Denitrification by sulfur-oxidizing bacteria in a eutrophic lake

Aquatic Microbial Ecology

Volumn 66, Issue 3, 2012, Pages 283-293

  Burgin, Amy J ^a   Hamilton, Stephen K ^a   Jones, Stuart E ^a,b   Lennon, Jay T ^a,c,d  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NOTRE DAME   (United States)

^c Indiana University ^*  (United States)

^d INDIANA UNIVERSITY   (United States)

Author keywords

Denitrification; Nitrate reduction; Sulfide; Sulfur oxidation; Sulfur driven denitrification; Sulfurimonas denitrificans; Wintergreen Lake

Indexed keywords

BACTERIA (MICROORGANISMS); SULFURIMONAS;

EID: 84863935166     PISSN: 09483055     EISSN: None     Source Type: Journal    
DOI: 10.3354/ame01574     Document Type: Article

References (57)

1. Alexander RB, Smith RA, Schwarz GE (2000) Effect of stream channel size on the delivery of nitrogen to the Gulf of Mexico. Nature 403: 758-761 (Pubitemid 30111834)
2. Amaral-Zettler LA, Rocca JD, Lamontagne MG, Dennett MR, Gast RJ (2008) Changes in microbial community structure in the wake of Hurricanes Katrina and Rita. Environ Sci Technol 42: 9072-9078
3. Aminot A, Kirkwood DS, Kerouel R (1997) Determination of ammonia in seawater by the indophenol-blue method: evaluation of the ICES NUTS I/C 5 questionnaire. Mar Chem 56: 59-75
4. Arango C, Tank J, Schaller JL, Royer TV, Bernot MJ, David MB (2007) Benthic organic carbon influences denitrification in streams with high nitrate concentration. Freshw Biol 52: 1210-1222 (Pubitemid 46872693)
5. Brettar I, Rheinheimer G (1991) Denitrification in the Central Baltic: evidence for H2S-oxidation as motor of denitrification at the oxic-anoxic interface. Mar Ecol Prog Ser 77: 157-169
6. Brettar I, Labrenz M, Flavier S, Bötel J, Kuosa H, Christen R, Höfle MG (2006) Identification of a Thiomicrospira denitrificans- like epsilonproteobacterium as a catalyst for autotrophic denitrification in the central Baltic Sea. Appl Environ Microbiol 72: 1364-1372 (Pubitemid 43271248)
7. Briée C, Moreira D, Lopez-Garcia P (2007) Archaeal and bacterial community composition of sediment and plankton from a suboxic freshwater pond. Res Microbiol 158: 213-227 (Pubitemid 46484032)
8. Brock TD (1978) The poisoned control in biogeochemical investigations. In: Krumbein WE (ed) Environmental biogeochemistry and geomicrobiology. Ann Arbor Science Publishers, Ann Arbor, MI, p 717-725
9. Brunet RC, Garcia-Gil LJ (1996) Sulfide-induced dissimilatory nitrate reduction to ammonia in anaerobic freshwater sediments. FEMS Microbiol Ecol 21: 131-138
10. Burgin AJ, Hamilton SK (2007) Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways. Front Ecol Environ 5: 89-96 (Pubitemid 46363885)
11. 4 2- production in freshwater ecosystems: implications for N and S cycling. Ecosystems 11: 908-922
12. Cardoso RB, Sierra-Alvarez R, Rowlette P, Flores ER, Gomez J, Field JA (2006) Sulfide oxidation under chemolithoautotrophic denitrifying conditions. Biotechnol Bioeng 95: 1148-1157 (Pubitemid 44901330)
13. Cornwell JC, Kemp WM, Kana TM (1999) Denitrification in coastal ecosystems: methods, environmental controls, and ecosystem level controls. Aquat Ecol 33: 41-54 (Pubitemid 30213364)
14. Cytryn E, van Rijn J, Schramm A, Gieseke A, de Beer D, Minz D (2005a) Identification of bacteria potentially responsible for oxic and anoxic sulfide oxidation in biofilters of a recirculating mariculture system. Appl Environ Microbiol 71: 6134-6141 (Pubitemid 41456911)
15. Cytryn E, Minz D, Gelfand I, Neori A, Gieseke A, De Beer D, Van Rijn J (2005b) Sulfide-oxidizing activity and bacte - rial community structure in a fluidized bed reactor from a zero-discharge mariculture system. Environ Sci Technol 39: 1802-1810 (Pubitemid 40387737)
