Plant community and nitrogen deposition as drivers of alpha and beta diversities of prokaryotes in reconstructed oil sand soils and natural boreal forest soils

Applied and Environmental Microbiology

Volumn 83, Issue 9, 2017, Pages

  Masse, Jacynthe ^a,b   Prescott, Cindy E ^a   Renaut, Sébastien ^b   Terrat, Yves ^b   Grayston, Sue J ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Biodiversity; Boreal forest soil; Microbial community; Nitrogen deposition; Oil sands; Plant community; Soil microbiology; Soil restoration

Indexed keywords

BACTERIA; BIODIVERSITY; CONSERVATION; DEPOSITS; FORESTRY; MICROBIOLOGY; MICROORGANISMS; NITROGEN; OIL SANDS; PETROLEUM DEPOSITS; RESTORATION; RNA; SAND;

BOREAL FORESTS; MICROBIAL COMMUNITIES; NITROGEN DEPOSITION; PLANT COMMUNITIES; SOIL MICROBIOLOGY; SOIL RESTORATION;

SOILS;

BIODIVERSITY; CONIFEROUS TREE; DECIDUOUS TREE; FOREST SOIL; GRASSLAND; MICROBIAL COMMUNITY; NITROGEN; OIL SAND; PLANT COMMUNITY; PROKARYOTE; SOIL MICROORGANISM; SPECIES DIVERSITY;

POACEAE; PROKARYOTA;

RIBOSOME DNA; RNA 16S; SOIL;

ARCHAEON; BACTERIUM; BIOTA; CANADA; CHEMISTRY; CLASSIFICATION; CLUSTER ANALYSIS; COMPARATIVE STUDY; DNA SEQUENCE; ECOSYSTEM RESTORATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; MICROBIOLOGY; PHYLOGENY; POACEAE; SOIL; TAIGA; TREE;

ARCHAEA; BACTERIA; BIOTA; CANADA; CLUSTER ANALYSIS; DNA, RIBOSOMAL; ENVIRONMENTAL RESTORATION AND REMEDIATION; PHYLOGENY; POACEAE; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SOIL; SOIL MICROBIOLOGY; TAIGA; TREES;

EID: 85018307901     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03319-16     Document Type: Article

References (104)

