Abstract
All restoration strategies to mitigate eutrophication depend on the success of phosphorus (P) removal from the water body. Therefore, the inputs from the watershed and from the enriched sediments, that were the sink of most P that has been discharged in the water body, should be controlled. In sediments, iron (hydr)oxides minerals are potent repositories of P and the release of P into the water column may occur upon dissolution of the iron (hydr)oxides mediated by iron reducing bacteria. Several species of these bacteria are also known as electroactive microorganisms and have been recently identified in lake sediments. This capacity of bacteria to transfer electrons to electrodes, producing electricity from the oxidation of organic matter, might play a role on P release in sediments. In the present work it is discussed the relationship between phosphorus and iron cycling as well as the application of an electrode to work as external electron acceptor in sediments, in order to prevent metal bound P dissolution under anoxic conditions.
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Altmann D, Stief P, Amann R, Beer DD (2004) Distribution and activity of nitrifying bacteria in natural stream sediment versus laboratory sediment microcosms. Aquat Microb Ecol 36:73–81
An J, Kim B, Nam J, Ng HY, Chang IS (2013) Comparison in performance of sediment microbial fuel cells according to depth of embedded anode. Bioresour Technol 127:138–142
Anderson I, Held B, Lapidus A, Nolan M, Lucas S, Tice H, Del Rio TG, Cheng J-F, Han C, Tapia R et al (2012) Genome sequence of the homoacetogenic bacterium Holophaga foetida type strain (TMBS4(T)). Stand Genomic Sci 6(2):174–184
Azzoni R, Giordani G, Viaroli P (2005) Iron–sulphur–phosphorus interactions: implications for sediment buffering capacity in a mediterranean eutrophic lagoon (Sacca di Goro, Italy). Hydrobiologia 550(1):131–148
Babu ML, Mohan SV (2012) Influence of graphite flake addition to sediment on electrogenesis in a sediment-type fuel cell. Bioresour Technol 110:206–213
Bedard DL, Ritalahti KM, Löffler FE (2007) The Dehalococcoides population in sediment-free mixed cultures metabolically dechlorinates the commercial polychlorinated biphenyl mixture Aroclor 1260. Appl Environ Microbiol 73(8):2513–2521
Bennett EM, Carpenter SR, Caraco NF (2001) Human impact on erodable phosphorus and eutrophication: a global perspective. Bioscience 51:227–234
Bond DR, Holmes DE, Tender LM, Lovley DR (2002) Electrode-reducing microorganisms that harvest energy from marine sediments. Science 295:483–485
Bryant MP, Campbell LL, Reddy CA, Crabill MR (1977) Growth of Desulfovibrio in lactate or ethanol media low in sulfate in association with H2-utilizing methanogenic bacteria. Appl Environ Microbiol 33:1162–1169
Burgin AJ, Yang WH, Hamilton SK, Silver WL (2011) Beyond carbon and nitrogen: how the microbial energy economy couples elemental cycles in diverse ecosystems. Front Ecol Environ 9(1):44–52
Caccavo F Jr, Lonergan DJ, Lovley DR, Davis M, Stolz JF, McInerney MJ (1994) Geobacter sulfurreducens sp. nov., a hydrogen- and acetateoxidizing dissimilatory metal-reducing microorganism. Appl Environ Microbiol 60:3752–3759
Canavan RW, Slomp CP, Jourabchi P, Cappellen PV, Laverman AM, Van Den Berg GA (2006) Organic matter mineralization in sediment of a coastal freshwater lake and response to salinization. Geochim Cosmochim Acta 70:2836–2855
Canfield DE, Jorgensen BB, Fossing H, Glud R, Gundersen J, Ramsing NB et al (1993) Pathways of organic-carbon oxidation in 3 continental-margin sediments. Mar Geol 113:27–40. doi:10.1016/0025-3227(93)90147-N
Carpenter SR (2005) Eutrophication of aquatic ecosystems: bistability and soil phosphorus. PNAS 102(29):10002–10005
Chacon N, Silver WL, Dubinsky EA, Cusack DF (2006) Iron reduction and soil phosphorus solubilization in humid tropical forests soils: the roles of labile carbon pools and an electron shuttle compound. Biogeochemistry 78:67–84
