8:96–100CrossRefGoogle Scholar
  40. Newville M. (2006) DataViewer.
  41. Nriagu J, Pacyna J (1988) Quantitative assessment of worldwide contamination of air, water and soils by trace metals. Nature 333:134–139CrossRefGoogle Scholar
  42. Nunan N, Ritz K, Crabb D, Harris K, Wu K, Crawford JW, Young IM (2001) Quantification of the in situ distribution of soil bacteria by large-scale imaging of thin sections of undisturbed soil. FEMS Microbiol Ecol 36:67–77CrossRefGoogle Scholar
  43. Oh N-H, Richter DD (2005) Element translocation and loss from three highly weathered soil-bedrock profiles in the southeastern United States. Geoderma 126:5–25Google Scholar
  44. Pacyna JM, Pacyna EG (2001) An assessment of global and regional emissions of trace metals to the atmosphere from anthropogenic sources worldwide. Environ Rev 9:269–298CrossRefGoogle Scholar
  45. Ravel B, Newville M (2005) Athena, Artemis, and Hephaestus: Data analysis for x-ray absorption spectroscopy using IFEFFIT. J Synchrotron Radiat 12:537–541CrossRefGoogle Scholar
  46. Ressler T, Wong J, Roos J, Smith IL (2000) Quantitative speciation of mn-bearing particulates emitted from autos burning (methylcyclopentadienyl)manganese tricarbonyl-added gasolines using xanes spectroscopy. Environ Sci Technol 34:950–958CrossRefGoogle Scholar
  47. Riesen O, Feller U (2005) Redistribution of nickel, cobalt, manganese, zinc, and cadmium via the phloem in young and maturing wheat. J Plant Nutr 28:421–430CrossRefGoogle Scholar
  48. Santelli CM, Pfister DH, Lazarus D, Sun L, Burgos WD, Hansel CM (2010) Promotion of Mn(II) oxidation and remediation of coal mine drainage in passive treatment systems by diverse fungal and bacterial communities. Appl Environ Microbiol 76:4871–4875CrossRefGoogle Scholar
  49. Santelli CM, Webb SM, Dohnalkova AC, Hansel CM (2011) Diversity of Mn oxides produced by Mn(II)-oxidizing fungi. Geochim Cosmochim Acta 75:2762–2776CrossRefGoogle Scholar
  50. Schulze D, McCay-Buis T, Sutton SR, Huber D (1995) Manganese oxidation states in Gaeumannomyces-infested wheat rhizospheres probed by micro-XANES spectroscopy. Phytopathology 85:990–994CrossRefGoogle Scholar
  51. St. Clair SB, Carlson JE, Lynch Jonathan P (2005) Evidence for oxidative stress in sugar maple stands growing on acidic, nutrient imbalanced forest soils. Oecologia 145:258–269CrossRefGoogle Scholar
  52. Suarez D, Langmuir D (1976) Heavy metal relationships in a Pennsylvania soil. Geochim Cosmochim Acta 40:589–598CrossRefGoogle Scholar
  53. Tebo BM, Bargar JR, Clement BG, Dick GJ, Murray KJ, Parker D, Verity R, Webb SM (2004) Biogenic manganese oxides: properties and mechanisms of formation. Annu Rev Earth Planet Sci 32:287–328CrossRefGoogle Scholar
  54. Thompson I, Huber DM, Guest C, Schulze DG (2005) Fungal manganese oxidation in a reduced soil. Environ Microbiol 7:1480–1487CrossRefGoogle Scholar
  55. Tippkotter R, Ritz K (1996) Evaluation of polyester, epoxy and acrylic resins for suitability in preparation of soil thin sections for in situ biological studies. Geoderma 69:31–57CrossRefGoogle Scholar
  56. Trouwborst RE, Clement BG, Tebo BM, Glazer BT, Luther GW (2006) Soluble Mn(III) in suboxic zones. Sci (New York, N.Y.) 313:1955–1957CrossRefGoogle Scholar
  57. U.S. Environmental Protection Agency (1984) Health assessment document for manganese. Cincinatti, OhioGoogle Scholar
  58. Webb SM, Dick GJ, Bargar JR, Tebo BM (2005) Evidence for the presence of Mn(III) intermediates in the bacterial oxidation of Mn(II). Proc Nat Acad Sci 102:5558–5563CrossRefGoogle Scholar
  59. White PJ (2012) Long-distance Transport in the Xylem and Phloem. In Marschner’s Mineral Nutrition of Higher Plants Elsevier Ltd. pp. 49–70Google Scholar
  60. Wubbels JK (2010) Tree species distribution in relation to stem hydraulic traits and soil moisture in a mixed hardwood forest in central Pennsylvania. Master’s Thesis, The Pennsylvania State UniversityGoogle Scholar
  61. Xu X, Shi J, Chen X, Chen Y, Hu T (2009) Chemical forms of manganese in the leaves of manganese hyperaccumulator Phytolacca acinosa Roxb. (Phytolaccaceae). Plant Soil 318:197–204CrossRefGoogle Scholar
  62. Zayed J, Hong B, L’esperance G (1999) Characterization of Manganese-Containing Particles Collected from the Exhaust Emissions of Automobiles Running with MMT Additive. Environ Sci Technol 33:3341–3346CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Elizabeth M. Herndon
    • 1
    • 3
    Email author
  • Carmen E. Martínez
    • 2
  • Susan L. Brantley
    • 1
  1. 1.Department of GeosciencesThe Pennsylvania State UniveristyUniversity ParkUSA
  2. 2.Department of Crop and Soil SciencesCornell UniversityIthacaUSA
  3. 3.Department of GeologyKent State UniversityKentUSA

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