1. Government of Alberta. 2016. Alberta energy: facts and statistics. Government of Alberta, Edmonton, Alberta, Canada
2. Government of Alberta. 2012. Oil sands: the resource 1-2. Government of Alberta, Edmonton, Alberta, Canada
3. Government of Alberta. 2013. Oil sands: reclamation 1-2. Government of Alberta, Edmonton, Alberta, Canada
4. Government of Alberta. 1993. Conservation and reclamation regulation (AR 115-1993). Government of Alberta, Edmonton, Alberta, Canada
5. Powter C, Chymko N, Dinwoodie G, Howat D, Janz A, Puhlmann R, Richens T, Watson D, Sinton H, Ball K, Patterson B, Brocke L, Dyer R. 2012. Regulatory history of Alberta' s industrial land conservation and reclamation program. Can J Soil Sci 92:39-51. https://doi.org/10.4141/cjss2010-033
6. Turcotte I, Quideau SA, Oh S-W. 2009. Organic matter quality in reclaimed boreal forest soils following oil sands mining. Org Geochem 40:510-519. https://doi.org/10.1016/j.orggeochem.2009.01.003
7. Hemsley TL. 2012. Ecological response of atmospheric nitrogen depo-sition on reconstructed soils in the Athabasca Oil Sands Region. University of Alberta, Edmonton, Alberta, Canada
8. Dimitriu PA, Prescott CE, Quideau SA, Grayston SJ. 2010. Impact of reclamation of surface-mined boreal forest soils on microbial community composition and function. Soil Biol Biochem 42:2289-2297. https://doi.org/10.1016/j.soilbio.2010.09.001
9. Hahn AS, Quideau SA. 2013. Long-term effects of organic amendments on the recovery of plant and soil microbial communities following disturbance in the Canadian boreal forest. Plant Soil 363:331-344. https://doi.org/10.1007/s11104-012-1306-4
10. Chazdon RL. 2008. Beyond deforestation: restoring degraded lands. Communities 1458:1458-1460
11. Hobbs RJ, Arico S, Aronson J, Baron JS, Cramer VA, Epstein PR, Ewel JJ, Klink CA, Lugo AE, Norton D, Ojima D, Richardson DM. 2006. Novel ecosystems: theoretical and management aspects of the new ecological world order. Glob Ecol Biogeogr 15:1-7. https://doi.org/10.1111/j.1466-822X.2006.00212.x
12. Quideau SA, Swallow MJB, Prescott CE, Grayston SJ, Oh SW. 2013. Comparing soil biogeochemical processes in novel and natural boreal forest ecosystems. Biogeosciences 10:5651-5661. https://doi.org/10.5194/bg-10-5651-2013
13. Bottomley PJ, Myrold DD. 2015. Biological N inputs, p 447-470. In Paul EA (ed), Soil microbiology, ecology, and biochemistry, 4th ed. Elsevier, Inc, New York, NY
14. Robertson GP, Groffman PM. 2014. Nitrogen transformations, p 421-446. In Paul EA (ed), Soil microbiology, ecology, and biochemistry, 4th ed. Elsevier, Inc, New York, NY
15. Schimel JP, Bennett J, Fierer N. 2005. Microbial community composition and soil nitrogen cycling: is there really a connection? In Bardgett RD, Usher MB, Hopkins DW (ed), Biological diversity and function in soils. Cambridge University Press, Cambridge, United Kingdom
16. Roesch LFW, Fulthorpe RR, Riva A, Casella G, Hadwin AKM, Kent AD, Daroub SH, Camargo FAO, Farmerie WG, Triplett EW. 2007. Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1:283-290. https://doi.org/10.1038/ismej.2007.53
17. Sun H, Terhonen E, Koskinen K, Paulin L, Kasanen R, Asiegbu FO. 2014. Bacterial diversity and community structure along different peat soils in boreal forest. Appl Soil Ecol 74:37-45. https://doi.org/10.1016/j.apsoil.2013.09.010
18. Fierer N, Jackson RB. 2006. The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626-631. https://doi.org/10.1073/pnas.0507535103
19. Hansel CM, Fendorf S, Jardine PM, Francis CA. 2008. Changes in bacterial and archaeal community structure and functional diversity along a geochemically variable soil profile. Appl Environ Microbiol 74: 1620-1633. https://doi.org/10.1128/AEM.01787-07
20. Brockett BFT, Prescott CE, Grayston SJ. 2012. Soil moisture is the major factor influencing microbial community structure and enzyme activities across seven biogeoclimatic zones in western Canada. Soil Biol Biochem 44:9-20. https://doi.org/10.1016/j.soilbio.2011.09.003
21. Ferrenberg S, O'Neill SP, Knelman JE, Todd B, Duggan S, Bradley D, Robinson T, Schmidt SK, Townsend AR, Williams MW, Cleveland CC, Melbourne BA, Jiang L, Nemergut DR. 2013. Changes in assembly processes in soil bacterial communities following a wildfire disturbance. ISME J 7:1102-1111. https://doi.org/10.1038/ismej.2013.11