Chen G, White PA (2004) The mutagenic hazards of aquatic sediments: a review. Mutat Res 567:151–225
Coates JD, Ellis DJ, Gaw CV, Lovley DR (1999) Geothrix fermentans gen. nov., sp nov., a novel Fe(III)-reducing bacterium from a hydrocarbon-contaminated aquifer. Int J Syst Bacteriol 49:1615–1622
Conley DJ, Paerl HW, Howarth RW, Boesch DF, Seitzinger SP, Havens KE, Lancelot C, Likens GE (2009) Controlling eutrophication: nitrogen and phosphorus. Science 323:1014–1015
Cordell D, Neset TS, Prior T (2012) The phosphorus mass balance: identifying ‘hotspots’ in the food system as a roadmap to phosphorus security. Curr Opin Biotechnol 23:1–7
Cummings DE, Snoeyenbos-West L, Newby DT, Niggemyer AM, Lovley DR, Achenbach LA, Rosenzweig RF (2003) Diversity of geobacteraceae species inhabiting metal polluted freshwater lake sediments ascertained by 16S rDNA analyses. Microb Ecol 46:257–269
Dalsgaard T, Thamdrup B, Canfield DE (2005) Anaerobic ammonium oxidation (anammox) in the marine environment. Res Microbiol 156:457–464
De Schamphelaire L, Boeckx P, Verstraete W (2010) Evaluation of biocathodes in freshwater and brackish sediment microbial fuel cells. Appl Microbiol Biotechnol 87:1675–1687
Donovan C, Dewan A, Heo D, Lewandowski Z, Beyenal H (2013) Sediment microbial fuel cell powering a submersible ultrasonic receiver: new approach to remote monitoring. J Power Sources 233:79–85
Du Z, Li H, Gu T (2007) A state of the art review on microbial fuel cells: a promising technology for wastewater treatment and bioenergy. Biotechnol Adv 25:464–482
Einsele W (1936) Über die beziehungen des eisenkreislaufs zum phosphatkreislauf im eutrophen See. Arch Hydrobiol 29:664–686
European Community (2000) Directive 2000/60/EC of October 23 2000 of the European Parliament and of the Council establishing a framework for community action in the field of water policy. Off J Eur Communities L327:1–72
Fennel K, Brady D, DiToro D, Fulweiler RW, Gardner WS, Giblin A, McCarthy MJ, Rao A, Seitzinger S, Thouvenot-Korppoo M, Tobias C (2009) Modeling denitrification in aquatic sediments. Biogeochemistry 93(1–2):159–178
Ferry JG, Lessner DJ (2008) Methanogenesis in marine sediments. Ann NY Acad Sci 1125:147–157
Fischer F, Bastian C, Happe M, Mabillard E, Schmidt N (2011) Microbial fuel cell enables phosphate recovery from digested sewage sludge as struvite. Bioresour Technol 102:5824–5830
Fu Y, Xu Q, Zai X, Liu Y, Lu Z (2014) Low electrical potential anode modified with Fe/ferric oxide and its application in marine benthic microbial fuel cell with higher voltage and power output. Appl Surf Sci 289:472–477
Gächter R, Müller B (2003) Why the phosphorus retention of lakes does not necessarily depend on the oxygen supply to their sediment surface. Limnol Oceanogr 48(2):929–933
Golterman HL (2001) Phosphate release from anoxic sediments or ‘What did Mortimer really write?’. Hydrobiologia 450(1–3):99–106
Gonsiorczyk T, Casper P, Koschel R (1998) Phosphorus-binding forms in the sediment of an oligotrophic and an eutrophic hardwater lake of the Baltic Lake District (Germany). Water Sci Technol 37(3):51–58
He Z, Shao H, Angenent LT (2007) Increased power production from a sediment microbial fuel cell with a rotating cathode. Biosens Bioelectron 22:3252–3255
Himmelheber DW, Taillefert M, Pennell KD, Hughes JB (2008) Spatial and temporal evolution of biogeochemical processes following in situ capping of contaminated sediments. Environ Sci Technol 42:4113–4120
Himmelheber DW, Thomas SH, Löffler FE, Taillefert M, Hughes JB (2009) Microbial colonization of an in situ sediment cap and correlation to stratified redox zones. Environ Sci Technol 43:66–74
Holmer M, Storkholm P (2001) Sulphate reduction and sulphur cycling in lake sediments: a review. Freshw Biol 46:431–451
