Abundances and potential activities of nitrogen cycling microbial communities along a chronosequence of a glacier forefield

ISME Journal

Volumn 5, Issue 6, 2011, Pages 1025-1037

  Brankatschk, Robert ^a   Töwe, Stefanie ^b   Kleineidam, Kristina ^c   Schloter, Michael ^c   Zeyer, Josef ^a  

^a ETH ZURICH   (Switzerland)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

chronosequence; functional genes; nitrogen cycle; real time PCR; soil development

Indexed keywords

NITROGEN;

ABUNDANCE; CHRONOSEQUENCE; DECOMPOSITION; DENITRIFICATION; ENZYME ACTIVITY; GENE; GLACIER DYNAMICS; MICROBIAL COMMUNITY; MINERALIZATION; NITROGEN CYCLE; ORGANIC MATTER; POLYMERASE CHAIN REACTION; SOIL IMPROVEMENT;

ARCHAEBACTERIUM; ARTICLE; BACTERIUM; CHEMISTRY; DENITRIFICATION; ECOSYSTEM; ENZYMOLOGY; GENETICS; ICE COVER; METABOLISM; MICROBIOLOGY; NITRIFICATION; NITROGEN FIXATION; PLANT; SOIL; SWITZERLAND;

ARCHAEA; BACTERIA; DENITRIFICATION; ECOSYSTEM; ICE COVER; NITRIFICATION; NITROGEN; NITROGEN FIXATION; PLANTS; SOIL; SOIL MICROBIOLOGY; SWITZERLAND;

DAMMAGLACIER; SWITZERLAND; URI;

EID: 79956287484     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2010.184     Document Type: Article

References (70)

