Oxygen availability and distance to surface environments determine community composition and abundance of ammonia-oxidizing prokaroytes in two superimposed pristine limestone aquifers in the Hainich region, Germany

FEMS Microbiology Ecology

Volumn 90, Issue 1, 2014, Pages 39-53

  Opitz, Sebastian ^a   Küsel, Kirsten ^a,b   Spott, Oliver ^c   Totsche, Kai Uwe ^a   Herrmann, Martina ^a,b  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b GERMAN CENTRE FOR INTEGRATIVE BIODIVERSITY RESEARCH IDIV HALLE JENA LEIPZIG   (Germany)

^c HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

Author keywords

Ammonia oxidation; Groundwater; Nitrification

Indexed keywords

AMMONIA; CALCIUM CARBONATE; GROUND WATER; OXYGEN; RNA 16S;

ARCHAEON; BACTERIA; BIODIVERSITY; CHEMISTRY; CLASSIFICATION; ENVIRONMENT; GENETICS; GERMANY; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NITRIFICATION; OXIDATION REDUCTION REACTION;

AMMONIA; ARCHAEA; BACTERIA; BIODIVERSITY; CALCIUM CARBONATE; ENVIRONMENT; GERMANY; GROUNDWATER; MOLECULAR SEQUENCE DATA; NITRIFICATION; OXIDATION-REDUCTION; OXYGEN; RNA, RIBOSOMAL, 16S;

EID: 84907900117     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/1574-6941.12370     Document Type: Article

References (72)