Holmes DE, Bond DR, O’Neil RA, Reimers CE, Tender LR, Lovley DR (2004) Microbial communities associated with electrodes harvesting electricity from a variety of aquatic sediments. Microb Ecol 48:178–190
Hong SW, Chang IS, Choi YS, Kim BH, Chung TH (2009) Responses from freshwater sediment during electricity generation using microbial fuel cells. Bioprocess Biosyst Eng 32:389–395
Hsu L, Chadwick B, Kagan J, Thacher R, Wotawa-Bergen A, Richter K (2013) Scale up considerations for sediment microbial fuel cells. RSC Adv 3:15947–15954
Huettel M, Røy H, Precht E, Ehrenhauss S (2003) Hydrodynamical impact on biogeochemical processes in aquatic sediments. Hydrobiologia 494:231–236
Hupfer M, Lewandowski J (2008) Oxygen controls the phosphorus release from lake sediments—a long-lasting paradigm in limnology. Int Rev Hydrobiol 93(4–5):415–432
Jeppesen E, Søndergaard M, Jensen JP, Havens K, Anneville O, Carvalho L, Coveney MF et al (2005) Lake responses to reduced nutrient loading—an analysis of contemporary long-term data from 35 case studies. Freshw Biol 50:1747–1771
Kemp WM, Sampou P, Caffrey J, Mayer M (1990) Ammonium recycling versus denitrification in Chesapeake Bay sediment. Limnol Oceanogr 35(7):1545–1563
Khoshmanesh A, Hart BT, Duncan A, Beckett R (2002) Luxury uptake of phosphorus by sediment bacteria. Water Res 36:774–778
Klueglein N, Lsekann-Behrens T, Obst M, Behrens S, Appel E, Kappler A (2013) Magnetite formation by the novel Fe(III)-reducing Geothrix fermentans Strain HradG1 isolated from a hydrocarbon-contaminated sediment with increased magnetic susceptibility. Geomicrobiol J 30(10):863–873
Lehtoranta J (2004) Benthic phosphorus release from sediment to water. In: Wassmann P, Olli K (eds) Drainage basin nutrient inputs and eutrophication: an integrated approach. University of Tromsø, Norway, pp 155–166
Lentini CJ, Wankel SD, Hansel CM (2012) Enriched iron(III)-reducing bacterial communities are shaped by carbon substrate and iron oxide mineralogy. Front Microbiol 3:404
Li H, Peng J, Weber K, Zhu Y (2011) Phylogenetic diversity of Fe(III)-reducing microorganisms in rice paddy soil: enrichment cultures with different short-chain fatty acids as electron donors. J Soils Sediments 11(7):1234–1242
Lin B, Hyacinthe C, Bonneville S, Braster M, Van Cappellen P, Röling WFM (2007) Phylogenetic and physiological diversity of dissimilatory ferric iron reducers in sediments of the polluted Scheldt estuary, Northwest Europe. Environ Microbiol 9(8):1956–1968
Logan BE (2008) Microbial fuel cells. Wiley, Hoboken
Logan B, Murano C, Scott K, Gray ND, Head IM (2005) Electricity generation from cysteine in a microbial fuel cell. Water Res 39:942–952
Logan BE, Hamelers B, Rozendal R, Schroder U, Keller J, Freguia S, Aelterman P, Verstraete W, Rabaey K (2006) Microbial fuel cells: methodology and technology. Environ Sci Technol 40:5181–5192
Logan BE, Cheng S, Watson V, Estadt G (2007) Graphite fiber brush anodes for increased power production in air–cathode microbial fuel cells. Environ Sci Technol 41(9):3341–3346
Lovley DR, Phillips EJP (1987) Rapid assay for reducible ferric iron in aquatic sediments. Appl Environ Microbiol 53:1536–1540
Lovley DR, Phillips EJP (1988) Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl Environ Microbiol 54:1472–1480
Lovley DR, Stolz JF, Nord GL Jr, Phillips EJP (1987) Anaerobic production of magnetite by a dissimilatory iron-reducing microorganism. Nature 330(6145):252–254
Lovley DR, Holmes DE, Nevin KP (2004) Dissimilatory Fe(III) and Mn(IV) reduction. Adv Microb Physiol 49:219–286
Lowy DA, Tender LM, Zeikus JG, Park DH, Lovely DR (2006) Harvesting energy from the marine sediment–water interface II: kinetic activity of anode materials. Biosens Bioelectron 21:2058–2063
Martins G, Ribeiro DC, Pacheco D, Cruz JV, Cunha R, Gonçalves V, Nogueira R, Brito AG (2008) Prospective scenarios for water quality and ecological status in Lake Sete Cidades (Portugal): the integration of mathematical modelling in decision processes. Appl Geochem 23:2171–2181