1. Babic KH, Schauss K, Hai B, Sikora S, Redzepovic S, Radl V et al. (2008). Influence of different Sinorhizo-bium meliloti inocula on abundance of genes involved in nitrogen transformations in the rhizosphere of alfalfa (Medicago sativa L.). Environ Microbiol 10: 2922-2930.
2. Bach HJ, Hartmann A, Schloter M, Munch JC. (2001). PCR primers and functional probes for amplification and detection of bacterial genes for extracellular pepti-dases in single strains and in soil. J Microbiol Meth 44: 173-182. (Pubitemid 32124783)
3. Bardgett RD, Walker LR. (2004). Impact of coloniser plant species on the development of decomposer microbial communities following deglaciation. Soil Biol Biochem 36: 555-559. (Pubitemid 38215050)
4. Bardgett RD, Richter A, Bol R, Garnett MH, Baumler R, Xu XL et al. (2007). Heterotrophic microbial commu¬nities use ancient carbon following glacial retreat. Biol Lett 3: 487-490.
5. Bernasconi SM. (2008). Weathering, soil formation and initial ecosystem evolution on a glacier forefield: a case study from the Damma Glacier, Switzerland. Mineral Mag 72: 19-22.
6. Braker G, Fesefeldt A, Witzel K. (1998). Development of PCR primer systems for amplification of nitrite reductase genes (nirK and nirS) to detect denitrifying bacteria in environmental samples. Appl Environ Microbiol 64: 3769-3775. (Pubitemid 28462971)
7. Cabrera ML, Beare MH. (1993). Alkaline persulfate oxidation for determining total nitrogen in microbial biomass extracts. Soil Sci Soc Am J 57: 1007-1012.
8. Chapin FS, Walker FS, Fastie CL, Sharman LC. (1994). Mechanisms of primary succession following degla-ciation at Glacier Bay, Alaska. Ecol Monogr 64: 149-175.
9. Chronakova A, Radl V, Cuhel J, Simek M, Elhottova D, Engel M et al. (2009). Overwintering management on upland pasture causes shifts in an abundance of denitrifying microbial communities, their activity and N2O-reducing ability. Soil Biol Biochem 41: 1132-1138.
10. Cohen-Kupiec R, Chet I. (1998). The molecular biology of chitin digestion. Curr Opin Biotechnol 9: 270-277. (Pubitemid 28291177)
11. De Boer W, Kowalchuk GA. (2001). Nitrification in acid soils: micro-organisms and mechanisms. Soil Biol Biochem 33: 853-866. (Pubitemid 32533107)
12. Deiglmayr K, Philippot L, Tscherko D, Kandeler E. (2006). Microbial succession of nitrate-reducing bacteria in the rhizosphere of Poa alpina across a glacier foreland in the Central Alps. Environ Microbiol 8: 1600-1612. (Pubitemid 44167986)
13. Di HJ, Cameron KC, Shen JP, Winefield CS, O'Callaghan M, Bowatte S et al. (2009). Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci 2: 621-624.
14. Di HJ, Cameron KC, Shen JP, Winefield CS, O'Callaghan M, Bowatte S et al. (2010). Ammonia oxidizing bacteria and archaea grow under contrasting soil nitrogen condi¬tions. FEMS Microbiol Ecol 72: 386-394.
15. Duc L, Noll M, Meier BE, Burgmann H, Zeyer J. (2009). High Diversity of diazotrophs in the forefield of a receding alpine glacier. Microb Ecol 57: 179-190.
16. Edwards IP, Burgmann H, Miniaci C, Zeyer J. (2006). Variation in microbial community composition and culturability in the rhizosphere of Leucanthemopsis alpina L Heywood and adjacent bare soil along an alpine chronosequence. Microb Ecol 52: 679-692. (Pubitemid 44924006)
17. Eparvier A, Lemanceau P, Alabouvette C. (1991). Popu¬lation dynamics of non-pathogenic Fusarium and fluorescent Pseudomonas strains in rockwool, a sub¬stratum for soilless culture. FEMS Microbiol Lett 86: 177-184.
18. Ferderal Commission for Air Hygiene. (2005). Stickstoff-haltige Luftschadstoffe in der Schweiz, Schriftenreihe Umwelt Nr. 384. Federal Office for the Environment: Bern.
19. Frank DA, Groffman PM, Evans RD, Tracy BF. (2000). Ungulate stimulation of nitrogen cycling and retention in Yellowstone Park grasslands. Oecologia 123: 116-121. (Pubitemid 30244387)
20. Fuka MM, Engel M, Gattinger A, Bausenwein U, Sommer M, Munch JC et al. (2008). Factors influencing variability of proteolytic genes and activities in arable soils. Soil Biol Biochem 40: 1646-1653.
21. Hallin S, Jones CM, Schloter M, Philippot L. (2009). Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. ISME J 3: 597-605.
22. Hammerli A, Waldhuber S, Miniaci C, Zeyer J, Bunge M. (2007). Local expansion and selection of soil bacteria in a glacier forefield. Eur J Soil Sci 58: 1437-1445. (Pubitemid 350135275)
23. Hendel B, Marxsen J. (2005). Fluorometric determination of the activity of beta-glucosidase and other extra¬cellular hydrolytic enzymes. In: Graça, MAS, Bärlo-cher F, Gessner MO (eds). Methods to study litter decomposition. Springer: Dordrecht, pp 261-266.