1. Albertin AR, Sickman JO, Pinowska A & Stevenson RJ (2012) Identification of nitrogen sources and transformations within karst springs using isotope tracers of nitrogen. Biogeochemistry 108: 219-232.
2. Andersson M, Kjøller A & Struwe S (2004) Microbial enzyme activities in leaf litter, humus and mineral soil layers of European forests. Soil Biol Biochem 36: 1527-1537.
3. Bakalowicz M (2005) Karst groundwater: A challenge for new resources. Hydrogeol J 13: 148-160.
4. Bonacci O, Pipan T & Culver DC (2009) A framework for karst ecohydrology. Environ Geol 56: 891-900.
5. Brady NC & Weil RR (1996) The Nature and Properties of Soils. Prentice-Hall Inc., Upper Saddle River, NJ.
6. 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.
7. Buss SR, Herbert AW, Morgan P, Thornton SF & Smith JWN (2004) A review of ammonium attenuation in soil and groundwater. Quart J Eng Geol Hydrogeol 37: 347-359.
8. Church MJ, Wai B, Karl DM & DeLong EF (2010) Abundances of crenarchaeal amoA genes and transcripts in the Pacific Ocean. Environ Microbiol 12: 679-688.
9. Clark DR, Rees AP & Joint I (2008a) Ammonium regeneration and nitrification rates in the oligotrophic Atlantic Ocean: implications for new production estimates. Limnol Oceanogr 53: 52-62.
10. 15N evidence for anaerobic oxidation (Anammox). Ground Water Monit Rem 28: 73-82.
11. Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18: 117-143.
12. Daims H, Brühl A, Amann R, Schleifer KH & Wagner M (1999) The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22: 434-444.
13. de Bie MJM, Speksnijder AGCL, Kowalchuk GA, Schuurman T, Zwart G, Stephen JR, Diekmann OE & Laanbroek HJ (2001) Shifts in the dominant populations of ammonia-oxidizing ß subclass Proteobacteria along the eutrophic Schelde estuary. Aquat Microb Ecol 23: 225-236.
14. DeLong EF (1992) Archaea in coastal marine environments. P Natl Acad Sci USA 89: 5685-5689.
15. Dibbern D, Schmalwasser A, Lueders T & Totsche KU (2014) Selective transport of plant root-associated bacterial populations in agricultural soils upon snowmelt. Soil Biol Biochem 69: 187-196.
16. Einsiedl F & Mayer B (2006) Hydrodynamic and microbial processes controlling nitrate in a fissured-porous karst aquifer of the Franconian Alb, southern Germany. Environ Sci Technol 40: 6697-6702.
17. Erguder TH, Boon N, Wittebolle L, Marzorati M & Verstraete W (2009) Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiol Rev 33: 855-869.
18. Erskine AD (2000) Transport of ammonium in aquifers: retardation and degradation. Quart J Eng Geol Hydrogeol 33: 161-170.
19. Ford DC & Williams PW (1989) Karst Geomorphology and Hydrology. Unwin Hyman, London.
20. Francis CA, O'Mullan GD & Ward BB (2003) Diversity of ammonia monooxygenase (amoA) genes across environmental gradients in Chesapeake Bay sediments. Geobiology 1: 129-140.
21. Francis CA, Roberts KJ, Beman JM, Santoro AE & Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. P Natl Acad Sci USA 102: 14683-14688.
22. 2O by nitrifying bacteria at reduced concentrations of oxygen. Appl Environ Microbiol 40: 526-532.
23. Grasshoff K, Kremling K & Ehrhardt M (1983) Methods of Seawater Analysis. Verlag Chemie Weinheim, Weinheim.
24. Gubry-Rangin C, Hai B, Quince C, Engel M, Thomson BC, James P, Schloter M, Griffiths RI, Prosser JI & Nicol GW (2011) Niche specialization of terrestrial archaeal ammonia oxidizers. P Natl Acad Sci USA 108: 21206-21211.
25. Hammer O, Harper DAT & Ryan PD (2001) past: paleontological statistics software package for education and data analysis. Paleontol Elec 4: 1-9.
26. Hatzenpichler R (2012) Diversity, physiology, and niche differentiation of ammonia-oxidizing archaea. Appl Environ Microbiol 78: 7501-7510.
27. Herrmann M, Saunders AM & Schramm A (2008) Archaea dominate the ammonia-oxidizing community in the rhizosphere of the freshwater macrophyte Littorella uniflora. Appl Environ Microbiol 74: 3279-3283.
28. Herrmann M, Scheibe A, Avrahami S & Kusel K (2011) Ammonium availability affects the ratio of ammonia-oxidizing bacteria to ammonia-oxidizing archaea in simulated creek ecosystems. Appl Environ Microbiol 77: 1896-1899.
29. Herrmann M, Hädrich A & Küsel K (2012) Predominance of thaumarchaeal ammonia oxidizer abundance and transcriptional activity in an acidic fen. Environ Microbiol 14: 3013-3025.
30. Ivanova IA, Stephen JR, Chang YJ, Brüggemann J, Long PE, McKinley JP, Kowalchuk GA, White DC & Macnaughton SJ (2000) A survey of 16S rRNA and amoA genes related to autotrophic ammonia-oxidizing bacteria of the beta-subdivision of the class Proteobacteria in contaminated groundwater. Can J Microbiol 46: 1012-1020.
31. Jost G, Dirnböck T, Grabner M-T & Mirtl M (2011) Nitrogen leaching of two forest ecosystems in a karst watershed. Water Air Soil Pollut 218: 633-649.
32. Kim BK, Jung M-Y, Yu DS, Park S-J, Oh TK, Rhee S-K & Kim JF (2011) Genome sequence of an ammonia-oxidizing soil archaeon, "Candidatus Nitrosoarchaeum koreensis" MY1. J Bacteriol 193: 5539-5540.
33. Klappenbach JA, Saxman PR, Cole JR & Schmidt TM (2001) rrndb: the ribosomal RNA operon copy number database. Nucleic Acids Res 29: 181-184.
34. Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB & Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437: 543-546.
35. Koops H-P & Pommerening-Röser A (2001) Distribution and ecophysiology of the nitrifying bacteria emphasizing cultured species. FEMS Microbiol Ecol 37: 1-9.
36. Laanbroek HJ & Speksnijder AGCL (2008) Niche separation of ammonia-oxidizing bacteria across a tidal freshwater marsh. Environ Microbiol 10: 3017-3025.
37. Lee ZM-P, Bussema C 3rd & Schmidt TM (2009) rrnDB: documenting the number of rRNA and tRNA genes in bacteria and archaea. Nucleic Acids Res 37: D489-D493.
38. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC & Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442: 806-809.