Martins G, Peixoto L, Ribeiro DC, Parpot P, Brito AG, Nogueira R (2010) Towards Benthic microbial fuel cell implementation in volcanic eutrophic lakes: bacterial electrochemical activity assessment in Lake Furnas (Azores)—Portugal. Bioelectrochemistry 78:67–71
Martins G, Terada A, Ribeiro DC, Corral AM, Brito AG, Smets BF, Nogueira R (2011) Structure and activity of lacustrine sediment bacteria involved in nutrient and iron cycles. FEMS Microbiol Ecol 77:666–679
Martins G, Henriques I, Ribeiro DC, Correia A, Bodelier PLE, Cruz JV, Brito AG, Nogueira R (2012) Bacterial diversity and geochemical profiles in sediments from eutrophic Azorean lakes. Geomicrobiol J 29(8):704–715
Martins G, Brito AG, Nogueira R, Ureña M, Fernández D, Luque FJ, Alcácer C (2013) Water resources management in southern Europe: clues for a research and innovation based regional hypercluster. J Environ Manage 119:76–84
Martins G, Peixoto L, Teodorescu S, Parpot P, Nogueira R, Brito AG (2014) Impact of an external electron acceptor on phosphorus mobility between water and sediments. Bioresour Technol 151:419–423
Mortimer CH (1941) The exchange of dissolved substances between mud and water in lakes. J Ecol 29:280–329
Mortimer CH (1942) The exchange of dissolved substances between mud and water in lakes. J Ecol 30:147–201
Muyzer G, Stams AJ (2008) The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev Microbiol 6(6):441–454
Nealson KH (1997) Sediment bacteria: who’s there, what are they doing, and what’s new? Annu Rev Earth Planet Sci 25:403–434
Nielsen LP, Risgaard-Petersen N, Fossing H, Christensen PB, Sayama M (2010) Electric currents couple spatially separated biogeochemical processes in marine sediment. Nature 463:1071–1075
Petrie L, North NN, Dollhopf SL, Balkwill DL, Kostka JE (2003) Enumeration and characterization of iron(III)-reducing microbial communities from acidic subsurface sediments contaminated with uranium(VI). Appl Environ Microbiol 69(12):7467–7479
Pettersson K (2001) Phosphorus characteristics of settling and suspended particles in Lake Erken. Sci Tot Environ 266:79–86
Pretty JN, Mason CF, Nedwell DB, Hine RE, Leaf S, Dils R (2003) Environmental costs of freshwater eutrophication in England and Wales. Environ Sci Technol 37(2):201–208
Rabaey K, Lissens G, Verstraete W (2005) Microbial fuel cells: performances and perspectives. In: Lens PN, Westermann P, Haberbauer M, Moreno A (eds) Biofuels for fuel cells: biomass fermentation towards usage in fuel cells. IWA, London, pp 377–399
Raghoebarsing AA, Pol A, Van De Pas-Schoonen KT, Smolders AJP, Ettwig KF, Rijpstra WIC, Schouten S, Damste JSS, Op Den Camp HJM, Jetten MSM, Strous M (2006) A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 440:918–921
Reimers CE, Tender LM, Fertig S, Wang W (2001) Harvesting energy from the marine water interface. Environ Sci Technol 35:192–195
Reimers CE, Girguis P, Stecher HA III, Tender LM, Ryckelynck N, Whaling P (2006) Microbial fuel cell energy from an ocean cold seep. Geobiology 4:123–136
Rezaei F, Richard TL, Logan BE (2008) Enzymatic hydrolysis of cellulose coupled with electricity generation in a microbial fuel cell. Biotechnol Bioeng 101:1163–1169
Ribeiro DC, Martins G, Nogueira R, Cruz JV, Brito AG (2008) Phosphorus fractionation in volcanic lake sediments (Azores—Portugal). Chemosphere 70:1256–1263
Roden EE, Zachara JM (1996) Microbial reduction of crystalline iron(III) oxides: influence of oxide surface area and potential for cell growth. Environ Sci Technol 30:1618–1628
Rozan TF, Taillefert M, Trouwborst RE, Glazer BT, Ma S, Herszage J, Valdes LM, Price KS, Luther GW III (2002) Iron–sulphur–phosphorus cycling in the sediments of a shallow coastal bay: implications for sediment nutrient release and benthic macroalgal blooms. Limnol Oceanogr 47:1346–1354