24. Henry S, Baudoin E, López-Gutiérrez JC, Martin-Laurent F, Brauman A, Philippot L. (2004). Quantification of denitrifying bacteria in soils by nirK gene targeted real-time PCR. J Microbiol Meth 59: 327-335. (Pubitemid 39370795)
25. Henry S, Bru D, Stres B, Hallet S, Philippot L. (2006). Quantitative detection of the nosZ gene, enco¬ding nitrous oxide reductase, and comparison of the abundances of 16S rRNA, narG, nirK, and nosZ genes in soils. Appl Environ Microbiol 72: 5181-5189.
26. Hodkinson ID, Webb NR, Coulson SJ. (2002). Primary community assembly on land-the missing stages: why are the heterotrophic organisms always there first? J Ecol 90: 569-577. (Pubitemid 34616955)
27. Hoffmann H, Schloter M, Wilke BM. (2007). Microscale-scale measurement of potential nitrification rates of soil aggregates. Bio Fert Soils 44: 411-413. (Pubitemid 350105276)
28. Joergensen RG. (1996). The fumigation-extraction method to estimate soil microbial biomass: Calibration of the k(EC) value. Soil Biol Biochem 28: 25-31.
29. Kandeler E, Deiglmayr K, Tscherko D, Bru D, Philippot L. (2006). Abundance of narG, nirS, nirK, and nosZ genes of denitrifying bacteria during primary successions of a glacier foreland. Appl Environ Microbiol 72: 5957-5962. (Pubitemid 44414623)
30. 2 fixation and N cycling by dryas along a chronosequence within the forelands of the Athabasca glacier, Canada. Soil Biol Biochem 26: 623-632.
31. Kowalchuk GA, Stienstra AW, Heilig GH, Stephen JR, Woldendorp JW. (2000). Changes in the community structure of ammonia-oxidizing bacteria during secon¬dary succession of calcareous grasslands. Environ Microbiol 2: 99-110. (Pubitemid 33124586)
32. Lazzaro A, Abegg C, Zeyer J. (2009). Bacterial community structure of glacier forefields on siliceous and calcareous bedrock. Eur J Soil Sci 60: 860-870.
33. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW et al. (2006). Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442: 806-809. (Pubitemid 44258909)
34. Luo J, White RE, Ball PR, Tillman RW. (1996). Measuring denitrification activity in soils under pasture: Opti¬mizing conditions for the short-term denitrification enzyme assay and effects of soil storage on denitrifica-tion activity. Soil Biol Biochem 28: 409-417.
35. Maisch M. (2000). The longterm signal of climate change in the swiss alps: glacier retreat since the end of the little ice age and future ice decay scenarios. Geogr Fis Dinam Quat 23: 139-151. (Pubitemid 32152620)
36. Matsui K, Ishii N, Honjo M, Kawabata Z. (2004). Use of the SYBR Green I fluorescent dye and a centrifugal filter device for rapid determination of dissolved DNA concentration in fresh water. Aquat Microb Ecol 36: 99-105. (Pubitemid 39104240)
37. Michotey V, Méjean V, Bonin P. (2000). Comparison of methods for quantification of cytochrome cd1-denitrifying bacteria in environmental marine samples. Appl Environ Microbiol 66: 1564-1571. (Pubitemid 30185633)
38. National Air Pollution Monitoring Network (NABEL) (2008). NABEL-Luftbelastung 2007, Umweltzustand Nr. 0823. Federal Office for the Environment: Bern.
39. Nemergut DR, Anderson SP, Cleveland CC, Martin AP, Miller AE, Seimon A et al. (2007). Microbial commu¬nity succession in an unvegetated, recently degla-ciated soil. Microb Ecol 53: 110-122. (Pubitemid 46192557)
40. 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.
41. 3) and PM. Norwegian Meteorological Institute: Oslo.
42. Ohtonen R, Fritze H, Pennanen T et al. (1999). Ecosystem properties and microbial community changes in primary succession on a glacier forefront. Oecologia 119: 239-246. (Pubitemid 29235433)
43. Olander LP, Vitousek PM. (2000). Regulation of soil phos-phatase and chitinase activity by N and P availability. Biogeochemistry 49: 175-190. (Pubitemid 30170285)
44. Reigstad LJ, Richter A, Daims H, Urich T, Schwark L, Schleper C. (2008). Nitrification in terrestrial hot springs of Iceland and Kamchatka. FEMS Microbiol Ecol 64: 167-174. (Pubitemid 351533426)
45. Rheinbaben WV, Trolldenier G. (1984). Influence of plant growth on denitrification in relation to soil moisture and potassium nutrition. Z Pflanzenernähr Bodenkd 147: 730-738.
46. Roling WFM. (2007). Do microbial numbers count? Quantifying the regulation of biogeochemicalfluxes by population size and cellular activity. FEMS Micro-biol Ecol 62: 202-210. (Pubitemid 47609658)
47. Rosch C, Mergel A, Bothe H. (2002). Biodiversity of denitrifying and dinitrogen-fixing bacteria in an acid forest soil. Appl Environ Microbiol 68: 3818-3829. (Pubitemid 34836690)
