Dominance of sulfur-fueled iron oxide reduction in low-sulfate freshwater sediments

ISME Journal

Volumn 9, Issue 11, 2015, Pages 2400-2412

  Hansel, Colleen M ^a   Lentini, Chris J ^b   Tang, Yuanzhi ^c   Johnston, David T ^d   Wankel, Scott D ^a   Jardine, Philip M ^e  

^a WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^b HARVARD UNIVERSITY   (United States)

^c GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^d HARVARD UNIVERSITY   (United States)

^e NONE

Author keywords

[No Author keywords available]

Indexed keywords

BIOGEOCHEMISTRY; DOMINANCE; FERMENTATION; FRESHWATER SEDIMENT; IRON OXIDE; NUTRIENT CYCLING; REDOX CONDITIONS; REDUCTION; RESPIRATION; SUBSTRATE; SULFATE; SULFUR;

FERRIC HYDROXIDE; FERRIC ION; FERRIC OXIDE; FERRIC OXYHYDROXIDE; FRESH WATER; GAS; IRON; IRON DERIVATIVE; MINERAL; OXIDE; RNA 16S; SULFATE; SULFIDE; SULFUR; SULFUR DERIVATIVE; SULFUR MONOXIDE;

CHEMISTRY; DESULFOVIBRIO; GAS; GENETICS; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION; OXYGEN CONSUMPTION; SEDIMENT; THERMODYNAMICS;

DESULFOVIBRIO; FERRIC COMPOUNDS; FRESH WATER; GASES; GEOLOGIC SEDIMENTS; IRON; IRON COMPOUNDS; MINERALS; OXIDATION-REDUCTION; OXIDES; OXYGEN CONSUMPTION; RNA, RIBOSOMAL, 16S; SULFATES; SULFIDES; SULFUR; SULFUR COMPOUNDS; THERMODYNAMICS;

EID: 84945467939     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2015.50     Document Type: Article

References (65)

