Microbial Ecology

, Volume 59, Issue 3, pp 563–573 | Cite as

Relationship Between Soil Properties and Patterns of Bacterial β-diversity Across Reclaimed and Natural Boreal Forest Soils

  • Pedro A. DimitriuEmail author
  • Susan J. Grayston
Soil Microbiology


Productivity gradients in the boreal forest are largely determined by regional-scale changes in soil conditions, and bacterial communities are likely to respond to these changes. Few studies, however, have examined how variation in specific edaphic properties influences the composition of soil bacterial communities along environmental gradients. We quantified bacterial compositional diversity patterns in ten boreal forest sites of contrasting fertility. Bulk soil (organic and mineral horizons) was sampled from sites representing two extremes of a natural moisture-nutrient gradient and two distinct disturbance types, one barren and the other vegetation-rich. We constructed 16S rRNA gene clone libraries to characterize the bacterial communities under phylogenetic- and species-based frameworks. Using a nucleotide analog to label DNA-synthesizing bacteria, we also assessed the composition of active taxa in disturbed sites. Most sites were dominated by sequences related to the α-Proteobacteria, followed by acidobacterial and betaproteobacterial sequences. Non-parametric multivariate regression indicated that pH, which was lowest in the natural sites, explained 34% and 16% of the variability in community structure as determined by phylogenetic-based (UniFrac distances) and species-based (Jaccard similarities) metrics, respectively. Soil pH was also a significant predictor of richness (Chao1) and diversity (Shannon) measures. Within the natural edaphic gradient, soil moisture accounted for 32% of the variance in phylogenetic (but not species) community structure. In the boreal system we studied, bacterial β-diversity patterns appear to be largely related to “master” variables (e.g., pH, moisture) rather than to observable attributes (e.g., plant cover) leading to regional-scale fertility gradients.


Bacterial Community Clone Library Natural Site Bacterial Community Composition Organic Horizon 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We want to thank David Lee for his invaluable help with the construction of clone libraries. Support for this work was provided by NSERC Collaborative Research and Development (CRD) grant CRDPJ 305475-03.


