Abstract
Purpose
Deposits of iron–manganese (Fe, Mn) concretions forming a large storage of phosphorus (P) and arsenic (As) are frequently under pressure of oscillating oxygen conditions in the eutrophic Gulf of Finland, the Baltic Sea. Yet, there is a poor understanding how anaerobic microbial processes regulate the cycling of elements in the concretions. The objective of this study was to highlight how the microbial processes control the release of elements from the concretions to brackish water during anoxia.
Materials and methods
Spherical concretions were collected from the oxic bottoms of the Gulf of Finland in the summer. Concretions and autoclaved controls were incubated in anoxic artificial brackish seawater with and without labile carbon, plus supplied with ammonium at 5, 10, and 20 °C for 15 weeks. Concentrations of Fe, Mn, P, and As were measured from the intact concretions and the ambient solutions during the experiment. Also, the consumption of the added ammonium and organic carbon and the formation of dissolved inorganic carbon were measured.
Results and discussion
At near-bottom temperature 5 °C, the concretions released at highest 0.12, 0.42, 0.02, and 0.0002 μmol g−1 day−1 of Fe, Mn, P, and As, respectively. The rates were significant only in the microcosms with added labile carbon, and only minor proportions (0.1–0.4 %) of their total contents were released during the incubations. The concretions removed completely the supplied ammonium only without carbon addition. We find that concretion deposit may form a local hot spot for the microbial reduction of Fe and Mn and release significant amounts of P and As, and participate in N cycling besides the bottom sediments of the Gulf of Finland during prolonged anoxia. However, the concretions may maintain their binding capacity for P and As longer than the fine-grained organic-rich sediment during anoxia.
Conclusions
During anoxia concretion deposits may form a temporal source of bioavailable P having ecological significance in the Gulf of Finland when concretions have access to labile organic carbon. Concretions from the Baltic Sea, the oceans, lakes, and soils contain high concentrations of Mn and Fe, but their proportions vary considerably. Anaerobic microbial processes may thus affect the stability of concretions from the different environments, but the outcome may depend on the ambient geochemical conditions.
Similar content being viewed by others
References
Ahmann D, Krumholz LR, Hemond HF, Lovley DR, Morel FMM (1997) Microbial mobilization of arsenic from sediments of the Aberjona Watershed. Environ Sci Technol 31:2923–2930
Akerman NH, Price RE, Pichler T, Amend JP (2011) Energy sources for chemolithotrophs in an arsenic- and iron-rich shallow-sea hydrothermal system. Geobiology 9:436–445
Anderson CF, Cook GM (2004) Isolation and characterization of arsenate-reducing bacteria from arsenic-contaminated sites in New Zealand. Curr Microbiol 48:341–347
Anufriev GS, Boltenkov BS (2007) Ferromanganese nodules of the Baltic Sea: composition, helium isotopes, and growth rate. Lithol Miner Resour 42:240–245
Anufriev GS, Blinov LN, Boltenkov BS, Arif M (2005) Chemical and isotope composition of Baltic iron–manganese concretions. Tech Phys 5:663–665
Arif M, Blinov LN (2004) Investigation of concretions from the Baltic Sea. Glass Phys Chem 30:359–361
Arshad MA, Arnaud RJ (1980) Occurrence and characteristics of ferromanganiferous concretions in some Saskatchewan soils. Can J Soil Sci 60:685–695
Bartlett R, Mortimer RJG, Morris KM (2007) The biogeochemistry of a manganese-rich Scottish sea loch: implications for the study of anoxic nitrification. Cont Shelf Res 27:1501–1509