22. Wardle DA. 2002. Communities and ecosystems. Linking the aboveground and belowground components. Princeton University Press, Princeton, NJ
23. Grayston SJ, Prescott CE. 2005. Microbial communities in forest floors under four tree species in coastal British Columbia. Soil Biol Biochem 37:1157-1167. https://doi.org/10.1016/j.soilbio.2004.11.014
24. Prescott CE, Grayston SJ. 2013. Tree species influence on microbial communities in litter and soil: current knowledge and research needs. For Ecol Manage 309:19-27. https://doi.org/10.1016/j.foreco.2013.02.034
25. Thoms C, Gattinger A, Jacob M, Thomas FM, Gleixner G. 2010. Direct and indirect effects of tree diversity drive soil microbial diversity in temperate deciduous forest. Soil Biol Biochem 42:1558-1565. https://doi.org/10.1016/j.soilbio.2010.05.030
26. Sorenson PT, Quideau SA, MacKenzie MD, Landhäusser SM, Oh SW. 2011. Forest floor development and biochemical properties in reconstructed boreal forest soils. Appl Soil Ecol 49:139-147. https://doi.org/10.1016/j.apsoil.2011.06.006
27. Thomson MD. 1979. Ecological habitat mapping of the AOSERP study area (supplement): phase 1. Alberta Oil Sands Environmental Research Program, Edmonton, Alberta, Canada
28. Ball PN, MacKenzie MD, DeLuca TH, Montana WEH. 2010. Wildfire and charcoal enhance nitrification and ammonium-oxidizing bacterial abundance in dry montane forest soils. J Environ Qual 39:1243. https://doi.org/10.2134/jeq2009.0082
29. Hart SC, DeLuca TH, Newman GS, MacKenzie MD, Boyle SI. 2005. Postfire vegetative dynamics as drivers of microbial community structure and function in forest soils. For Ecol Manage 220:166-184. https://doi.org/10.1016/j.foreco.2005.08.012
30. Switzer JM, Hope GD, Grayston SJ, Prescott CE. 2012. Changes in soil chemical and biological properties after thinning and prescribed fire for ecosystem restoration in a Rocky Mountain Douglas fir forest. For Ecol Manage 275:1-13. https://doi.org/10.1016/j.foreco.2012.02.025
31. Dimitriu PA, Grayston SJ. 2010. Relationship between soil properties and patterns of bacterial β-diversity across reclaimed and natural boreal forest soils. Microb Ecol 59:563-573. https://doi.org/10.1007/s00248-009-9590-0
32. Anderson CR, Condron LM, Clough TJ, Fiers M, Stewart A, Hill RA, Sherlock RR. 2011. Biochar induced soil microbial community change: implications for biogeochemical cycling of carbon, nitrogen, and phosphorus. Pedobiologia 54:309-320. https://doi.org/10.1016/j.pedobi.2011.07.005
33. Koch AL. 2001. Oligotrophs versus copiotrophs. Bioessays 23:657-661. https://doi.org/10.1002/bies.1091
34. Fierer N, Bradford MA, Jackson RB. 2007. Toward an ecological classification of soil bacteria. Ecology 88:1354-1364. https://doi.org/10.1890/05-1839
35. Eilers KG, Lauber CL, Knight R, Fierer N. 2010. Shifts in bacterial community structure associated with inputs of low molecular weight carbon compounds to soil. Soil Biol Biochem 42:896-903. https://doi.org/10.1016/j.soilbio.2010.02.003
36. Fierer N, Lauber CL, Ramirez KS, Zaneveld J, Bradford MA, Knight R. 2012. Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J 6:1007-1017. https://doi.org/10.1038/ismej.2011.159
37. Li C, Yan K, Tang L, Jia Z, Li Y. 2014. Change in deep soil microbial communities due to long-term fertilization. Soil Biol Biochem 75: 264-272. https://doi.org/10.1016/j.soilbio.2014.04.023
38. Freedman Z, Zak DR. 2014. Atmospheric N deposition increases bacterial laccase-like multicopper oxidases: implications for organic matter decay. Appl Environ Microbiol 80:4460-4468. https://doi.org/10.1128/AEM.01224-14
39. Leff JW, Nemergut DR, Grandy AS, O'Neill SP, Wickings K, Townsend AR, Cleveland CC. 2012. The effects of soil bacterial community structure on decomposition in a tropical rain forest. Ecosystems 15:284-298. https://doi.org/10.1007/s10021-011-9510-2
40. Nemergut DR, Cleveland CC, Wieder WR, Washenberger CL, Townsend AR. 2010. Plot-scale manipulations of organic matter inputs to soils correlate with shifts in microbial community composition in a lowland tropical rain forest. Soil Biol Biochem 42:2153-2160. https://doi.org/10.1016/j.soilbio.2010.08.011
