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

  • Soil Microbiology
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Abstract

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.

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References

  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 36:859–868

    Article  CAS  Google Scholar 

  2. Allison SD, Czimczik CI, Treseder KK (2008) Microbial activity and soil respiration under nitrogen addition in Alaskan boreal forest. Glob Chang Biol 14:1156–1164

    Article  Google Scholar 

  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 39:1878–1887

    Article  CAS  Google Scholar 

  4. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–35

    Article  Google Scholar 

  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 72:5734–574

    Article  CAS  PubMed  Google Scholar 

  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 48:655–667

    Article  CAS  PubMed  Google Scholar 

  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 35:955–963

    Article  CAS  Google Scholar 

  8. Bach LH, Frostegard A, Ohlson M (2008) Variation in soil microbial communities across a boreal spruce forest landscape. Can J For Res 38:1504–1514

    Article  CAS  Google Scholar 

  9. Beckingham JD, Archibald JH (1996) Field guide to ecosites of northern Alberta. Canadian Forest Service, Edmonton

    Google Scholar 

  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 39:2429–2436

    Article  CAS  Google Scholar 

  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 15:149–157

    Article  CAS  PubMed  Google Scholar 

  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 58:247–254

    Article  CAS  PubMed  Google Scholar 

  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 6:211–223

    Article  Google Scholar 

  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 53:371–381

    Article  CAS  PubMed  Google Scholar 

  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 74:4877–4888

    Article  CAS  PubMed  Google Scholar 

  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 74:5422–5433

    Article  CAS  PubMed  Google Scholar 

  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 66:3998–4003

    Article  CAS  PubMed  Google Scholar 

  18. Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1361

    Article  PubMed  Google Scholar 

  19. Fierer N, Carney KM, Horner-Devine MC, Megonigal JP (2009) The biogeography of ammonia-oxidizing bacterial communities in soil. Microb Ecol 58:435–445

    Article  PubMed  Google Scholar 

  20. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626–631

    Article  CAS  PubMed  Google Scholar 

  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 69:1800–1809

    Article  CAS  PubMed  Google Scholar 

  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 37:661–673

    Article  CAS  Google Scholar 

  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 70:5057–5065

    Article  CAS  PubMed  Google Scholar 

  24. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  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 3:597–605

    Article  CAS  PubMed  Google Scholar 

  26. Hanson CA, Allison SD, Bradford MA, Wallenstein MD, Treseder KK (2008) Fungal taxa target different carbon sources in forest soil. Ecosystems 11:1157–1169

    Article  CAS  Google Scholar 

  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 23–95

    Google Scholar 

  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 150:590–599

    Article  PubMed  Google Scholar 

  29. Johnson EA, Miyanishi K (2008) Creating new landscapes and ecosystems: the Alberta oil sands. Ann NY Acad Sci 1134:120–133

    Article  CAS  PubMed  Google Scholar 

  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 3:442–450

    Article  CAS  PubMed  Google Scholar 

  31. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175

    Google Scholar 

  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 40:2407–2418

    Article  CAS  Google Scholar 

  33. Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8236

    Article  CAS  PubMed  Google Scholar 

  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 73:1576–1585

    Article  CAS  PubMed  Google Scholar 

  35. Lozupone CA, Knight R (2008) Species divergence and the measurement of microbial diversity. FEMS Microbiol Rev 32:557–568

    Article  CAS  PubMed  Google Scholar 

  36. Martin AP (2002) Phylogenetic approaches for describing and comparing the diversity of microbial communities. Appl Environ Microbiol 68:3673–3680

    Article  CAS  PubMed  Google Scholar 

  37. McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–294

    Article  Google Scholar 

  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 65:1721–1730

    CAS  PubMed  Google Scholar 

  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 36:1470–1481

    Article  CAS  PubMed  Google Scholar 

  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 71:8191–8200

    Article  CAS  PubMed  Google Scholar 

  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 75:3045–3054

    Article  CAS  PubMed  Google Scholar 

  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 72:1346–1356

    Article  CAS  PubMed  Google Scholar 

  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 34:1717–1728

    Article  CAS  Google Scholar 

  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 71:5710–5717

    Article  CAS  PubMed  Google Scholar 

  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 38:168–177

    Article  PubMed  Google Scholar 

  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 33:17–27

    Article  CAS  Google Scholar 

  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 303–320

    Chapter  Google Scholar 

  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 38:1580–1590

    Article  CAS  PubMed  Google Scholar 

  49. Saetre P, Bååth E (2000) Spatial variation and patterns of soil microbial community structure in a mixed spruce–birch stand. Soil Biol Biochem 32:909–917

    Article  CAS  Google Scholar 

  50. Schloss PD (2008) Evaluating different approaches that test whether microbial communities have the same structure. ISME J 2:265–274

    Article  PubMed  Google Scholar 

  51. Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1511

    Article  CAS  PubMed  Google Scholar 

  52. Schloss PD, Handelsman J (2006) Introducing TreeClimber, a test to compare microbial community structures. Appl Environ Microbiol 72:2379–2384

    Article  CAS  PubMed  Google Scholar 

  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 67:2284–2293

    Article  CAS  PubMed  Google Scholar 

  54. Smith NR, Kishchuk BE, Mohn WW (2008) Effects of wildfire and harvest disturbances on forest soil bacterial communities. Appl Environ Microbiol 74:216–226

    Article  CAS  PubMed  Google Scholar 

  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 7:1081–1092

    Article  Google Scholar 

  56. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web-servers. Syst Biol 75:758–771

    Article  Google Scholar 

  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 64:2958–2965

    CAS  PubMed  Google Scholar 

  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 50:793–804

    Article  CAS  PubMed  Google Scholar 

  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 13:78

    Article  Google Scholar 

  60. Treves DS, **a B, Zhou J, Tiedje JM (2003) A two-species test of the hypothesis that spatial isolation influences microbial diversity in soil. Microb Ecol 45:20–28

    Article  CAS  PubMed  Google Scholar 

  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 50:57–68

    CAS  Google Scholar 

  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 52:237–247

    Article  CAS  Google Scholar 

  63. Yin B, Crowley D, Sparovek G, de Melo WJ, Borneman J (2000) Bacterial functional redundancy along a soil reclamation gradient. Appl Environ Microbiol 66:4361–4365

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

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.

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Correspondence to Pedro A. Dimitriu.

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Dimitriu, P.A., Grayston, S.J. Relationship Between Soil Properties and Patterns of Bacterial β-diversity Across Reclaimed and Natural Boreal Forest Soils. Microb Ecol 59, 563–573 (2010). https://doi.org/10.1007/s00248-009-9590-0

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