Baturin GN (2009) Geochemistry of ferromanganese nodules in the Gulf of Finland, Baltic Sea. Lithol Miner Resour 44:411–426
Baturin GN, Dubinchuk VT (2009) Composition of ferromanganese nodules from Riga Bay (Baltic Sea). Oceanology 49:111–120
Bischoff JL, Piper DZ, Leong K (1981) The aluminosilicate fraction of North Pacific manganese nodules. Geochim Cosmochim Ac 45:2047–2063
Blomqvist S, Larsson U (1994) Detrital bedrock elements as tracers of settling resuspended particulate matter in a coastal area of the Baltic Sea. Limnol Oceanogr 39:880–896
Bock B, Liebetrau V, Eisenhauer A, Frei R, Leipe T (2005) Nd isotope signature of holocene Baltic Mn/Fe precipitates as monitor of climate change during the Little Ice Age. Geochim Cosmochim Ac 69:2253–2263
Canfield DE, Thamdrup B (2009) Towards a consistent classification scheme for geochemical environments, or, why we wish the term ‘suboxic’ would go away. Geobiology 7:385–392
Canfield DE, Thamdrup B, Hansen JW (1993) The anaerobic degradation of organic matter in Danish coastal sediments: iron reduction, manganese reduction, and sulfate reduction. Geochim Cosmochim Ac 57:3867–3883
Canfield DE, Thamdrup B, Kristensen E (2005) Advances in marine biology. Aquatic geomicrobiology. Elsevier Academic Press, ISBN 0–12–026147–2, 636 pp
Chen Z, Kim K-W, Zhu Y-G, McLaren R, Liu F, He J-Z (2006) Adsorption (AsIII,V) and oxidation (AsIII) of arsenic by pedogenic Fe–Mn nodules. Geoderma 136:566–572
Ehrlich HL (1968) Bacteriology of manganese nodules II. Manganese oxidation by cell-free extract from a manganese nodule bacterium. Appl Microbiol 16:197–202
Eusterhues K, Rennert T, Knicker H, Kogel-Knabner I, Totsche KU, Schwertmann U (2011) Fractionation of organic matter due to reaction with ferrihydrite: coprecipitation versus adsorption. Environ Sci Technol 45:527–533
Farquhar ML, Charnock JM, Livens FR, Vaughan DJ (2002) Mechanisms of arsenic uptake from aqueous solution by interaction with goethite, lepidocrocite, mackinawite, and pyrite: an X-ray absorption spectroscopy study. Environ Sci Technol 36:1757–1762
Gasparatos D, Tarenidis D, Haidouti C, Oikonomou G (2005) Microscopic structure of soil Fe–Mn nodules: environmental implication. Environ Chem Lett 2:175–178
Ghiorse WC, Hirsch P (1982) Isolation and properties of ferromanganese-depositing budding bacteria from Baltic sea ferromanganese concretions. Appl Environ Microb 43:1464–1472
Glasby GP (1973) Mechanisms of enrichment of rarer elements in marine manganese nodules. Mar Chem 1:105–125
Glasby GP, Stoffers P, Sioulas A, Thijssen T, Friedrich G (1982) Manganese nodule formation in the Pacific Ocean: a general theory. Geo Mar Lett 2:47–53
Glasby GP, Emelyanov EM, Zhamoida VA, Baturin GN, Leipe T, Bahlo R, Bonacker P (1997) Environments of formation of ferromanganese concretions in the Baltic sea: a critical review. In: Nicholson K, Hein JR, Bühn B, Dasgupta S (eds) Manganese mineralization: geochemistry and mineralogy of terrestrial and marine deposits. Geol Soc Spec Pub 119:213–237
Golterman HL (1995) The role of the iron hydroxide–phosphate–sulphide system in the phosphate exchange between sediments and overlying water. Hydrobiologia 297:43–54
Grigoriev AG, Zhamoida VA, Gruzdov KA, Krymsky Grigoriev RS (2013) Age and growth rates of ferromanganese concretions from the Gulf of Finland derived from 210Pb measurements. Oceanology 53:345–351
Gunnars A, Blomqvist S (1997) Phosphate exchange across the sediment–water interface when shifting from anoxic to oxic conditions—an experimental comparison of freshwater and brackish–marine systems. Biogeochemistry 37:203–226
