Habitat Specialization Along a Wetland Moisture Gradient Differs Between Ammonia-oxidizing and Denitrifying Microorganisms

Abstract

Gradients in abiotic parameters, such as soil moisture, can strongly influence microbial community structure and function. Denitrifying and ammonia-oxidizing microorganisms, in particular, have contrasting physiological responses to abiotic factors such as oxygen concentration and soil moisture. Identifying abiotic factors that govern the composition and activity of denitrifying and ammonia-oxidizing communities is critical for understanding the nitrogen cycle. The objectives of this study were to (i) examine denitrifier and archaeal ammonia oxidizer community composition and (ii) assess the taxa occurring within each functional group related to soil conditions along an environmental gradient. Soil was sampled across four transects at four locations along a dry to saturated environmental gradient at a restored wetland. Soil pH and soil organic matter content increased from dry to saturated plots. Composition of soil denitrifier and ammonia oxidizer functional groups was assessed by terminal restriction fragment length polymorphism (T-RFLP) community analysis, and local soil factors were also characterized. Microbial community composition of denitrifiers and ammonia oxidizers differed along the moisture gradient (denitrifier: ANOSIM R = 0.739, P < 0.001; ammonia oxidizers: ANOSIM R = 0.760, P < 0.001). Individual denitrifier taxa were observed over a larger range of moisture levels than individual archaeal ammonia oxidizer taxa (Wilcoxon rank sum, W = 2413, P value = 0.0002). Together, our data suggest that variation in environmental tolerance of microbial taxa have potential to influence nitrogen cycling in terrestrial ecosystems.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. 1.

    Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH (2010) Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 4:337–345. doi:10.1038/ismej.2009.122

    Article  PubMed  Google Scholar 

  2. 2.

    Gutknecht JLM, Goodman RM, Balser TC (2006) Linking soil process and microbial ecology in freshwater wetland ecosystems. Plant Soil 289:17–34. doi:10.1007/s11104-006-9105-4

    CAS  Article  Google Scholar 

  3. 3.

    Ikenaga M, Guevara R, Dean AL, Pisani C, Boyer JN (2010) Changes in community structure of sediment bacteria along the Florida Coastal Everglades marsh-mangrove-seagrass salinity gradient. Microb Ecol 59:284–295. doi:10.1007/s00248-009-9572-2

    Article  PubMed  Google Scholar 

  4. 4.

    Pett-Ridge J, Firestone MK (2005) Redox fluctuation structures microbial communities in a wet tropical soil. Appl Environ Microbiol 71:6998–7007. doi:10.1128/aem.71.11.6998-7007.2005

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  5. 5.

    Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351. doi:10.1038/ismej.2010.58

    Article  PubMed  Google Scholar 

  6. 6.

    Swan BK, Ehrhardt CJ, Reifel KM, Moreno LI, Valentine DL (2010) Archaeal and bacterial communities respond differently to environmental gradients in anoxic sediments of a California hypersaline lake, the Salton Sea. Appl Environ Microbiol 76:757–768. doi:10.1128/aem.02409-09

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  7. 7.

    Shelford VE (1913) Animal communities in a Temperate America. University of Chicago Press, Chicago, IL

    Google Scholar 

  8. 8.

    Grinnell J (1917) The niche relationship of the California Thrasher. Auk 34:427–433

    Article  Google Scholar 

  9. 9.

    Hughes JB (2000) The scale of resource specialization and the distribution and abundance of lycaenid butterflies. Oecologia 123:375–383. doi:10.1007/s004420051024

    Article  Google Scholar 

  10. 10.

    Silvertown J, Dodd M, Gowing D, Lawson C, McConway K (2006) Phylogeny and the hierarchical organization of plant diversity. Ecology 87:S39–S49, doi:10.1890/0012-9658(2006)87[39:PATHOO]2.0.CO;2

    Article  PubMed  Google Scholar 

  11. 11.

    Soberon J (2007) Grinnellian and Eltonian niches and geographic distributions of species. Ecol Lett 10:1115–1123. doi:10.1111/j.1461-0248.2007.01107.x

    Article  PubMed  Google Scholar 

  12. 12.

    Giri B, Giang P, Kumari R, Prasad R, Varma A (2005) Microbial diversity in soils. In: Buscot F, Varma A (eds) Microorganisms in soils: roles in genesis and functions. Springer, Berlin, pp 19–55

    Google Scholar 

  13. 13.