16. Dalsgaard T, Thamdrup B, Canfield DE (2005) Anaerobic ammonium oxidation (anammox) in the marine environment. Res Microbiol 156: 457-464 (Pubitemid 40615411)
17. Davidsson TE, Stahl M (2000) The influence of organic carbon on nitrogen transformations in five wetland soils. Soil Sci Soc Am J 64: 1129-1136 (Pubitemid 30416635)
18. Fossing H, Gallardo VA, Jorgensen BB, Huttel M and others (1995) Concentration and transport of nitrate by the matforming sulfur bacterium Thioploca. Nature 374: 713-715
19. Gardner WS, McCarthy MJ (2009) Nitrogen dynamics at the sediment-water interface in shallow, sub-tropical Florida Bay: why denitrification efficiency may decrease with increased eutrophication. Biogeochemistry 95: 185-198
20. Gardner WS, McCarthy MJ, An SM, Sobolev D, Sell KS, Brock D (2006) Nitrogen fixation and dissimilatory nitrate reduction to ammonium (DNRA) support nitrogen dynamics in Texas estuaries. Limnol Oceanogr 51: 558-568 (Pubitemid 43259740)
21. Golterman HL, Clymo RS (1969) Methods for chemical analysis of fresh waters. Blackwell, Oxford
22. Grote J, Jost G, Labrenz M, Herndl GJ, Juergens K (2008) Epsilonproteobacteria represent the major portion of chemoautotrophic bacteria in sulfidic waters of pelagic redoxclines of the Baltic and Black Seas. Appl Environ Microbiol 74: 7546-7551
23. 2 in 15N tracer experiments. Limnol Oceanogr Methods 5: 233-240 (Pubitemid 351773981)
24. Hamilton SK, Bruesewitz DA, Horst GP, Sarnelle O (2009) Biogenic calcite-phosphorus precipitation as a negative feedback to lake eutrophication. Can J Fish Aquat Sci 66: 343-350
25. Hill AR, Cardaci M (2004) Denitrification and organic carbon availability in riparian wetland soils and subsurface sediments. Soil Sci Soc Am J 68: 320-325 (Pubitemid 38086480)
26. Höfle MG, Flavier S, Christen R, Bötel J, Labrenz M, Brettar I (2005) Retrieval of nearly complete 16S rRNA gene sequences from environmental DNA following 16S rRNA-based community fingerprinting. Environ Microbiol 7: 670-675 (Pubitemid 40580587)
27. Holmer M, Storkholm P (2001) Sulphate reduction and sulphur cycling in lake sediments: a review. Freshw Biol 46: 431-451 (Pubitemid 32402364)
28. + in marine, estuarine and fresh waters: an adaptation of the ammonia diffusion method for samples with low ammonium concentrations. Mar Chem 60: 235-243 (Pubitemid 28253417)
29. Jones SE, Lennon JT (2009) Evidence for limited microbial transfer of methane in a planktonic food web. Aquat Microb Ecol 58: 45-53
30. Jorgensen BB, Gallardo VA (1999) Thioploca spp: filamentous sulfur bacteria with nitrate vacuoles. FEMS Microbiol Ecol 28: 301-313 (Pubitemid 29142429)
31. Joye SB, Hollibaugh JT (1995) Influence of sulfide inhibition of nitrification on nitrogen regeneration in sediments. Science 270: 623-625 (Pubitemid 26457191)
32. Kamp A, Stief P, Schulz-Vogt HN (2006) Anaerobic sulfide oxidation with nitrate by a freshwater Beggiatoa enrichment culture. Appl Environ Microbiol 72: 4755-4760 (Pubitemid 44078801)
33. King GM, Klug MJ (1980) Sulfhydrolase activity in sediments of Wintergreen Lake, Kalamazoo County, Michigan. Appl Environ Microbiol 39: 950-956
34. King GM, Klug MJ (1982) Comparative aspects of sulfur mineralization in sediments of a eutrophic lake basin. Appl Environ Microbiol 43: 1406-1412 (Pubitemid 12061317)
35. Labrenz M, Brettar I, Christen R, Flavier S, Bötel J, Höfle MG (2004) Development and application of a real-time PCR approach for quantification of uncultured bacteria in the central Baltic Sea. Appl Environ Microbiol 70: 4971-4979 (Pubitemid 39095527)
36. Merrill AG, Zak DR (1992) Factors controlling denitrification rates in upland and swamp forests. Can J For Res 22: 1597-1604 (Pubitemid 23378234)