1. Akob DM, Mills HJ, Gihring TM, Kerkhof L, Stucki JW, Chin K-J, et al. (2008). Functional diversity and electron donor dependence of microbial populations capable of U(VI) reduction in radionuclide contaminated subsurface sediments. App Environ Microb 74: 3159-3170
2. Benner SG, Hansel CM, Wielinga BW, Barber TM, Fendorf S. (2002). Reductive dissolution and biomineralization of iron hydroxide under dynamic flow conditions. Environ Sci Technol 36: 1705-1711
3. Bethke CM, Sanford RA, Kirk MF, Jin QS, Flynn TM. (2011). The thermodynamic ladder in geomicrobiology. Am J Sci 311: 183-210
4. Burdige DJ. (1993). The biogeochemistry of manganese and iron reduction in marine-sediments. Earth Sci Rev 35: 249-284
5. Canfield DE. (2005). The early history of atmospheric oxygen: Homage to Robert M. Garrels. Ann Rev Earth Planet Sci 33: 1-36
6. Canfield DE, Stewart FJ, Thamdrup B, De Brabandere L, Dalsgaard T, DeLong EF, et al. (2010). A cryptic sulfur cycle in oxygen-minimum-zone waters off the Chilean coast. Science 330: 1375-1378
7. Caporaso JG, Kuczynski J, Stombaugh J, Bigginger K, Bushman FD, Costello EK, et al. (2010). QIIME allows analysis of high-Throughput community sequencing data. Nat Methods 7: 335-336
8. Champ DR, Gulens J, Jackson RE. (1979). Oxidationreduction sequences in ground water flow systems. Can J Earth Sci 16: 12-23
9. Chapelle FH, Lovley DR. (1992). Competative exclusion of sulfate reduction by Fe(III)-reducing bacteria: A mechanism for producing discrete zones of high-iron ground water. Groundwater 30: 29-36
10. Cline JD. (1969). Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14: 454-45
11. Coleman ML, Hedrick DB, Lovley DR, White DC, Pye K. (1993). Reduction of Fe(III) in sediments by sulfatereducing bacteria. Nature 361: 436-438
12. Cutting RS, Coker VS, Fellowes JW, Lloyd JR, Vaughan DJ. (2009). Mineralogical and morphological constraints on the reduction of Fe(III) minerals by Geobacter sulfurreducens. Geochim Cosmochim Acta 73: 4004-4022
13. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. 2006 Greengenes, a chimera-checked 16 S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72 5069-5072
14. Dobbin PS, Carter JP, Garcia-Salamanca San Juan C, von Hobe M, Powell AK, Richardson DJ. (1999). Dissimilatory Fe(III) reduction by Clostridium beijerinckii isolated from freshwater sediment using Fe (III) maltol enrichment. FEMS Microb Lett 176: 131-138
15. Dominik P, Pohl H, Bousserrhine N, Berthelin J, Kaupenjohann M. (2002). Limitations to the reductive dissolution of Al-substituted goethites by Clostridium butyricum. Soil Biol Biochem 34: 1147-1155
16. Dowd S, Callaway T, Wolcott R, Sun Y, McKeehan T, Hagevoort R, et al. (2008). Evaluation of the bacterial diversity in the feces of cattle using 16 S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC. Microbiology 8: 125
17. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200
18. Elsgard L, Jorgensen BB. (1992). Anoxic transformations of radiolabeled hydrogen sulfide in marine and freshwater sediments. Geochim Cosmochim Acta 56: 2425-2435
19. Emerson D, Weiss JV, Megonigal JP. (1999). Iron-oxidizing bacteria are associated with ferric hydroxide precipitates (Fe-plaque) on the roots of wetland plants. Appl Environ Microbiol 65: 2758-2761
20. Flynn TM, O'Loughlin EJ, Mishra B, DiChristina TJ, Kemner KM. (2014). Sulfur-mediated electron shuttling during bacterial iron reduction. Science 344: 1039-1042
21. Froelich PN, Klinkhammer GP, Bender ML, Luedtke NA, Heath GR, Cullen D, et al. (1979). Early oxidation of organic matter in pelagic sediments of the eastern equatorial Atlantic: Suboxic diagenesis. Geochim Cosmochim Acta 43: 1075-1090
22. Halevy I. (2013). Production, preservation, and biological processing of mass-independent sulfur isotope fractionation in the Archean surface environment. Proc Natl Acad Sci USA 110: 17644-17649
23. Hansel CM, Fendorf S, Sutton SR, Newville M. (2001). Characterization of Fe plaque and associated metals on the roots of mine-waste impacted aquatic plants. Environ Sci Technol 35: 3863-3868
24. Hansel CM, Benner SG, Neiss J, Dohnalkova A, Kukkadapu RK, Fendorf S. (2003). Secondary mineralization pathways induced by dissimilatory iron reduction of ferrihydrite under advective flow. Geochim Cosmochim Acta 67: 2977-2992
25. Hansel CM, Benner SG, Nico P, Fendorf S. 2004 Structural constraints of ferric (hydr oxides on dissimilatory iron reduction and the fate of Fe(II). Geochim Cosmochim Acta 68 3217-3229
26. Heitmann T, Blodau C. (2006). Oxidation and incoporation of hydrogen sulfide by dissolved organic matter. Chem Geol 235: 12-20
27. Hoehler TM, Alperin MJ, Albert DB, Martens CS. (1998). Thermodynamic control on hydrogen concentrations in anoxic sediments. Geochim Cosmochim Acta 62: 1745-1756
28. Holmkvist L, Ferdelman TG, Jorgensen BB. (2011). A cryptic sulfur cycle driven by iron in the methane zone of marine sediment (Aarhus Bay, Denmark). Geochim Cosmochim Acta 75: 3581-3599
29. Jakobsen R, Postma D. (1999). Redox zoning, rates of sulfate reduction and interactions with Fe-reduction and methanogenesis in a shallow sandy aquifer, Romo, Denmark. Geochim Cosmochim Acta 63: 137-151
30. Johnston DT, Poulton SW, Dehler C, Porter S, Husson J, Canfield DE, et al. (2010). An emerging picture of Neoproterozoic ocean chemistry: Insights from the Chuar Group, Grand Canyon, USA. Earth Planet Sci Let 290: 64-73
31. Jorgensen BB. (1990). A thiosulfate shunt in the sulfur cycle of marine sediments. Science 249: 152-154
32. Komlos J, Moon HS, Jaffe PR. (2008). Effect of Sulfate on the Simultaneous Bioreduction of Iron and Uranium. J Environ Qual 37: 2058-2062