    Strickland MS, Lauber C, Fierer N, Bradford MA (2009) Testing the functional significance of microbial community composition. Ecology 90:441–451. doi:10.1111/j.1574-6941.2007.00386.x

    Article  PubMed  Google Scholar 

  14. 14.

    DeAngelis KM, Silver WL, Thompson AW, Firestone MK (2010) Microbial communities acclimate to recurring changes in soil redox potential status. Environ Microbiol 12:3137–3149. doi:10.1111/j.1462-2920.2010.02286.x

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Picek T, Šimek M, Santruckova H (2000) Microbial responses to fluctuation of soil aeration status and redox conditions. Biol Fertil Soils 31:315–322. doi:10.1007/s003740050662

    CAS  Article  Google Scholar 

  16. 16.

    Keddy PA (2000) Wetland ecology: principles and conservation. Cambridge University Press, Cambridge

    Google Scholar 

  17. 17.

    Francis CA, Beman JM, Kuypers MMM (2007) New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. ISME J 1:19–27. doi:10.1038/ismej.2007.8

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Wallenstein MD, Myrold DD, Firestone M, Voytek M (2006) Environmental controls on denitrifying communities and denitrification rates: insights from molecular methods. Ecol Appl 16:2143–2152, doi:10.1890/1051-0761(2006)016[2143:ECODCA]2.0.CO;2

    Article  PubMed  Google Scholar 

  19. 19.

    Bodelier PLE, Libochant JA, Blom C, Laanbroek HJ (1996) Dynamics of nitrification and denitrification in root-oxygenated sediments and adaptation of ammonia-oxidizing bacteria to low-oxygen or anoxic habitats. Appl Environ Microbiol 62:4100–4107. doi:10.1364/AO.35.002649

    PubMed Central  CAS  PubMed  Google Scholar 

  20. 20.

    Jayakumar A, O’Mullan GD, Naqvi SWA, Ward BB (2009) Denitrifying bacterial community composition changes associated with stages of denitrification in oxygen minimum zones. Microb Ecol 58:350–362. doi:10.1007/s00248-009-9487-y

    CAS  Article  PubMed  Google Scholar 

  21. 21.

    Nogales B, Timmis KN, Nedwell DB, Osborn AM (2002) Detection and diversity of expressed denitrification genes in estuarine sediments after reverse transcription-PCR amplification from mRNA. Appl Environ Microbiol 68:5017–5025. doi:10.1128/aem.68.10.5017-5025.2002

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  22. 22.

    Rich JJ, Heichen RS, Bottomley PJ, Cromack K, Myrold DD (2003) Community composition and functioning of denitrifying bacteria from adjacent meadow and forest soils. Appl Environ Microbiol 69:5974–5982. doi:10.1128/aem.69.10.5974-5982.2003

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  23. 23.

    Rich JJ, Myrold DD (2004) Community composition and activities of denitrifying bacteria from adjacent agricultural soil, riparian soil, and creek sediment in Oregon, USA. Soil Biol Biochem 36:1431–1441. doi:10.1016/j.soilbio.2004.03.008

    CAS  Article  Google Scholar 

  24. 24.

    Peralta AL, Matthews JW, Kent AD (2010) Microbial community structure and denitrification in a wetland mitigation bank. Appl Environ Microbiol 76:4207–4215. doi:10.1128/aem.02977-09

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  25. 25.

    Cavigelli MA, Robertson GP (2000) The functional significance of denitrifier community composition in a terrestrial ecosystem. Ecology 81:1402–1414, doi:10.1890/0012-9658(2000)081[1402:TFSODC]2.0.CO;2

    Article  Google Scholar 

  26. 26.

    Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Ann Rev Microbiol 55:485–529. doi:10.1146/annurev.micro.55.1.485

    CAS  Article  Google Scholar 

  27. 27.

    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. Proc Natl Acad Sci USA 102:14683–14688. doi:10.1073/pnas.0506625102

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  28. 28.

    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. doi:10.1111/j.1574-6976.2009.00179.x

    CAS  Article  PubMed  Google Scholar 

  29. 29.

    Prosser JI, Nicol GW (2008) Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ Microbiol 10:2931–2941. doi:10.1111/j.1462-2920.2008.01775.x

    CAS  Article  PubMed  Google Scholar 

  30. 30.