37. Mulholland PJ, Helton AM, Poole GC, Hall RO and others (2008) Stream denitrification across biomes and its response to anthropogenic nitrate loading. Nature 452: 202-205 (Pubitemid 351380244)
38. Nielsen PH, de Muro MA, Nielsen JL (2000) Studies on the in situ physiology of Thiothrix spp. present in activated sludge. Environ Microbiol 2: 389-398 (Pubitemid 33136700)
39. Otte S, Kuenen JG, Nielsen LP, Paerl HW and others (1999) Nitrogen, carbon, and sulfur metabolism in natural Thioploca samples. Appl Environ Microbiol 65: 3148-3157 (Pubitemid 29315593)
40. Payne EK, Burgin AJ, Hamilton SK (2009) Sediment nitrate manipulation using porewater equilibrators reveals potential for N and S coupling in freshwaters. Aquat Microb Ecol 54: 233-241
41. Porter ML, Engle AS, Kane TC, Kinkle BK (2009) Productivity- diversity relationships from chemolithoautotrophically based sulfidic karst systems. Int J Speleol 38: 27-40
42. Rivett MO, Buss SR, Morgan P, Smith JWN, Bemment CD (2008) Nitrate attenuation in groundwater: a review of biogeochemical controlling processes. Water Res 42: 4215-4232
43. Saunders DL, Kalff J (2001) Nitrogen retention in wetlands, lakes and rivers. Hydrobiologia 443: 205-212 (Pubitemid 32442340)
44. Schubert CJ, Durisch-Kaiser E, Wehrli B, Thamdrup B, Lam P, Kuypers MMM (2006) Anaerobic ammonium oxidation in a tropical freshwater system (Lake Tanganyika). Environ Microbiol 8: 1857-1863 (Pubitemid 44326477)
45. Schulz HN, Brinkhoff T, Ferdelman TG, Marine MH, Teske A, Jorgensen BB (1999) Dense populations of a giant sulfur bacterium in Namibian shelf sediments. Science 284: 493-495 (Pubitemid 29289623)
46. Scott JT, McCarthy MJ, Gardner WS, Doyle RD (2008) De - nitrification, dissimilatory nitrate reduction to ammonium, and nitrogen fixation along a nitrate concentration gradient in a created freshwater wetland. Biogeochemistry 87: 99-111
47. Seitzinger S, Harrison JA, Bohlke JK, Bouwman AF and others (2006) Denitrification across landscapes and waterscapes: a synthesis. Ecol Appl 16: 2064-2090 (Pubitemid 44917572)
48. 2S on dissimilatory nitrate reduction. Estuar Coast Shelf Sci 67: 231-238 (Pubitemid 43227538)
49. Shao MF, Zhang T, Fang HHP (2010) Sulfur driven denitrification: diversity, biochemistry, and engineering applications. Appl Microbiol Biotechnol 88: 1027-1042
50. Sher Y, Schneider K, Schwermer CU, van Rijn J (2008) Sulfide- induced nitrate reduction in the sludge of an anaerobic digester of a zero-discharge recirculating mariculture system. Water Res 42: 4386-4392
51. Sievert SM, Scott KA, Klotz MG, Chain PSG and others (2008) Genome of the epsilonproteobacterial chemo litho - autotroph Sulfurimonas denitrificans. Appl Environ Microbiol 74: 1145-1156 (Pubitemid 351287086)
52. Vila X, Abella CA, Figueras JB, Hurley JP (1998) Vertical models of phototrophic bacterial distribution in the meta - limnetic microbial communities of several freshwater North-American kettle lakes. FEMS Microbiol Ecol 25: 287-299 (Pubitemid 28108160)
53. Wang FY, Chapman PM (1999) Biological implications of sulfide in sediment-a review focusing on sediment toxicity. Environ Toxicol Chem 18: 2526-2532 (Pubitemid 29491657)
54. Weber KA, Achenbach LA, Coates JD (2006) Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nat Rev Microbiol 4: 752-764 (Pubitemid 44420126)
55. Wetzel RG (2001) Limnology: lake and river ecosystems. Academic Press, San Diego, CA
56. Whitmire SL (2003) Anaerobic biogeochemical functions of Michigan wetlands and the influence of water source. PhD dissertation, Michigan State University, East Lansing, MI
57. Wolfinger R, Chang M 1999. Comparing the SAS GLM and MIXED procedures for repeated measures. SAS Institute, Cary, NC