48. Rotthauwe JH, Witzel K, Liesack W. (1997). The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural am¬monia-oxidizing populations. Appl Environ Microbiol 63: 4704-4712. (Pubitemid 27524201)
49. Schauss K, Focks A, Leininger S, Kotzerke A, Heuer H, Thiele-Bruhn S et al. (2009). Dynamics and functional relevance of ammonia-oxidizing archaea in two agri¬cultural soils. Environ Microbiol 11: 446-456.
50. Schimel JP, Bennett J. (2004). Nitrogen mineralization: Challenges of a changing paradigm. Ecology 85: 591-602. (Pubitemid 38398271)
51. Schmalenberger A, Noll M. (2009). Shifts in desulfonating bacterial communities along a soil chronosequence in the forefield of a receding glacier. FEMS Microbiol Ecol 71: 208-217.
52. Schmidt SK, Reed SC, Nemergut DR, Grandy AS, Cleveland CC, Weintraub MN et al. (2008). The earliest stages of ecosystem succession in high-elevation (5000 metres above sea level), recently deglaciated soils. Proc R Soc B 275: 2793-2802. (Pubitemid 352790141)
53. Schutte UME, Abdo Z, Bent SJ, William CJ, Schneider GM, Solhein B et al. (2009). Bacterial succession in a glacier foreland of the High Arctic. ISME J 3: 1258-1268.
54. Sigler WV, Crivii S, Zeyer J. (2002). Bacterial succession in glacial forefield soils characterized by community structure, activity and opportunistic growth dyna¬mics. Microb Ecol 44: 306-316. (Pubitemid 36941361)
55. Sigler WV, Zeyer J. (2002). Microbial diversity and activity along the forefields of two receding glaciers. Microb Ecol 43: 397-407. (Pubitemid 36941331)
56. Throback IN, Enwall K, Jarvis A, Hallin S. (2004). Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE. FEMS Microbiol Ecol 49: 401-417. (Pubitemid 39119598)
57. Towe S, Albert A, Kleineidam K, Brankatschk R, Dumig A, Welzl G et al. (2010a). Abundance of microbes involved in nitrogen transformation in the rhizosphere of Leucanthemopsis alpina (L.) HEYWOOD grown in soils from different sites of the Damma glacier forefield. Microb Ecol 60: 762-770.
58. Towe S, Kleineidam K, Schloter M. (2010b). Differences in amplification efficiency of standard curves in quanti¬tative real-time PCR assays and consequences for gene quantification in environmental samples. J Microbiol Methods 82: 338-341.
59. Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk HP, Schleper C. (2005). Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ Microbiol 7: 1985-1995. (Pubitemid 41752386)
60. Tscherko D, Rustemeier J, Richter A, Wanek W, Kandeler E. (2003). Functional diversity of the soil microflora in primary succession across two glacier forelands in the Central Alps. Eur J Soil Sci 54: 685-696. (Pubitemid 37502492)
61. Tscherko D, Hammesfahr U, Marx MC, Kandeler E. (2004). Shifts in rhizosphere microbial communities and enzyme activity of Poa alpina across an alpine chronosequence. Soil Biol Biochem 36: 1685-1698. (Pubitemid 39348025)
62. Tscherko D, Hammesfahr U, Zeltner G, Kandeler E, Bocker R. (2005). Plant succession and rhizosphere microbial communities in a recently deglaciated alpine terrain. Basic Appl Ecol 6: 367-383. (Pubitemid 40968420)
63. Tsunogai U, Kido T, Hirota A, Ohkubo SB, Komatsu DD, Nakagawa F. (2008). Sensitive determinations of stable nitrogen isotopic composition of organic nitro¬gen through chemical conversion into N2O. Rapid Commun Mass Sp 22: 345-354. (Pubitemid 351212860)
64. Vance ED, Brookes PC, Jenkinson DS. (1987). An extrac¬tion method for measuring soil microbial biomass-C. Soil Biol Biochem 19: 703-707.
65. Xiang SR, Shang TC, Chen Y, Yao TD. (2009). Deposition and postdeposition mechanisms as possible drivers of microbial population variability in glacier ice. FEMS Microbiol Ecol 70: 9-20.
66. Walker LR, del Moral R. (2003). Primary Succession and Ecosystem Rehabilitation. Cambridge University Press: Cambridge.
67. Xiao X, Yin X, Lin J, Sun L, You Z, Wang P et al. (2005). Chitinase genes in lake sediments of Ardley Island, Antarctica. Appl Environ Microbiol 71: 7904-7909. (Pubitemid 41803909)
68. Yoshitake S, Uchida M, Koizumi H, Nakatsubo T. (2007). Carbon and nitrogen limitation of soil microbial respiration in a High Arctic successional glacier foreland near Ny-angstrom lesund, Svalbard. Polar Res 26: 22-30. (Pubitemid 46359496)
69. Zehr JP, Jenkins BD, Short SM, Steward GF. (2003). Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Micro-biol 5: 539-554. (Pubitemid 36832210)
70. Zumft WG. (1997). Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61: 522-616.