Selman M, Greenhalgh S (2009) Eutrophication: sources and drivers of nutrient pollution. World Resources Institute policy note, water quality: eutrophication and hypoxia no 2
Søndergaard M, Jensen JP, Jeppesen E (2003) Role of sediment and internal loading of phosphorus in shallow lakes. Hydrobiologia 506–509:135–145
Søndergaard M, Jeppesen E, Lauridsen TL, Skov C, Van Nes EH, Roijackers R, Lammens E, Portielje R (2007) Lake restoration: successes, failures and long-term effects. J Appl Ecol 44:1095–1105
Song TS, Yan ZS, Zhao ZW, Jiang HL (2010) Removal of organic matter in freshwater sediment by microbial fuel cells at various external resistances. J Chem Technol Biotechnol 85:1489–1493
Song T, Tan W, Wu X, Zhou CC (2012) Effect of graphite felt and activated carbon fiber felt on performance of freshwater sediment microbial fuel cell. J Chem Technol Biotechnol 87:1436–1440
Stein LY, La Duc MT, Grundl TJ, Nealson KH (2001) Bacterial and archaeal populations associated with freshwater ferromanganous micronodules and sediments. Environ Microbiol 3:10–18
Stockdale A, Davison W, Zhang H (2009) Micro-scale biogeochemical heterogeneity in sediments: a review of available technology and observed evidence. Earth Sci Rev 92:81–97
Tender LM, Reimers CE, Stecher HA, Holmes DE, Bond DR, Lowy DA, Pilobello K, Fertig SJ, Lovley DR (2002) Harnessing microbially generated power on the seafloor. Nat Biotechnol 20:821–825
Tender LM, Gray SA, Groveman E, Lowy DA, Kauffman P, Melhado J, Tyce RC, Flynn D, Petrecca R, Dobarro J (2008) The first demonstration of a microbial fuel cell as a viable power supply: powering a meteorological buoy. J Power Sources 179:571–575
Thamdrup B (2000) Bacterial manganese and iron reduction in aquatic sediments. In: Schink B (ed) Advances in microbial ecology, vol 16. Kluwer Academic/Plenum Publications, New York, pp 41–84
Thamdrup B, Dalsgaard T (2002) Production of N2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl Environ Microbiol 68:1312–1318
Thomsen U, Thamdrup B, Stahl DA, Canfield DE (2004) Pathways of organic carbon oxidation in a deep lacustrine sediment, Lake Michigan. Limnol Oceanogr 49(6):2046–2057
United Nations Environment Programme (UNEP) (2012) http://www.unep.or.jp/ietc/publications/short_series/lakereservoirs-3/2.asp. Accessed 26 Sept 2012
Venkata Mohan S, Srikanth S, Veer Raghuvulu S, Mohanakrishna G, Kiran Kumar A, Sarma PN (2008) Evaluation of various types of aquatic eco-system potential in harnessing bioelectricity through benthic fuel cell: effect of water characteristics and electrode assembly. Bioresource Technol. doi:10.1016/j.biortech.2008.10.020
Wetzel RG (1983) Limnology, 2nd edn. Saunders College Publishing, Philadelphia
Wobus A, Bleul C, Maassen S, Scheerer C, Schuppler M, Jacobs E, Röske I (2003) Microbial diversity and functional characterization of sediments from reservoirs of different trophic state. FEMS Microbiol Ecol 46:331–347
Zhou YL, Yang Y, Chen M, Zhao ZW, Jiang HL (2014) To improve the performance of sediment microbial fuel cell through amending colloidal iron oxyhydroxide into freshwater sediments. Bioresour Technol 159:232–239
Acknowledgments
The authors are grateful to two anonymous reviewers of a previous version of the manuscript for the constructive comments and suggestions. The authors also acknowledge the Grant SFRH/BPD/80528/2011 from the Foundation for Science and Technology, Portugal, awarded to Gilberto Martins.
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Martins, G., Peixoto, L., Brito, A.G. et al. Phosphorus–iron interaction in sediments: can an electrode minimize phosphorus release from sediments?. Rev Environ Sci Biotechnol 13, 265–275 (2014). https://doi.org/10.1007/s11157-014-9343-5
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DOI: https://doi.org/10.1007/s11157-014-9343-5