Gunnars A, Blomqvist S, Johansson P, Andersson C (2002) Formation of Fe(III) oxyhydroxide colloids in freshwater and brackish seawater, with incorporation of phosphate and calcium. Geochim Cosmochim Ac 66:745–758
Haahti H, Kangas P (2006) State of the Gulf of Finland in 2004. MERI– Report series of the Finnish Institute of Marine Research. No 55. Helsinki, Finland
Hansson M, Andersson L, Axe P (2011) Areal extent and volume of anoxia and hypoxia in the Baltic Sea, 1960–2011. SMHI Swedish Meteorological and Hydrological Institute, Report Oceanography No. 42, Norrköping, Sweden, 76 pp
He J, Zhang L, Jin S, Zhu Y (2008) Bacterial communities inside and surrounding soil iron–manganese nodules. Geomicrobiol J 25:14–24
Heiskanen AS, Leppänen JM (1995) Estimation of export production in the coastal Baltic Sea: effect of resuspension and microbial decomposition on sedimentation measurements. Hydrobiologia 316:211–224
Hulth S, Aller RC, Gilbert F (1999) Coupled anoxic nitrification/manganese reduction in marine sediments. Geochim Cosmochim Ac 63:49–66
Ingri J (1985) Geochemistry of ferromanganese concretions and associated sediments in the Gulf of Finland. Dissertation. Luleå, Sweden: University of Technology
Jensen HS, Mortensen PB, Andersen FØ, Rasmussen E, Jensen A (1995) Phosphorus cycling in a coastal marine sediment, Aarhus Bay, Denmark. Limnol Oceanogr 40:908–917
Jetten MSM, Strous M, van de Pas-Schoonen KT, Schalk J, van Dongen UGJM, van de Graaf AA, Logemann S, Muyzer G, van Loosdrecht MCM, Kuenen JG (1999) The anaerobic oxidation of ammonium. FEMS Microbiol Rev 22:421–437
Jilbert T, Slomp CP (2013) Iron and manganese shuttles control the formation of authigenic phosphorus minerals in the euxinic basins of the Baltic Sea. Geochim Cosmochim Ac 107:155–169
Jilbert T, Slomp CP, Gustafsson BG, Boer W (2011) Beyond the Fe–P–redox connection: preferential regeneration of phosphorus from organic matter as a key control on Baltic Sea nutrient cycles. Biogeosciences 8:1699–1720
Kankaanpää H, Korhonen M, Heiskanen A-S, Suortti A-M (1997) Seasonal sedimentation of organic matter and contaminants in the Gulf of Finland. Boreal Environ Res 2:257–274
Kersten M, Kulik DA (2005) Competitive scavenging of trace metals by HFO and HMO during redox-driven early diagenesis of ferromanganese nodules. J Soils Sediments 5:37–47
Knoblauch C, Jørgensen BB (1999) Effect of temperature on sulphate reduction, growth rate and growth yield in five psychrophilic sulphate-reducing bacteria from Arctic sediments. Environ Microbiol 1:457–467
Kristiansen KD, Kristensen E, Jensen MH (2002) The influence of water column hypoxia on the behaviour of manganese and iron in sandy coastal marine sediment. Estuar Coast Shelf Sci 55:645–654
Lehtoranta J (2003) Dynamics of sediment phosphorus in the brackish Gulf of Finland. Monograph Boreal Environ Res 24. ISBN 952–11–1400–2
Lehtoranta J, Heiskanen A-S (2003) Dissolved iron:phosphate ratio as an indicator of phosphate release to oxic water of the inner and outer coastal Baltic Sea. Hydrobiologia 492:69–84
Lehtoranta J, Pitkänen H (2003) Binding of phosphate in sediment accumulation areas of the eastern Gulf of Finland, Baltic Sea. Hydrobiologia 492:55–67
Lehtoranta J, Heiskanen A-S, Pitkänen H (2004) Particulate N and P characterizing the fate of nutrients along the estuarine gradient of the River Neva (Baltic Sea). Estuar Coast Shelf Sci 61:275–287
Leivuori M (1998) Heavy metal contamination in surface sediments in the Gulf of Finland and comparison with the Gulf of Bothnia. Chemosphere 36:43–59