39. Loy A, Lehner A, Lee N, Adamczyk J, Meier H, Ernst J, Schleifer K-H & Wagner M (2002) Oligonucleotide microarray for 16S rRNA gene-based detection of all recognized lineages of sulfate-reducing prokaryotes in the environment. Appl Environ Microbiol 68: 5064-5081.
40. Ludwig W, Strunk O, Westram R et al. (2004) arb: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
41. Mußmann M, Brito I, Pitcher A et al. (2011) Thaumarchaeotes abundant in refinery nitrifying sludges express amoA but are not obligate autotrophic ammonia oxidizers. P Natl Acad Sci USA 108: 16771-16776.
42. Muyzer G & Smalla K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie Van Leeuwenhoek 73: 127-141.
43. Nicol GW, Leininger S, Schleper C & Prosser JI (2008) The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia-oxidizing archaea and bacteria. Environ Microbiol 10: 2966-2978.
44. Nicolaisen MH & Ramsing NB (2002) Denaturing gradient gel electrophoresis (DGGE) approaches to study the diversity of ammonia-oxidizing bacteria. J Microbiol Methods 50: 189-203.
45. Okano Y, Hristova KR, Leutenegger CM, Jackson LE, Denison RF, Gebreyesus B, Lebauer D & Scow KM (2004) Application of real-time PCR to study effects of ammonium on population size of ammonia-oxidizing bacteria in soil. Appl Environ Microbiol 70: 1008-1016.
46. Panno S, Hackley K, Hwang H & Kelly W (2001) Determination of the sources of nitrate contamination in karst springs using isotopic and chemical indicators. Chem Geol 179: 113-128.
47. Patel A, Noble RT, Steele JA, Schwalbach MS, Hewson I & Fuhrman JA (2007) Virus and prokaryote enumeration from planktonic aquatic environments by epifluore-scence microscopy with SYBR Green I. Nat Protoc 2: 269-276.
48. Pester M, Schleper C & Wagner M (2011) The Thaumarchaeota: an emerging view of their phylogeny and ecophysiology. Curr Opin Microbiol 14: 300-306.
49. Prosser JI & Nicol GW (2008) Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ Microbiol 10: 2931-2941.
50. Ragon M, Van Driessche AES, García-Ruíz JM, Moreira D & López-García P (2013) Microbial diversity in the deep-subsurface hydrothermal aquifer feeding the giant gypsum crystal-bearing Naica Mine, Mexico. Front Microbiol 4: 37.
51. Ramette A (2007) Multivariate analyses in microbial ecology. FEMS Microbiol Ecol 62: 142-160.
52. Reed DW, Smith JM, Francis CA & Fujita Y (2010) Responses of ammonia-oxidizing bacterial and archaeal populations to organic nitrogen amendments in low-nutrient groundwater. Appl Environ Microbiol 76: 2517-2523.
53. Rees GN, Baldwin DS, Watson GO, Perryman S & Nielsen DL (2004) Ordination and significance testing of microbial community composition derived from terminal restriction fragment length polymorphisms: application of multivariate statistics. Antonie Van Leeuwenhoek 86: 339-347.
54. Rogers DR & Casciotti KL (2010) Abundance and diversity of archaeal ammonia oxidizers in a coastal groundwater system. Appl Environ Microbiol 76: 7938-7948.
55. Rotthauwe JH, Witzel KP & Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63: 4704-4712.
56. Santoro AE, Francis CA, de Sieyes NR & Boehm AB (2008) Shifts in the relative abundance of ammonia-oxidizing bacteria and archaea across physicochemical gradients in a subterranean estuary. Environ Microbiol 10: 1068-1079.
57. Schloss PD, Westcott SL, Ryabin T et al. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541.
58. Sims A, Horton J, Gajaraj S, McIntosh S, Miles RJ, Mueller R, Reed R & Hu Z (2012) Temporal and spatial distributions of ammonia-oxidizing archaea and bacteria and their ratio as an indicator of oligotrophic conditions in natural wetlands. Water Res 46: 4121-4129.
59. Smith RL, Baumgartner LK, Miller DN, Repert DA & Böhlke JK (2006) Assessment of nitrification potential in ground water using short term, single-well injection experiments. Microb Ecol 51: 22-35.
60. Smorczewski WT & Schmidt EL (1991) Numbers, activities, and diversity of autotrophic ammonia-oxidizing bacteria in a freshwater, eutrophic lake sediment. Can J Microbiol 37: 828-833.
61. Spang A, Poehlein A, Offre P et al. (2012) The genome of the ammonia-oxidizing Candidatus Nitrososphaera gargensis: insights into metabolic versatility and environmental adaptations. Environ Microbiol 14: 3122-3145.
62. Speksnijder AGCL, Kowalchuk GA, Roest K & Laanbroek HJ (1998) Recovery of a Nitrosomonas-like 16S rDNA sequence group from freshwater habitats. Syst Appl Microbiol 21: 321-330.
63. ®. Rapid Commun Mass Spectrom 20: 3267-3274.
64. 15N abundance and concentration of ammonium, nitrite, or nitrate in aqueous samples by the SPINMAS technique. Isot Environ Health Stud 43: 227-236.
65. Stephen JR, Kowalchuk GA, Bruns M-AV, McCaig AE, Phillips CJ, Embley TM & Prosser JI (1998) Analysis of β-subgroup proteobacterial ammonia oxidizer populations in soil by denaturing gradient gel electrophoresis analysis and hierarchical phylogenetic probing. Appl Environ Microbiol 64: 2958-2965.
66. Takai K & Horikoshi K (2000) Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl Environ Microbiol 66: 5066-5072.
67. Van der Wielen PWJJ, Voost S & van der Kooij D (2009) Ammonia-oxidizing bacteria and archaea in groundwater treatment and drinking water distribution systems. Appl Environ Microbiol 75: 4687-4695.
68. Velghe N & Claeys A (1985) Rapid spectrophotometric determination of nitrate in mineral waters with resorcinol. Analyst 110: 313.
69. Vitousek PM, Gosz JR, Grier CC, Melillo JM & Reiners WA (1982) A comparative analysis of potential nitrification and nitrate mobility in forest ecosystems. Ecol Monogr 52: 155-177.
70. Wood WW & Low WH (1986) Aqueous geochemistry and diagenesis in the eastern Snake River Plain aquifer system, Idaho. Geol Soc Am Bull 97: 1456-1466.
71. Wuchter C, Abbas B, Coolen MJL et al. (2006) Archaeal nitrification in the ocean. P Natl Acad Sci USA 103: 12317-12322.
72. Zhou Y, Kellermann C & Griebler C (2012) Spatio-temporal patterns of microbial communities in a hydrologically dynamic pristine aquifer. FEMS Microbiol Ecol 81: 230-242.