    Caffrey JM, Bano N, Kalanetra K, Hollibaugh JT (2007) Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia. ISME J 1:660–662. doi:10.1038/ismej.2007.79

    Article  PubMed  Google Scholar 

  31. 31.

    Martens-Habbena W, Berube PM, Urakawa H, de la Torre JR, Stahl DA (2009) Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria. Nature 461:976–981. doi:10.1038/nature08465

    CAS  Article  PubMed  Google Scholar 

  32. 32.

    Moin NS, Nelson KA, Bush A, Bernhard AE (2009) Distribution and diversity of archaeal and bacterial ammonia oxidizers in salt marsh sediments. Appl Environ Microbiol 75:7461–7468, doi: :10.1128/aem.01001-09

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  33. 33.

    Lennon JT, Aanderud ZT, Lehmkuhl BK, Schoolmaster DR (2012) Mapping the niche space of soil microorganisms using taxonomy and traits. Ecology 93:1867–1879

    Article  PubMed  Google Scholar 

  34. 34.

    Gee GW, Bauder JW (1979) Particle-size analysis by hydrometer—simplified method for routine textural analysis and a sensitivity test of measurement parameters. Soil Sci Soc Am J 43:1004–1007

    Article  Google Scholar 

  35. 35.

    Wang DL, Anderson DW (1998) Direct measurement of organic carbon content in soils by the leco CR-12 carbon analyzer. Commun Soil Sci Plan 29:15–21. doi:10.1080/00103629809369925

    CAS  Article  Google Scholar 

  36. 36.

    Kent AD, Yannarell AC, Rusak JA, Triplett EW, McMahon KD (2007) Synchrony in aquatic microbial community dynamics. ISME J 1:38–47. doi:10.1038/ismej.2007.6

    CAS  Article  PubMed  Google Scholar 

  37. 37.

    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. Anton Leeuw Int J G 86:339–347. doi:10.1007/s10482-004-0498-x

    Article  Google Scholar 

  38. 38.

    Yannarell AC, Triplett EW (2005) Geographic and environmental sources of variation in lake bacterial community composition. Appl Environ Microbiol 71:227–239. doi:10.1128/aem.71.1.227-239.2005

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  39. 39.

    Fierer N, Schimel JP (2003) A proposed mechanism for the pulse in carbon dioxide production commonly observed following the rapid rewetting of a dry soil. Soil Sci Soc Am J 67:798–805. doi:10.2307/3546335

    CAS  Article  Google Scholar 

  40. 40.

    Legendre P, Legendre L (1998) Numerical ecology. Elsevier, Amsterdam

    Google Scholar 

  41. 41.

    Decaens T (2010) Macroecological patterns in soil communities. Global Ecol Biogeogr 19:287–302. doi:10.1111/j.1466-8238.2009.00517.x

    Article  Google Scholar 

  42. 42.

    Smith J, Wagner-Riddle C, Dunfield K (2010) Season and management related changes in the diversity of nitrifying and denitrifying bacteria over winter and spring. Appl Soil Ecol 44:138–146. doi:10.1016/j.apsoil.2009.11.004

    Article  Google Scholar 

  43. 43.

    Šimek M, Cooper JE (2002) The influence of soil pH on denitrification: progress towards the understanding of this interaction over the last 50 years. Eur J Soil Sci 53:345–354. doi:10.1046/j.1365-2389.2002.00461.x

    Article  Google Scholar 

  44. 44.

    Henderson SL, Dandie CE, Patten CL, Zebarth BJ, Burton DL, Trevors JT, Goyer C (2010) Changes in denitrifier abundance, denitrification gene mRNA levels, nitrous oxide emissions, and denitrification in anoxic soil microcosms amended with glucose and plant residues. Appl Environ Microbiol 76:2155–2164. doi:10.1128/aem.02993-09

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  45. 45.

    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. doi:10.1111/j.1462-2920.2008.01701.x

    CAS  Article  PubMed  Google Scholar 

  46. 46.

    Bernhard AE, Landry ZC, Blevins A, de laTorre JR, Giblin AE, Stahl DA (2010) Abundance of ammonia-oxidizing archaea and bacteria along an estuarine salinity gradient in relation to potential nitrification rates. Appl Environ Microbiol 76:1285–1289. doi:10.1128/aem.02018-09

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  47. 47.