Leivuori M, Niemistö L (1993) Trace metals in the sediments of the Gulf of Bothnia. Aqua Fennica 23:89–100
Leivuori M, Niemistö L (1995) Sedimentation of trace metals in the Gulf of Bothnia. Chemosphere 31:3839–3856
Leivuori M, Vallius H (1998) A case study of seasonal variation in the chemical compositions of accumulating suspended sediments in the central Gulf of Finland. Chemosphere 36:2417–2435
Leivuori M, Jokšas K, Seisuma Z, Petersell V, Larsen B, Pedersen B, Floderus S (2000) Distribution of heavy metals in sediments of the Gulf of Riga, the Baltic Sea. Boreal Environ Res 5:165–185
Leppäranta M, Myrberg K (2009) Physical oceanography of the Baltic Sea. Springer–Praxis books in geophysical sciences. ISBN 978–3–540–79702–9
Lovley DR (1991) Dissimilatory Fe(III) and Mn(IV) reduction. Microbiol Rev 55:259–287
Lovley DR, Phillips EJP (1987) Competitive mechanisms for inhibition of sulfate reduction and methane production in the zone of ferric iron reduction in sediments. Appl Environ Microb 53:2636–2641
Lovley DR, Phillips EJP (1988a) Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl Environ Microb 54:1472–1480
Lovley DR, Phillips EJP (1988b) Manganese inhibition of microbial iron reduction in anaerobic sediments. Geomicrobiol J 6:145–155
Lukkari K, Leivuori M, Kotilainen A (2009a) The chemical character and behaviour of phosphorus in poorly oxygenated sediments from open sea to organic-rich inner bay in the Baltic Sea. Biogeochemistry 96:25–48
Lukkari K, Leivuori M, Vallius H, Kotilainen A (2009b) The chemical character and burial of phosphorus in shallow coastal sediments in the northeastern Baltic Sea. Biogeochemistry 94:141–162
Mackin JE, Aller RC (1984) Ammonium adsorption in marine sediments. Limnol Oceanogr 29:250–257
Marcus MA, Manceau A, Kersten M (2004) Mn, Fe, Zn and As speciation in a fast-growing ferromanganese marine nodule. Geochim Cosmochim Ac 68:3125–3136
Martin AJ, Pedersen TF (2002) Seasonal and interannual mobility of arsenic in a lake impacted by metal mining. Environ Sci Technol 36:1516–1523
McKnight DM, Bencala KE, Zellweger GW, Aiken GR, Feder GL, Thorn KA (1992) Sorption of dissolved organic carbon by hydrous aluminum and iron oxides occurring at the confluence of Deer Creek with the Snake River, Summit County, Colorado. Environ Sci Technol 26:1388–1396
Mort HP, Slomp CP, Gustafsson BG, Andersen TJ (2010) Phosphorus recycling and burial in Baltic Sea sediments with contrasting redox conditions. Geochim Cosmochim Ac 74:1350–1362
Müller B, Granina L, Schaller T, Ulrich A, Wehrli B (2002) P, As, Sb, Mo, and other elements in sedimentary Fe/Mn layers of Lake Baikal. Environ Sci Technol 36:411–420
Myers CR, Nealson KH (1988) Microbial reduction of manganese oxides: interactions with iron and sulphur. Geochim Cosmochim Ac 52:2727–2732
Neidhardt H, Berner ZA, Freikowski D, Biswas A, Majumder S, Winter J, Gallert C, Chatterjee D, Norra S (2014) Organic carbon induced mobilization of iron and manganese in a West Bengal aquifer and muted response of groundwater arsenic concentrations. Chem Geol 367:51–62
Oscarsson DW, Huang PM, Hammer VT (1983) Oxidation and sorption of arsenite by manganese dioxide as influenced by surface coatings of iron and aluminium oxides and calcium carbonate. Water Air Soil Poll 20:233–244
Pakhomova SV, Hall POJ, Kononets MY, Rozanov AG, Tengberg A, Vershinin AV (2007) Fluxes of iron and manganese across the sediment–water interface under various redox conditions. Mar Chem 197:319–331
Pitkänen H, Lehtoranta J, Räike A (2001) Internal nutrient fluxes counteract decreases in external load: the case of the estuarial eastern Gulf of Finland, Baltic Sea. Ambio 30:195–201