33. Koretsky CM, Moore CM, Lowe KL, Meile C, Dichristina TJ, Van Cappellen P. (2003). Seasonal oscillation of microbial iron and sulfate reduction in saltmarsh sediments (Sapelo Island, GA, USA). Biogeochem 64: 179-203
34. Kwon MJ, Boyanov MI, Antonopoulos DA, Brulc JM, Johnston ER, Skinner KA, et al.2014). Effects of dissimilatory sulfate reduction on Fe-III (hydr)oxide reduction and microbial community development. Geochim Cosmochim Acta 129: 177-190
35. LaRowe DE, Van Cappellen P. (2011). Degradation of natural organic matter: A thermodynamic analysis. Geochim Cosmochim Acta 75: 2030-2042
36. Lentini CJ, Wankel SD, Hansel CM. (2012). Enriched iron (III)-reducing bacterial communities are shaped by carbon substrate and iron oxide mineralogy. Frontiers in Microbiology 3: 19
37. Lentini CJ. (2013). The Role of Fe(III) Oxyhydroxides in Shaping Microbial Communities Capable of Fe(III) Reduction (Doctoral dissertation). Harvard University: Cambridge, MA, USA
38. Li Y-L, Vali H, Yang J, Phelps TJ, Zhang CL. (2006). Reduction of iron oxides enhanced by sulfate-reducing bacterium and biogenic H2S. Geomicrob J 23: 103-117
39. Lohmayer R, Kappler A, Behrens-Losekann T, Planer-Friedrich B. (2014). Sulfur species as redox partners and electron shuttles for ferrihydrite reduction by Sulfospirillum deleyianum. Appl Environ Microbiol 80: 3141-3149
40. 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 Microbiol 53: 2636-2641
41. Lovley DR, Phillips EJP. (1988). Novel mode of microbial energy metabolism: Organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl Environ Microb 54: 1472-1480
42. Lovley DR, Holmes DE, Nevin KP. (2004). Dissimilatory Fe (III) and Mn(IV) Reduction. Adv Microb Physiol 49: 219-286
43. Ludwig W, Mittenhuber G, Friedrich CG. (1993). Transfer of Thiosphaera pantotropha to Paracoccus denitrificans. Int J Syst Bacteriol 43: 363-367
44. Majzlan J, Grevel K-D, Navrotsky A. (2003). Thermodynamics of Fe oxides: Part II. Enthalpies of formation and relative stability of goethite (a-FeOOH), lepidocrocite (g-FeOOH), and maghemite (g-Fe2O3). Am Mineral 88: 855-859
45. Majzlan J, Navrotsky A, Schwertmann U. (2004). Thermodynamics of iron oxides: Part III. Enthalpies of formation and stability of ferrihydrite (~ Fe(OH)3), schwertmannite ( ~ FeO(OH)3/4(SO4)1/8), and epsilon-Fe2O3. Geochimica Et Cosmochimica Acta 68: 1049-1059
46. Mikucki JA, Pearson A, Johnston DT, Turchyn AV, Farquhar J, Schrag DP, et al. (2009). A Contemporary Microbially Maintained Subglacial Ferrous Ocean Science 324: 397-400
47. Newville M. (2001). EXAFS analysis using FEFF and FEFFIT. J Synchr Rad 8: 96-100
48. Osorio H, Mangold S, Denis Y, Nancucheo I, Esparza M, Johnson DB, et al. (2013). Anaerobic sulfur metabolism coupled to dissimilatory iron reduction in the extremophile Acidithiobacillus ferrooxidans. Appl Environ Microbiol 79: 2172-2181
49. Oyekola OO, van Hille RP, Harrison STL. (2009). Competition between lactate oxidisers and fermenters under bisulphidogenic conditions: Implications in the biological treatment of AMD. Adv Mater Res 71: 689-692
50. Patrick WH, Henderson RE. (1981). Reduction and reoxidation cycles of manganese and iron in flooded soil and in water solution. Soil Sci Soc Am J 45: 855-859
51. Pester M, Knorr KH, Friedrich MW, Wagner M, Loy A. (2012). Sulfate-reducing microorganisms in wetlands-fameless actors in carbon cycling and climate change. Front Microbiol 3: 19
52. Planavsky NJ, McGoldrick P, Scott CT, Li C, Reinhard CT, Kelly AE, et al. (2011). Widespread iron-rich conditions in the mid-Proterozoic ocean. Nature 477: 448-U495
53. Postma D, Jakobsen R. (1996). Redox zonation: Equilibrium constraints on the Fe(III)/SO4- reduction interface. Geochim Cosmochim Acta 60: 3169-3175
54. Poulton SW. (2003). Sulfide oxidation and iron dissolution kinetics during the reaction of dissolved sulfide with ferrihydrite. Chem Geol 202: 79-94
55. Rabus R, Hansen RA, Widdel F. (2006). Dissimilatory sulfate- and sulfur-reducing prokaryotes. In Dworkin M (ed) The Prokaryotes: An Evolving Electronic Resource for the Microbiology Community. Springer-Verlag: New York, pp 659-768
56. Ruffroberts AL, Kuenen JG, Ward DM. (1994). Distribution of cultivated and uncultivated cyanobacteria and Chloroflexus-like bacteria in hot spring microbial mats. Appl Environ Microbiol 60: 697-704
57. Schwertmann U, Cornell RM. (2000). Iron Oxides in the Laboratory: Preparation and Characterization. Wiley-VCH: NY
58. Snow CL, Lilova KI, Radha AV, Shi Q, Smith S, Navrotsky A, et al. (2013). Heat capacity and thermodynamics of a synthetic two-line ferrihydrite, FeOOH0.027H2O. J Chem Thermo 58: 307-314
59. Stookey LL. (1970). Ferrozine- a new spectrophotometric reagent for iron. Anal Chem 42: 779-781
60. Straub KL, Schink B. (2004). Ferrihydrite-dependent growth of Sulfurospirillum deleyianum through electran transfer via sulfur cycling. App Environ Microb 70: 5744-5749
61. Wang Q, Garrity GM, Tiedje JM, Cole JR. (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261-5267
62. Webb SM. (2005). SIXPack a graphical user interface for XAS analysis using IFEFFIT. Physica Scripta, T115
63. Weber KA, Achenbach LA, Coates JD. (2006). Microorganisms pumping iron: Anaerobic microbial iron oxidation and reduction. Nature 4: 752-764
64. Williams KH, Long PE, Davis JA, Wilkins MJ, N'Guessan AL, Steefel CI, et al. (2011). Acetate availability and its influence on sustainable bioremediation of uraniumcontaminated groundwater. Geomicrob J 28: 519-539
65. Wuebbles DJ, Hayhoe K. (2002). Atmospheric methane and global change. Earth Sci Rev 57: 177-210