    Philippot L (2002) Denitrifying genes in bacterial and archaeal genomes. BBA-Gene Struct Expr 1577:355–376. doi:10.1016/S0167-4781(02)00420-7

    CAS  Article  Google Scholar 

  48. 48.

    Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol R 61:533–616, 10.1.1.110.7225

    CAS  Google Scholar 

  49. 49.

    Blom C (1999) Adaptations to flooding stress: from plant community to molecule. Plant Biol 1:261–273. doi:10.1111/j.1438-8677.1999.tb00252.x

    CAS  Article  Google Scholar 

  50. 50.

    Bodelier PLE, Wijlhuizen AG, Blom C, Laanbroek HJ (1997) Effects of photoperiod on growth of and denitrification by Pseudomonas chlororaphis in the root zone of Glyceria maxima, studied in a gnotobiotic microcosm. Plant Soil 190:91–103. doi:10.1023/A:1004212814097

    CAS  Article  Google Scholar 

  51. 51.

    Prosser JI (2007) The ecology of nitrifying bacteria. In: Bothe H, Ferguson SJ, Newton WE (eds) Biology of the nitrogen cycle. Elsevier, Oxford, pp 223–244

    Google Scholar 

  52. 52.

    Worthen WB (1996) Community composition and nested-subset analyses: basic descriptors for community ecology. Oikos 76:417–426

    Article  Google Scholar 

  53. 53.

    Naeem S, Wright JP (2003) Disentangling biodiversity effects on ecosystem functioning: deriving solutions to a seemingly insurmountable problem. Ecol Lett 6:567–579. doi:10.1046/j.1461-0248.2003.00471.x

    Article  Google Scholar 

  54. 54.

    Petchey OL, Gaston KJ (2006) Functional diversity: back to basics and looking forward. Ecol Lett 9:741–758. doi:10.1111/j.1461-0248.2006.00924.x

    Article  PubMed  Google Scholar 

  55. 55.

    Botton S, van Heusden M, Parsons JR, Smidt H, van Straalen N (2006) Resilience of microbial systems towards disturbances. Crit Rev Microbiol 32:101–112. doi:10.1080/10408410600709933

    CAS  Article  PubMed  Google Scholar 

  56. 56.

    Folke C, Holling CS, Perrings C (1996) Biological diversity, ecosystems, and the human scale. Ecol Appl 6:1018–1024. doi:10.2307/2269584

    Article  Google Scholar 

  57. 57.

    Loreau M, Mouquet N, Gonzalez A (2003) Biodiversity as spatial insurance in heterogeneous landscapes. Proc Natl Acad Sci USA 100:12765–12770. doi:10.1073/pnas.2235465100

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  58. 58.

    Naeem S, Li SB (1997) Biodiversity enhances ecosystem reliability. Nature 390:507–509. doi:10.1038/37348

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We would like to thank M. Lemke, S. McClure, T. Hobson, and D. Blodgett for logistical assistance in the field. Emiquon Preserve is being restored by The Nature Conservancy. S. Paver, D. Nelson, J. Tsai, and R. Darmody provided technical assistance in the laboratory and R. Lankau and E. Wheeler for statistical assistance. S. Paver, O. Sinno and R. Andrus assisted in the field. Y. Cao, J. Dalling, M. Wander, K. Amato, S. Paver, C. Allsup, D. Keymer, E. Wheeler, A. Yannarell, and two anonymous reviewers contributed helpful comments to earlier versions of this manuscript. This work was supported by the Cooperative State Research, Education and Extension Service, U.S. Department of Agriculture, under project number ILLU 875-374. This research was also supported, in part, by the Program in Ecology, Evolution, and Conservation Biology at the University of Illinois at Urbana–Champaign.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Angela D. Kent.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 467 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Peralta, A.L., Matthews, J.W. & Kent, A.D. Habitat Specialization Along a Wetland Moisture Gradient Differs Between Ammonia-oxidizing and Denitrifying Microorganisms. Microb Ecol 68, 339–350 (2014). https://doi.org/10.1007/s00248-014-0407-4

Download citation

Keywords

  • Denitrification
  • Environmental Gradient
  • Terminal Restriction Fragment Length Polymorphism
  • Cetyl Trimethyl Ammonium Bromide
  • Microbial Community Composition