Pitkänen H, Lehtoranta J, Peltonen H, Laine A, Kotta J, Kotta I, Moskalento P, Mäkinen A et al (2003) Benthic release of phosphorus and its relation to environmental conditions in the estuarial Gulf of Finland, Baltic Sea in the early 2000s. Proc Eston Acad Sci Biol Ecol 52:173–193
Plugge CM (2005) Anoxic media design, preparation and considerations. Method Enzymol 397:3–16
Postma D, Appelo CAJ (2000) Reduction of Mn-oxides by ferrous iron in a flow system: column experiment and reactive transport modelling. Geochim Cosmochim Ac 64:1237–1247
Riedel GF, Sanders JG, Osman RW (1999) Biogeochemical control on the flux of trace elements from estuarine sediments: effects of seasonal and short-term hypoxia. Mar Environ Res 47:349–372
Riedel T, Zak D, Biester H, Dittmar T (2013) Iron traps terrestrially derived dissolved organic matter at redox interfaces. Proc Natl Acad Sci U S A 110:10101–10105
Roden EE, Edmonds JW (1997) Phosphate mobilization in iron-rich anaerobic sediments: microbial Fe(III) oxide reduction versus iron–sulfide formation. Arch Hydrobiol 39:347–378
Roden EE, Urrutia MM, Mann CJ (2000) Bacterial reductive dissolution of crystalline Fe(III) oxide in continuous–flow column reactors. Appl Environ Microbiol 3:1062–1065
Rona P, Lenoble J (2004) Marine mineral resources: scientific advances and economic perspectives. United Nations Division for Ocean Affairs and the Law of the Sea, Office of Legal Affairs, and the International Seabed Authority 62
Rydin E, Malmaeus JM, Karlsson OM, Jonsson P (2011) Phosphorus release from coastal Baltic Sea sediments as estimated from sediment profiles. Estuar Coast Shelf Sci 92:111–117
Savchuk OP (2000) Studies of the assimilation capacity and effects of nutrient load reductions in the eastern Gulf of Finland with geochemical model. Boreal Environ Res 5:147–163
Sharma P, Ofner J, Kappler A (2010) Formation of binary and ternary colloids and dissolved complexes of organic matter, Fe and As. Environ Sci Technol 44:4479–4485
Slomp CP, Mort HP, Jilbert T, Reed DC, Gustafsson BG, Wolthers M (2013) Coupled dynamics of iron and phosphorus in sediments of an oligotrophic coastal basin and the impact of anaerobic oxidation of methane. PLOS One 8:e62386. doi:10.1371/journal.pone.0062386
Stookey LL (1970) Ferrozine—a new spectrophotometric reagent for Iron. Anal Chem 42:779–781
Suess E, Djafari D (1977) Trace metal distribution in Baltic Sea ferromanganese concretions: inferences on accretion rates. Earth Planet Sc Lett 35:49–54
Szymanski W, Skiba M (2013) Distribution, morphology, and chemical composition of Fe–Mn nodules in albeluvisols of the Carpathian Foothills, Poland. Pedosphere 23:445–454
Tan W-F, Liu F, Li Y-H, Hu H-Q, Huang Q-Y (2006) Elemental composition and geochemical characteristics of iron–manganese nodules in main soils of China. Pedosphere 16:72–81
Tebo BM, Emerson S (1986) Microbial manganese(II) oxidation in the marine environment: a quantitative study. Biogeochemistry 2:149–161
Thamdrup B, Dalsgaard T (2000) The fate of ammonium in anoxic manganese oxide-rich marine sediment. Geochim Cosmochim Ac 64:4157–4164
Thamdrup B, Rosselló-Mora R, Amann R (2000) Microbial manganese and sulfate reduction in Black Sea shelf sediments. Appl Environ Microb 66:2888–2897
Tuominen L, Kairesalo T, Hartikainen H (1994) Comparison of methods for inhibiting bacterial activity in sediment. Appl Environ Microb 60:3454–3457
Vallius H (2012) Arsenic and heavy metal distribution in the bottom sediments of the Gulf of Finland through the last decades. Baltica 25:23–32