41. Fenn ME, Bytnerowicz A, Schilling SL, Ross CS. 2015. Atmospheric deposition of nitrogen, sulfur and base cations in jack pine stands in the Athabasca Oil Sands Region, Alberta, Canada. Environ Pollut 196: 497-510. https://doi.org/10.1016/j.envpol.2014.08.023
42. Proemse BC, Mayer B, Fenn ME, Ross CS. 2013. A multi-isotope approach for estimating industrial contributions to atmospheric nitrogen deposition in the Athabasca Oil Sands Region in Alberta, Canada. Environ Pollut 182:80-91. https://doi.org/10.1016/j.envpol.2013.07.004
43. Fontaine S, Bardoux G, Abbadie L, Mariotti A. 2004. Carbon input to soil may decrease soil carbon content. Ecol Lett 7:314-320. https://doi.org/10.1111/j.1461-0248.2004.00579.x
44. Masse J, Prescott CE, Müller C, Grayston SJ. 2016. Gross nitrogen transformation rates differ in reconstructed oil-sand soils from natural boreal-forest soils as revealed using a 15N tracing method. Geoderma 282:37-48. https://doi.org/10.1016/j.geoderma.2016.07.007
45. Angelov A, Liebl W. 2006. Insights into extreme thermoacidophily based on genome analysis of Picrophilus torridus and other thermoacidophilic archaea. J Biotechnol 126:3-10. https://doi.org/10.1016/j.jbiotec.2006.02.017
46. Lin X, Handley KM, Gilbert JA, Kostka JE. 2015. Metabolic potential of fatty acid oxidation and anaerobic respiration by abundant members of Thaumarchaeota and Thermoplasmata in deep anoxic peat. ISME J 9:2740-2744. https://doi.org/10.1038/ismej.2015.77
47. Weber EB, Lehtovirta-Morley LE, Prosser JI, Gubry-Rangin C. 2015. Ammonia oxidation is not required for growth of group 1.1c soil Thaumarchaeota. FEMS Microbiol Ecol 91:1-7. https://doi.org/10.1093/femsec/fiu014
48. 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. https://doi.org/10.1111/j.1462-2920.2008.01701.x
49. He JZ, Hu HW, Zhang LM. 2012. Current insights into the autotrophic thaumarchaeal ammonia oxidation in acidic soils. Soil Biol Biochem 55:146-154. https://doi.org/10.1016/j.soilbio.2012.06.006
50. Lehtovirta LE, Prosser JI, Nicol GW. 2009. Soil pH regulates the abundance and diversity of group 1.1c Crenarchaeota. FEMS Microbiol Ecol 70:367-376. https://doi.org/10.1111/j.1574-6941.2009.00748.x
51. Oton EV, Quince C, Nicol GW, Prosser JI, Gubry-Rangin C. 2016. Phylogenetic congruence and ecological coherence in terrestrial Thaumarchaeota. ISME J 10:85-96. https://doi.org/10.1038/ismej.2015.101
52. Nicol GW, Tscherko D, Embley TM, Prosser JI. 2005. Primary succession of soil Crenarchaeota across a receding glacier foreland. Environ Microbiol 7:337-347. https://doi.org/10.1111/j.1462-2920.2005.00698.x
53. Kemnitz D, Kolb S, Conrad R. 2007. High abundance of Crenarchaeota in a temperate acidic forest soil. FEMS Microbiol Ecol 60:442-448. https://doi.org/10.1111/j.1574-6941.2007.00310.x
54. Robertson G, Groffman PM. 2007. Nitrogen transformations, p 341-364. In Paul EA (ed), Soil microbiology, ecology, and biochemistry, 3rd ed. Elsevier, Burlington, MA
55. Mussmann M, Brito I, Pitcher A, Sinninghe Damste JS, Hatzenpichler R, Richter A, Nielsen JL, Nielsen PH, Muller A, Daims H, Wagner M, Head IM. 2011. Thaumarchaeotes abundant in refinery nitrifying sludges express amoA but are not obligate autotrophic ammonia oxidizers. Proc Natl Acad Sci U S A 108:16771-16776. https://doi.org/10.1073/pnas.1106427108
56. Hallam SJ, Mincer TJ, Schleper C, Preston CM, Roberts K, Richardson PM, DeLong EF. 2006. Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biol 4:520-536. https://doi.org/10.1371/journal.pbio.0040095
57. Kowalchuk GA, Buma DS, de Boer W, Klinkhamer PGL, van Veen JA. 2002. Effects of above-ground plant species composition and diversity on the diversity of soil-borne microorganisms. Int J Gen Mol Microbiol 81:509-520
58. Ding GC, Piceno YM, Heuer H, Weinert N, Dohrmann AB, Carrillo A, Andersen GL, Castellanos T, Tebbe CC, Smalla K. 2013. Changes of soil bacterial diversity as a consequence of agricultural land use in a semi-arid ecosystem. PLoS One 8:e59497. https://doi.org/10.1371/journal.pone.0059497