  1. 1.
    Agnelli A, Ascher J, Corti G, Ceccherini MT, Nannipieri P, Pietramellara G (2004) Distribution of microbial communities in a forest soil profile investigated by microbial biomass, soil respiration and DGGE of total and extracellular DNA. Soil Biol Biochem 36:859–868CrossRefGoogle Scholar
  2. 2.
    Allison SD, Czimczik CI, Treseder KK (2008) Microbial activity and soil respiration under nitrogen addition in Alaskan boreal forest. Glob Chang Biol 14:1156–1164CrossRefGoogle Scholar
  3. 3.
    Allison SD, Hanson CA, Treseder KK (2007) Nitrogen fertilization reduces diversity and alters community structure of active fungi in boreal ecosystems. Soil Biol Biochem 39:1878–1887CrossRefGoogle Scholar
  4. 4.
    Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–35CrossRefGoogle Scholar
  5. 5.
    Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ (2006) New screening software shows that most recent large 16S rRNA gene clone libraries contain chimeras. Appl Environ Microbiol 72:5734–574CrossRefPubMedGoogle Scholar
  6. 6.
    Axelrood PE, Chow ML, Radomski CC, McDermott JM, Davies J (2002) Molecular characterization of bacterial diversity from British Columbia forest soils subjected to disturbance. Can J Microbiol 48:655–667CrossRefPubMedGoogle Scholar
  7. 7.
    Bååth E, Anderson TH (2003) Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biol Biochem 35:955–963CrossRefGoogle Scholar
  8. 8.
    Bach LH, Frostegard A, Ohlson M (2008) Variation in soil microbial communities across a boreal spruce forest landscape. Can J For Res 38:1504–1514CrossRefGoogle Scholar
  9. 9.
    Beckingham JD, Archibald JH (1996) Field guide to ecosites of northern Alberta. Canadian Forest Service, EdmontonGoogle Scholar
  10. 10.
    Bengtson P, Basiliko N, Prescott CE, Grayston SJ (2007) Spatial dependency of soil nutrient availability and microbial properties in a mixed forest of Tsuga heterophylla and Pseudotsuga menziesii, in coastal British Columbia, Canada. Soil Biol Biochem 39:2429–2436CrossRefGoogle Scholar
  11. 11.
    Bois G, Pichó Y, Fung MYP, Khasa DP (2005) Mycorrhizal inoculum potentials of pure reclamation materials and revegetated tailing sands from the Canadian oil sand industry. Mycorrhiza 15:149–157CrossRefPubMedGoogle Scholar
  12. 12.
    Chan OC, Yang X, Fu Y, Feng Z, Sha L, Casper P, Zou X (2006) 16S rRNA gene analyses of bacterial community structures in the soils of evergreen broad-leaved forests in south-west China. FEMS Microbiol Ecol 58:247–254CrossRefPubMedGoogle Scholar
  13. 13.
    Chapin FS III, Mcguire AD, Randerson J, Pielke R, Baldocchi D, Hobbie SE, Roulet N, Eugster W, Kasischke E, Rastetter EB, Zimov SA, Running SW (2000) Arctic and boreal ecosystems of western North America as components of the climate system. Glob Chang Biol 6:211–223CrossRefGoogle Scholar
  14. 14.
    DeSantis TZ, Brodie EL, Moberg JP, Zubieta IX, Piceno YM, Andersen GL (2007) High-density universal 16S rRNA microarray analysis reveals broader diversity than typical clone library when sampling the environment. Microb Ecol 53:371–381CrossRefPubMedGoogle Scholar
  15. 15.
    Dimitriu PA, Pinkart HC, Peyton BM, Mormile MR (2008) Spatial and temporal patterns in the microbial fiversity of a meromictic soda lake in Washington State. Appl Environ Microbiol 74:4877–4888CrossRefPubMedGoogle Scholar
  16. 16.
    Elshahed MS, Youssef NH, Spain AM, Sheik C, Najar FZ, Sukharnikov LO, Roe BA, Davis JP, Schloss PD, Bailey VL, Krumholz LR (2008) Novelty and uniqueness patterns of rare members of the soil biosphere. Appl Environ Microbiol 74:5422–5433CrossRefPubMedGoogle Scholar
  17. 17.
    Felske A, Wolterink A, van Lis R, de Vos WM, Akkermans ADL (2000) Response of a soil bacterial community to grassland succession as monitored by 16S rRNA levels of the predominant ribotypes. Appl Environ Microbiol 66:3998–4003CrossRefPubMedGoogle Scholar
  18. 18.
    Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1361CrossRefPubMedGoogle Scholar
  19. 19.
    Fierer N, Carney KM, Horner-Devine MC, Megonigal JP (2009) The biogeography of ammonia-oxidizing bacterial communities in soil. Microb Ecol 58:435–445CrossRefPubMedGoogle Scholar
  20. 20.
    Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626–631CrossRefPubMedGoogle Scholar
  21. 21.