Vallius H, Leivuori M (1999) The distribution of heavy metals and arsenic in recent sediments in the Gulf of Finland. Boreal Environ Res 4:19–29
Vallius H, Ryabchuk D, Kotilainen A (2007) Distribution of heavy metals and arsenic in soft surface sediments of the coastal area off Kotka, Northeastern Gulf of Finland, Baltic Sea. In: Vallius H (ed) Holocene sedimentary environment and sediment geochemistry of the Eastern Gulf of Finland, Baltic Sea. Geol Surv Finland, Special Paper 45:33–48
Vallius H, Zhamoida V, Kotilainen A, Ryabchuk D (2011) Seafloor desertification—a future scenario for the Gulf of Finland? Central and Eastern European Development Studies 365–372. doi:10.1007/978–3–642–17220–5_17
Viktorsson L, Almroth-Rosell E, Tengberg A, Vankevich R, Neelov I, Isaev A, Kravtsov V, Hall POJ (2012) Benthic phosphorus dynamics in the Gulf of Finland, Baltic Sea. Aquat Geochem 18:543–564
Viktorsson L, Ekeroth N, Nilsson M, Kononets M, Hall POJ (2013) Phosphorus recycling in sediments of the central Baltic Sea. Biogeosciences 10:3901–3916
Virtasalo J, Kotilainen AT (2008) Phosphorus forms and reactive iron in lateglacial, postglacial and brackish–water sediments of the Archipelago Sea, northern Baltic Sea. Mar Geol 252:1–12
Virtasalo J, Kohonen T, Vuorinen I, Huttula T (2005) Sea bottom anoxia in the Archipelago Sea, northern Baltic Sea—implications for phosphorus remineralization at the sediment surface. Mar Geol 224:103–122
Winterhalter B (1966) Pohjanlahden ja Suomenlahden rauta-mangaani-saostumista (Ferromanganese concretions of the Gulf of Bothnia and the Gulf of Finland). Geoteknillisiä julkaisuja N:o 69 (in Finnish)
Wu Y-H, Liao L, Wang C-S, Ma W-L, Meng F-X, Wu M, Xu X-W (2013) A comparison of microbial communities in deep-sea polymetallic nodules and the surrounding sediments in the Pacific Ocean. Deep Sea Res I 79:40–49
Yli-Hemminki P, Jørgensen KS, Lehtoranta J (2014) Iron–manganese concretions sustaining microbial life in the Baltic Sea: the structure of the bacterial community and enrichments in metal-oxidizing conditions. Geomicrobiol J 31:263–275
Zhamoida V, Grigoriev A, Gruzdov K, Ryabchuk D (2007) The influence of ferromanganese concretions-forming processes in the eastern Gulf of Finland on the marine environment. In: Vallius H (ed) Holocene sedimentary environment and sediment geochemistry of the Eastern Gulf of Finland, Baltic Sea. Geological Survey of Finland, Special Paper 45:21–31
Zhang F-S, Lin C-Y, Bian L-Z, Glasby GP, Zhamoida VA (2002) Possible evidence for the biogenic formation of spheroidal ferromanganese concretions from the eastern Gulf of Finland, the Baltic Sea. Baltica 15:23–29
Zhang G, Liu F, Liu H, Qu J, Liu R (2014) Respective role of Fe and Mn oxide contents for arsenic sorption in iron and manganese binary oxide: an X-ray absorption spectroscopy investigation. Environ Sci Technol 48:10316–10322
Acknowledgments
This work was financially supported by the Maj and Tor Nessling Foundation, K.H. Renlund Foundation and Maa- ja vesitekniikan tuki ry. The authors wish to thank Suvi Tyynelä for her contribution to the laboratory work, and R/V Muikku and Anna Downey for the sampling of concretions.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible editor: Nives Ogrinc
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 20 kb)
Rights and permissions
About this article
Cite this article
Yli-Hemminki, P., Sara-Aho, T., Jørgensen, K.S. et al. Iron–manganese concretions contribute to benthic release of phosphorus and arsenic in anoxic conditions in the Baltic Sea. J Soils Sediments 16, 2138–2152 (2016). https://doi.org/10.1007/s11368-016-1426-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11368-016-1426-1