59. Miethling R, Wieland G, Backhaus H, Tebbe CC. 2000. Variation of microbial rhizosphere communities in response to crop species, soil origin, and inoculation with Sinorhizobium meliloti L33. Microb Ecol 40:43-56. https://doi.org/10.1007/s002480000021
60. Carlsson G, Huss-Danell K. 2003. Nitrogen fixation in perennial forage legumes in the field. Plant Soil 253:353-372. https://doi.org/10.1023/A:1024847017371
61. Bell TH, El-Din Hassan S, Lauron-Moreau A, Al-Otaibi F, Hijri M, Yergeau E, St-Arnaud M. 2014. Linkage between bacterial and fungal rhizosphere communities in hydrocarbon-contaminated soils is related to plant phylogeny. ISME J 8:331-343. https://doi.org/10.1038/ismej.2013.149
62. Bell TH, Cloutier-Hurteau B, Al-Otaibi F, Turmel MC, Yergeau E, Courchesne F, St Arnaud M. 2015. Early rhizosphere microbiome composition is related to the growth and Zn uptake of willows introduced to a former landfill. Environ Microbiol 17:3025-3038. https://doi.org/10.1111/1462-2920.12900
63. Kourtev PS, Ehrenfeld JG, Häggblom M. 2002. Exotic plant species alter the microbial community structure and function in the soil. Ecology 83: 3152-3166. https://doi.org/10.1890/0012-9658(2002)083[3152:EPSATM]2.0.CO;2
64. Männistö MK, Kurhela E, Tiirola M, Häggblom MM. 2013. Acidobacteria dominate the active bacterial communities of Arctic tundra with widely divergent winter-time snow accumulation and soil temperatures. FEMS Microbiol Ecol 84:47-59. https://doi.org/10.1111/1574-6941.12035
65. Robertson SJ, McGill WB, Massicotte HB, Rutherford PM. 2007. Petroleum hydrocarbon contamination in boreal forest soils: a mycorrhizal ecosystems perspective. Biol Rev 82:213-240. https://doi.org/10.1111/j.1469-185X.2007.00012.x
66. Zackrisson O, DeLuca TH, Nilsson MC, Sellstedt A, Berglund LM. 2004. Nitrogen fixation increases with successional age in boreal forests. Ecology 85:3327-3334. https://doi.org/10.1890/04-0461
67. Gundale MJ, Bach LH, Nordin A. 2013. The impact of simulated chronic nitrogen deposition on the biomass and N2 fixation activity of two boreal feather moss-cyanobacteria associations. Biol Lett 9:3-7. https://doi.org/10.1098/rsbl.2013.0797
68. Rousk K, Jones DL, Deluca TH. 2013. Moss-cyanobacteria associations as biogenic sources of nitrogen in boreal forest ecosystems. Front Microbiol 4:150. https://doi.org/10.3389/fmicb.2013.00150
69. DeLuca TH, Zackrisson O, Nilsson M-C, Seastedt A. 2002. Quantifying nitrogen-fixation in feather moss carpets of boreal forests. Nature 419:917-920. https://doi.org/10.1038/nature01051
70. Rousk K, Jones DL, DeLuca TH. 2014. Moss-nitrogen input to boreal forest soils: tracking 15N in a field experiment. Soil Biol Biochem 72: 100-104. https://doi.org/10.1016/j.soilbio.2014.01.031
71. Mulder A, Graaf AA, Robertson LA, Kuenen JG. 1995. Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor. FEMS Microbiol 16:177-184. https://doi.org/10.1111/j.1574-6941.1995.tb00281.x
72. Hayatsu M, Tago K, Saito M. 2008. Various players in the nitrogen cycle: diversity and functions of the microorganisms involved in nitrification and denitrification. Soil Sci Plant Nutr 54:33-45. https://doi.org/10.1111/j.1747-0765.2007.00195.x
73. Lauber CL, Hamady M, Knight R, Fierer N. 2009. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75: 5111-5120. https://doi.org/10.1128/AEM.00335-09
74. Yamada T, Sekiguchi Y. 2009. Cultivation of uncultured chloroflexi subphyla: significance and ecophysiology of formerly uncultured chloroflexi "subphylum I" with natural and biotechnological relevance. Microbes Environ 24:205-216
75. Breuker A, Köweker G, Blazejak A, Schippers A. 2011. The deep biosphere in terrestrial sediments in the Chesapeake Bay area, Virginia, USA. Front Microbiol 2:1-13. https://doi.org/10.3389/fmicb.2011.00156
76. Laidlaw M. 2015. Soil carbon stabilization under three reclaimed vegetation types in the Alberta oil sands. University of British Columbia, Vancouver, British Columbia, Canada
77. Vos M, Wolf AB, Jennings SJ, Kowalchuk GA. 2013. Microscale determinants of bacterial diversity in soil. FEMS Microbiol Rev 37:936-954. https://doi.org/10.1111/1574-6976.12023
78. Environment Canada. 2015. Canadian climate normals, 1821-2000: Fort McMurray. Government of Canada, Edmonton, Alberta, Canada. http://climateweather.gc.ca/climate_normals/results_1981_2010_e.html?.stnID=2519&lang=f&StationName=Fort&SearchType=Contains&stnNameSubmit=go&dCode=1