    Girvan MS, Bullimore J, Pretty JN, Osborn AM, Ball AS (2003) Soil type is the primary determinant of the composition of the total and active bacterial communities in arable soils. Appl Environ Microbiol 69:1800–1809CrossRefPubMedGoogle Scholar
  22. 22.
    Hackl E, Pfeffer M, Donat C, Bachmann G, Zechmeister-Boltenstern S (2005) Composition of the microbial communities in the mineral soil under different types of natural forest. Soil Biol Biochem 37:661–673CrossRefGoogle Scholar
  23. 23.
    Hackl E, Zechmeister-Boltenstern S, Bodrossy L, Sessitsch A (2004) Comparison of diversities and compositions of bacterial populations inhabiting natural forest soils. Appl Environ Microbiol 70:5057–5065CrossRefPubMedGoogle Scholar
  24. 24.
    Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  25. 25.
    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 3:597–605CrossRefPubMedGoogle Scholar
  26. 26.
    Hanson CA, Allison SD, Bradford MA, Wallenstein MD, Treseder KK (2008) Fungal taxa target different carbon sources in forest soil. Ecosystems 11:1157–1169CrossRefGoogle Scholar
  27. 27.
    Harris RF (1981) Effect of water potential on microbial growth and activity. In: Parr JF, Gardner WR, Elliott LF (eds) Water potential relations in soil microbiology. Soil Science Society of America, Madison, pp 23–95Google Scholar
  28. 28.
    Högberg MN, Högberg P, Myrold DD (2007) Is microbial community composition in boreal forest soils determined by pH, C-to-N ratio, the trees, or all three? Oecologia 150:590–599CrossRefPubMedGoogle Scholar
  29. 29.
    Johnson EA, Miyanishi K (2008) Creating new landscapes and ecosystems: the Alberta oil sands. Ann NY Acad Sci 1134:120–133CrossRefPubMedGoogle Scholar
  30. 30.
    Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R, Fierer N (2009) A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 3:442–450CrossRefPubMedGoogle Scholar
  31. 31.
    Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175Google Scholar
  32. 32.
    Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2418CrossRefGoogle Scholar
  33. 33.
    Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8236CrossRefPubMedGoogle Scholar
  34. 34.
    Lozupone CA, Hamady M, Kelley ST, Knight R (2007) Quantitative and qualitative β-diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microbiol 73:1576–1585CrossRefPubMedGoogle Scholar
  35. 35.
    Lozupone CA, Knight R (2008) Species divergence and the measurement of microbial diversity. FEMS Microbiol Rev 32:557–568CrossRefPubMedGoogle Scholar
  36. 36.
    Martin AP (2002) Phylogenetic approaches for describing and comparing the diversity of microbial communities. Appl Environ Microbiol 68:3673–3680CrossRefPubMedGoogle Scholar
  37. 37.
    McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–294CrossRefGoogle Scholar
  38. 38.
    McCaig AE, Glover LA, Prosser JI (1999) Molecular analysis of bacterial community structure and diversity in unimproved and improved upland grass pastures. Appl Environ Microbiol 65:1721–1730PubMedGoogle Scholar
  39. 39.
    McMillan R, Quideau SA, MacKenzie MD, Biryukova O (2007) Nitrogen mineralization and microbial activity in oil sands reclaimed boreal forest soils. J Environ Qual 36:1470–1481CrossRefPubMedGoogle Scholar
  40. 40.
    Metje M, Frenzel P (2005) Effect of temperature on anaerobic ethanol oxidation and methanogenesis in acidic peat from a northern wetland. Appl Environ Microbiol 71:8191–8200CrossRefPubMedGoogle Scholar
  41. 41.
    Mieszkin S, Furet J-P, Corthier G, Gourmelon M (2009) Estimation of pig fecal contamination in a river catchment by real-time PCR using two pig-specific Bacteroidales 16S rRNA genetic markers. Appl Environ Microbiol 75:3045–3054CrossRefPubMedGoogle Scholar
  42. 42.
    Mohanty SR, Bodelier PLE, Floris V, Conrad R (2006) Differential effects of nitrogenous fertilizers on methane-consuming microbes in rice field and forest soils. Appl Environ Microbiol 72:1346–1356CrossRefPubMedGoogle Scholar
  43. 43.
    Mummey DL, Stahl PD, Buyer JS (2002) Soil microbiological properties 20 years after surface mine reclamation: spatial analysis of reclaimed and undisturbed sites. Soil Biol Biochem 34:1717–1728CrossRefGoogle Scholar
  44. 44.
    Neufeld JD, Mohn WW (2005) Unexpectedly high bacterial diversity in arctic tundra relative to boreal forest soils, revealed by serial analysis of ribosomal sequence tags. Appl Environ Microbiol 71:5710–5717CrossRefPubMedGoogle Scholar
  45. 45.
    Pennanen T, Liski J, Bååth E, Kitunen V, Uotila J, Westman CJ, Fritze H (1999) Structure of the microbial communities in coniferous forest soils in relation to site fertility and stand development stage. Microb Ecol 38:168–177CrossRefPubMedGoogle Scholar
  46. 46.
    Priha O, Grayston SJ, Hiukka R, Pennanen T, Smolander A (2001) Microbial community structure and characteristics of the organic matter in soils under Pinus sylvestris, Picea abies and Betula pendula at two forest sites. Biol Fertil Soils 33:17–27CrossRefGoogle Scholar
  47. 47.
    Quoreshi AM (2008) The use of mycorrhizal biotechnology in restoration of disturbed ecosystem. In: Siddiqui ZA, Akhtar MS, Kazuyoshi F (eds) Mycorrhizae: sustainable agriculture and forestry. Springer, Amsterdam, pp 303–320CrossRefGoogle Scholar
  48. 48.
    Rowland S, Prescott CE, Grayston SJ, Quideau SA, Bradfield GE (2009) Recreating a functioning forest soil in reclaimed oil sands in northern Alberta: an approach for measuring success in ecological restoration. J Environ Qual 38:1580–1590CrossRefPubMedGoogle Scholar
  49. 49.
    Saetre P, Bååth E (2000) Spatial variation and patterns of soil microbial community structure in a mixed spruce–birch stand. Soil Biol Biochem 32:909–917CrossRefGoogle Scholar
  50. 50.
    Schloss PD (2008) Evaluating different approaches that test whether microbial communities have the same structure. ISME J 2:265–274CrossRefPubMedGoogle Scholar
  51. 51.
    Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1511CrossRefPubMedGoogle Scholar
  52. 52.
    Schloss PD, Handelsman J (2006) Introducing TreeClimber, a test to compare microbial community structures. Appl Environ Microbiol 72:2379–2384CrossRefPubMedGoogle Scholar
  53. 53.
    Smit E, Leeflang P, Gommans S, van den Broek J, van Mil S, Wernars K (2001) Diversity and seasonal fluctuations of the dominant members of the bacterial soil community in a wheat field as determined by cultivation and molecular methods. Appl Environ Microbiol 67:2284–2293CrossRefPubMedGoogle Scholar
  54. 54.
    Smith NR, Kishchuk BE, Mohn WW (2008) Effects of wildfire and harvest disturbances on forest soil bacterial communities. Appl Environ Microbiol 74:216–226CrossRefPubMedGoogle Scholar
  55. 55.
    Staddon WJ, Trevors JT, Duchesne LC, Colombo C (1998) Soil microbial diversity and community structure across a climatic gradient in western Canada. Biodivers Conserv 7:1081–1092CrossRefGoogle Scholar
  56. 56.
    Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web-servers. Syst Biol 75:758–771CrossRefGoogle Scholar
  57. 57.
    Stephen JR, Kowalchuk GA, Bruns MAV, McCaig AE, Phillips CJ, Embley TM (1998) Analysis of β-subgroup proteobacterial ammonia oxidizer populationsin soil by denaturing gradient gel electrophoresis analysis and hierarchical phylogenetic probing. Appl Environ Microbiol 64:2958–2965PubMedGoogle Scholar
  58. 58.
    Thormann MN, Bayley SE, Currah RS (2004) Microcosm tests of the effects of temperature and microbial species number on the decomposition of Carex aquatilis and Sphagnum fuscum litter from southern boreal peatlands. Can J Microbiol 50:793–804CrossRefPubMedGoogle Scholar
  59. 59.
    Treseder KK, Turner KM, Mack MC (2007) Mycorrhizal responses to nitrogen fertilization in boreal ecosystems: potential consequences for soil carbon storage. Glob Chang Biol 13:78CrossRefGoogle Scholar
  60. 60.
    Treves DS, Xia B, Zhou J, Tiedje JM (2003) A two-species test of the hypothesis that spatial isolation influences microbial diversity in soil. Microb Ecol 45:20–28CrossRefPubMedGoogle Scholar
  61. 61.
    Tsai SH, Selvam A, Chang Y-P, Yang S-S (2009) Soil bacterial community composition across different topographic sites characterized by 16S rRNA gene clones in the Fushan forest of Taiwan. Bot Stud 50:57–68Google Scholar
  62. 62.
    Wakelin SA, Gregg AL, Simpson RJ, Li GD, Riley IT, McKay AC (2009) Pasture management clearly affects soil microbial community structure and N-cycling bacteria. Pedobiologia 52:237–247CrossRefGoogle Scholar
  63. 63.
    Yin B, Crowley D, Sparovek G, de Melo WJ, Borneman J (2000) Bacterial functional redundancy along a soil reclamation gradient. Appl Environ Microbiol 66:4361–4365CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.Department of Forest SciencesUniversity of British ColumbiaVancouverCanada

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