79. Natural Regions Committee. 2006. Natural regions and subregions of Alberta. Government of Alberta, Edmonton, Alberta, Canada
80. Government of Alberta. 2015. Historical wildfire database. Government of Canada, Edmonton, Alberta, Canada. http://wildfire.alberta.ca/resources/historical-data/historical-wildfire-database.aspx
81. Bergeron Y, Gauthier S, Kafka V, Lefort P, Lesieur D. 2001. Natural fire frequency for the eastern Canadian boreal forest: consequences for sustainable forestry. Can J For Res 31:384-391. https://doi.org/10.1139/x00-178
82. Binkley D, Fisher RF. 2013. Ecology and management of forest soils, 4th ed. Wiley-Blackwell, West Sussex, United Kingdom
83. Rowland SM, 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. https://doi.org/10.2134/jeq2008.0317
84. Anderson J. 2014. Organic matter accumulation in reclaimed soils beneath different vegetation types in the Athabasca oil sands. University of British Columbia, Vancouver, British Columbia, Canada
85. Blake GR, Hartge KH. 1986. Bulk density, p 363-375. In Klute A (ed), Method of soil analysis. 1. Physical and mineralogical methods, 2nd ed. ASA-SSSA, Madison, WI
86. Thomas GW. 1996. Soil pH and soil acidity, p 475-490. In Sparks DL (ed), Methods of soil analysis. 3. Chemical methods. ASA-SSSA, Madison, WI
87. Rutherford PM, McGill WB, Arocena JM, Figueiredo CT. 2008. Total nitrogen, p 239-250. In Carter MR, Gregorich EG (ed), Soil sampling and methods of analysis, 2nd ed. Canadian Society of Soil Science/CRC Press, Boca Raton, FL
88. Skjemstad JO, Baldock JA. 2008. Total and organic carbon, p 225-237. In Carter MR, Gregorich EG (ed), Soil sampling and methods of analysis, 2nd ed. Canadian Society of Soil Science/CRC Press, Boca Raton, FL
89. Konert M, Vandenberghe J. 1997. Comparison of laser grain size analysis with pipette and sieve analysis: a solution for the underestimation of the clay fraction. Sedimentology 44:523-535
90. Tate KR, Ross DJ, Feltham CW. 1988. A direct extraction method to estimate soil microbial C: effects of experimental variables and some different calibration procedures. Soil Biol Biochem 20:329-335. https://doi.org/10.1016/0038-0717(88)90013-2
91. Davis M, Bajwa K, Person R. 2015. Predicted spatial variations of sulphur and nitrogen compound concentrations and deposition in the AOSR, p 51-63. In Clair TA, Percy KE (ed), Assessing forest health in the Alberta Oil Sands Region. Wood Buffalo Environmental Association, Fort Mc-Murray, Alberta, Canada
92. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R. 2012. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621-1624. https://doi.org/10.1038/ismej.2012.8
93. Caporaso G. 2011. Earth Microbiome Project: 16S rRNA amplification protocol. http://press.igsb.anl.gov/earthmicrobiome/protocols-andstandards/16s/
94. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. 2013. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112-5120. https://doi.org/10.1128/AEM.01043-13
95. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:590-596. https://doi.org/10.1093/nar/gks1219
96. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194-2200. https://doi.org/10.1093/bioinformatics/btr381
97. Simpson EH. 1949. Measurement of diversity. Nature 163:688-688. https://doi.org/10.1038/163688a0
98. Legendre P. 2007. anova.1way. Université de Montreal, Montreal, Quebec, Canada
99. Legendre P, Legendre L. 2012. Numerical ecology, 3rd ed. Elsevier, Amsterdam, Netherlands
100. Dray S, Legendre P, Blanchet G. 2011. packfor: forward selection with permutation (Canoco p.46). R package version 0.0-8. https://rdrr.io/rforge/packfor/
101. Borcard D, Gillet F, Legendre P. 2011. Numerical ecology with R. Springer, New York, NY
102. Legendre P, Gallagher ED. 2001. Ecologically meaningful transformations for ordination of species data. Oecologia 129:271-280. https://doi.org/10.1007/s004420100716
103. Giraudoux P. 2016. pgirmess: data analysis in ecology. R package version 1.6.5. https://rdrr.io/cran/pgirmess/
104. R Core Team. 2016. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria