The seasonal pattern of soil microbial community structure in mesic low arctic tundra

Soil Biology and Biochemistry

Volumn 65, Issue , 2013, Pages 338-347

  Buckeridge, Kate M ^a   Banerjee, Samiran ^b,c   Siciliano, Steven D ^b   Grogan, Paul ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

^c CSIRO   (Australia)

Author keywords

Arctic birch hummock tundra; Bacteria; Epifluorescent microscopy; Fungi; Microbial carbon; Microbial nitrogen; Microbial phosphorus; PLFA; QPCR; Seasonal

Indexed keywords

ARCTIC BIRCH HUMMOCK TUNDRA; MICROBIAL CARBONS; MICROBIAL PHOSPHORUS; PLFA; QPCR; SEASONAL;

CARBON; ECOSYSTEMS; FUNGI; LANDFORMS; NUTRIENTS; PHOSPHOLIPIDS; POLYMERASE CHAIN REACTION; SOCIAL SCIENCES; SOIL MOISTURE; THAWING;

BACTERIA;

ARCTIC ENVIRONMENT; BACTERIUM; BIOMASS; COMMUNITY STRUCTURE; FUNGUS; MICROSCOPY; NUTRIENT AVAILABILITY; POLYMERASE CHAIN REACTION; SOIL CARBON; SOIL MICROORGANISM; SOIL NUTRIENT; SUBSTRATE; TERRESTRIAL ECOSYSTEM; TUNDRA;

EID: 84880580122     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2013.06.012     Document Type: Article

References (82)

1. ACIA Arctic Climate Impact Assessment 2005.
2. Baldrian P., Větrovský T., Cajthaml T., Dobiášová P., Petránková M., Šnajdr J., Eichlerová I. Estimation of fungal biomass in forest litter and soil. Fungal Ecology 2012, 6(1):1-11.
3. Balkwill D.L., Leach F.R., Wilson J.T., McNabb J.F., White D.C. Equivalence of microbial biomass measures based on membrane lipid and cell-wall components, adenosine-triphosphate, and direct counts in subsurface aquifer sediments. Microbial Ecology 1988, 16:73-84.
4. Banerjee S., Si B.C., Siciliano S.D. Evidence of high microbial abundance and spatial dependency in three Arctic soil ecosystems. Soil Science Society of America Journal 2011, 75:2227-2232.
5. Bardgett R.D., Lovell R.D., Hobbs P.J., Jarvis S.C. Seasonal changes in soil microbial communities along a fertility gradient of temperate grasslands. Soil Biology and Biochemistry 1999, 31:1021-1030.
6. Bardgett R.D., McAlister E. The measurement of soil fungal: bacterial biomass ratios as an indicator of ecosystem self-regulation in temperate meadow grasslands. Biology and Fertility of Soils 1999, 29:282-290.
7. Björk R.G., Björkman M.P., Andersson M.X., Klemedtsson L. Temporal variation in soil microbial communities in Alpine tundra. Soil Biology and Biochemistry 2008, 40:266-268.
8. Bligh E.G., Dyer W.J. Arapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 1959, 37:911-917.
9. Bloem J., Bolhuis P.R., Veninga M.R., Wieringa J. Microscopic methods for counting bacteria and fungi in soil 1995, 576. Academic Press, San Diego. K. Alef, P. Nannipieri (Eds.).
10. Bossio D.A., Scow K.M., Gunapala N., Graham K.J. Determinants of soil microbial communities: effects of agricultural management, season, and soil type on phospholipid fatty acid profiles. Microbial Ecology 1998, 36:1-12.
11. Brookes P.C., Landman A., Pruden G., Jenkinson D.S. Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biology and Biochemistry 1985, 17:837-842.
12. Brookes P.C., Powlson D.S., Jenkinson D.S. Measurement of microbial biomass phosphorus in soil. Soil Biology and Biochemistry 1982, 14:319-329.
13. Brooks P.D., Williams M.W., Schmidt S.K. Inorganic nitrogen and microbial biomass dynamics before and during spring snowmelt. Biogeochemistry 1998, 43:1-15.
14. Buckeridge K.M., Grogan P. Deepened snow alters soil microbial nutrient limitations in arctic birch hummock tundra. Applied Soil Ecology 2008, 39:210-222.
15. Buckeridge K.M., Grogan P. Deepened snow increases late thaw biogeochemical pulses in mesic low arctic tundra. Biogeochemistry 2010, 101:105-121.
16. Churchland C., Mayo-Bruinsma L., Ronson A., Grogan P. Soil microbial and plant community responses to single large carbon and nitrogen additions in low arctic tundra. Plant and Soil 2010, 334:409-421.
17. Cruz-Martinez K., Suttle K.B., Brodie E.L., Power M.E., Andersen G.L., Banfield J.F. Despite strong seasonal responses, soil microbial consortia are more resilient to long-term changes in rainfall than overlying grassland. Isme Journal 2009, 3:738-744.
18. Davidson E.A., Janssens I.A. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 2006, 440:165-173.
19. Dufrene M., Legendre P. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs 1997, 67:345-366.
20. Dumonceaux T.J., Hill J.E., Briggs S.A., Amoako K.K., Hemmingsen S.M., Van Kessel A.G. Enumeration of specific bacterial populations in complex intestinal communities using quantitative PCR based on the chaperonin-60 target. Journal of microbiological methods 2006, 64:46-62.
21. Edwards K.A., McCulloch J., Kershaw G.P., Jefferies R.L. Soil microbial and nutrient dynamics in a wet Arctic sedge meadow in late winter and early spring. Soil Biology and Biochemistry 2006, 38:2843-2851.
22. Ekelund F., Rønn R. Notes on protozoa in agricultural soil with emphasis on heterotrophic flagellates and naked amoebae and their ecology. FEMS Microbiology Reviews 1994, 15:321-353.
23. Elser J.J., Acharya K., Kyle M., Cotner J., Makino W., Markow T., Watts T., Hobbie S., Fagan W., Schade J., Hood J., Sterner R.W. Growth rate-stoichiometry couplings in diverse biota. Ecology Letters 2003, 6:936-943.
24. Farrelly V., Rainey F.A., Stackebrandt E. Effect of genome size and rrn gene copy number on PCR amplification of 16S rRNA genes from a mixture of bacterial species. Applied and Environmental Microbiology 1995, 61:2798-2801.
25. Fierer N., Bradford M.A., Jackson R.B. Toward an ecological classification of soil bacteria. Ecology 2007, 88:1354-1364.
26. Fierer N., Schimel J.P., Holden P.A. Variations in microbial community composition through two soil depth profiles. Soil Biology and Biochemistry 2003, 35:167-176.
27. Fraterrigo J.M., Balser T.C., Turner M.G. Microbial community variation and its relationship with nitrogen mineralization in historically altered forests. Ecology 2006, 87:570-579.
28. Fritze H., Pietikainen J., Pennanen T. Distribution of microbial biomass and phospholipid fatty acids in Podzol profiles under coniferous forest. European Journal of Soil Science 2000, 51:565-573.
29. Frostegard A., Baath E., Tunlid A. Shifts in the structure of soil microbial communities in limed forests as revealed by phospholipid fatty-acid analysis. Soil Biology and Biochemistry 1993, 25:723-730.
30. Gardes M., Bruns T.D. ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Molecular Ecology 1993, 2:113-118.
31. Grayston S.J., Griffith G.S., Mawdsley J.L., Campbell C.D., Bardgett R.D. Accounting for variability in soil microbial communities of temperate upland grassland ecosystems. Soil Biology and Biochemistry 2001, 33:533-551.
32. Grogan P., Jonasson S. Controls on annual nitrogen cycling in the understorey of a sub-arctic birch forest. Ecology 2003, 84:202-218.
33. Guckert J.B., Hood M.A., White D.C. Phospholipid ester-linked fatty-acid profile changes during nutrient deprivation of Vibrio cholerae - increases in the trans cis ratio and proportions of cyclopropyl fatty-acids. Applied and Environmental Microbiology 1986, 52:794-801.
34. Hobbie S.E., Miley T.A., Weiss M.S. Carbon and nitrogen cycling in soils from acidic and nonacidic tundra with different glacial histories in Northern Alaska. Ecosystems 2002, 5:761-774.
35. Jaeger C.H., Monson R.K., Fisk M.C., Schmidt S.K. Seasonal partitioning of nitrogen by plants and soil microorganisms in an alpine ecosystem. Ecology 1999, 80:1883-1891.
36. Jefferies R.L., Walker N.A., Edwards K.A., Dainty J. Is the decline of soil microbial biomass in late winter coupled to changes in the physical state of cold soils?. Soil Biology and Biochemistry 2010, 42:129-135.
37. Joergensen R., Wichern F. Quantitative assessment of the fungal contribution to microbial tissue in soil. Soil Biology and Biochemistry 2008, 40:2977-2991.
38. Jonasson S., Michelsen A., Schmidt I.K., Nielsen E.V. Responses in microbes and plants to changed temperature, nutrient, and light regimes in the arctic. Ecology 1999, 80:1828-1843.
39. Kieft T.L., Ringelberg D.B., White D.C. Changes in ester-linked phospholipid fatty-acid profiles of subsurface bacteria during starvation and desiccation in a porous-medium. Applied and Environmental Microbiology 1994, 60:3292-3299.
40. Kraft A.E. Psychotrophic Bacteria in Foods: Disease and Spoilage 1992, CRC Press, Boca Raton, Fl.
41. Kruskal J.B. Multidimensional-scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 1964, 29:1-27.
42. Kuo S. Phosphorus. Soil Science Society of America and American Society of Agronomy 1996, 869-919. Madison, WI. D.L. Sparks (Ed.).
43. Lafleur P.M., Humphreys E.R. Spring warming and carbon dioxide exchange over low Arctic tundra in central Canada. Global Change Biology 2008, 14:740-756.
44. Lipson D.A., Schadt C.W., Schmidt S.K. Changes in soil microbial community structure and function in an alpine dry meadow following spring snow melt. Microbial Ecology 2002, 43:307-314.
45. Lipson D.A., Schmidt S.K. Seasonal changes in an alpine soil bacterial community in the Colorado Rocky Mountains. Applied and Environmental Microbiology 2004, 70:2867-2879.
46. McCune B., Grace J.B. Analysis of Ecological Communities 2002, MjM Software, Gleneden Beach, OR.
47. McCune B., Mefford M.J. PC-ORD. Multivariate Analysis of Ecological Data 2006.
48. McKane R.B., Rastetter E.B., Shaver G.R., Nadelhoffer K.J., Giblin A.E., Laundre J.A., Chapin F.S. Climatic effects on tundra carbon storage inferred from experimental data and a model. Ecology 1997, 78:1170-1187.
49. McMahon S.K., Wallenstein M.D., Schimel J.P. Microbial growth in Arctic tundra soil at-2°C. Environmental Microbiology Reports 2009, 1:162-166.
50. Mielke P.W. The application of multivariate permutation methods based on distance functions in the earth-sciences. Earth-Science Reviews 1991, 31:55-71.
51. Moat A.G., Foster J.W., Spector M.P. Microbial Physiology 2002, Wiley-Liss, New York. fourth ed.
52. Nelson D.W., Sommers L.E. Total Carbon, Organic Carbon and Organic Matter 1996, 961-1010. Soil Science Society of America and American Society of Agronomy, Madison, WI. D.L. Sparks (Ed.).
53. Newsham K.K., Upson R., Read D.J. Mycorrhizas and dark septate root endophytes in polar regions. Fungal Ecology 2009, 2:10-20.
54. Nobrega S., Grogan P. Deeper snow enhances winter respiration from both plant-associated and bulk soil carbon pools in birch hummock tundra. Ecosystems 2007, 10:419-431.
55. Nobrega S., Grogan P. Landscape and ecosystem-level controls on net carbon dioxide exchange along a natural moisture gradient in Canadian low arctic tundra. Ecosystems 2008, 11:377-396.
56. Ovreås L., Forney L., Daae F.L., Torsvik V. Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Applied and Environmental Microbiology 1997, 63:3367-3373.
57. Panikov N.S., Flanagan P.W., Oechel W.C., Mastepanov M.A., Christensen T.R. Microbial activity in soils frozen to below-39 [deg]C. Soil Biology and Biochemistry 2006, 38:785-794.
58. Pokarzhevskii, A.D., van Straalen, N.M., Zaboev, D.P., Zaitsev, A.S., 2003. Microbial links and element flows in nested detrital food-webs. 47, 213-224.
59. Polyanskaya L.M., Ivanov K.E., Guzev V.S., Zvyagintsev D.G. Estimation of abundance dynamics of gram-negative bacteria in soil. Microbiology 2008, 77:760-764.
60. Rinnan R., Michelsen A., Baath E., Jonasson S. Fifteen years of climate change manipulations alter soil microbial communities in a subarctic heath ecosystem. Global Change Biology 2007, 13:28-39.
61. Rodríguez-Zaragoza S. Ecology of free-living amoebae. Critical Reviews in Microbiology 1994, 20:225-241.
62. Rogers B.F., Tate R.L. Temporal analysis of the soil microbial community along a toposequence in Pineland soils. Soil Biology and Biochemistry 2001, 33:1389-1401.
63. Schadt C.W., Martin A.P., Lipson D.A., Schmidt S.K. Seasonal dynamics of previously unknown fungal lineages in tundra soils. Science 2003, 301:1359-1361.
64. Schafer A.N., Snape I., Siciliano S.D. Influence of liquid water and soil temperature on petroleum hydrocarbon toxicity in Antarctic soil. Environmental Toxicology and Chemistry/SETAC 2009, 28:1409-1415.
65. Schimel J., Balser T.C., Wallenstein M. Microbial stress-response physiology and its implications for ecosystem function. Ecology 2007, 88:1386-1394.
66. Schimel J.P., Clein J.S. Microbial response to freeze-thaw cycles in tundra and taiga soils. Soil Biology and Biochemistry 1996, 28:1061-1066.
67. Schimel J.P., Gulledge J. Microbial community structure and global trace gases. Global Change Biology 1998, 4:745-758.
68. Schimel J.P., Lange O.L., Mooney H.A. Ecosystem consequences of microbial diversity and community structure 1995, 239-254. Springer-Verlag, Berlin, pp. pp. F.S. Chapin, C. Korner (Eds.).
69. Schimel J.P., Mikan C. Changing microbial substrate use in Arctic tundra soils through a freeze-thaw cycle. Soil Biology and Biochemistry 2005, 37:1411-1418.
70. Schmidt S.K., Costello E.K., Nemergut D.R., Cleveland C.C., Reed S.C., Weintraub M.N., Meyer A.F., Martin A.M. Biogeochemical consequences of rapid microbial turnover and seasonal succession in soil. Ecology 2007, 88:1379-1385.
71. Schuur E.A.G., Bockheim J., Canadell J.G., Euskirchen E., Field C.B., Goryachkin S.V., Hagemann S., Kuhry P., Lafleur P.M., Lee H., Mazhitova G., Nelson F.E., Rinke A., Romanovsky V.E., Shiklomanov N., Tarnocai C., Venevsky S., Vogel J.G., Zimov S.A. Vulnerability of permafrost carbon to climate change: implications for the global carbon cycle. BioScience 2008, 58:701-714.
72. Skogland T., Lomeland S., Goksoyr J. Respiratory burst after freezing and thawing of soil - experiments with soil bacteria. Soil Biology and Biochemistry 1988, 20:851-856.
73. Strickland M.S., Rousk J. Considering fungal:bacterial dominance in soils - methods, controls, and ecosystem implications. Soil Biology and Biochemistry 2010, 42:1385-1395.
74. Tarnocai C., Canadell J.G., Schuur E.A.G., Kuhry P., Mazhitova G., Zimov S. Soil organic carbon pools in the northern circumpolar permafrost region. Global Biogeochemical Cycles 2009, 23:1-11.
75. Wallenstein M.D., McMahon S., Schimel J. Bacterial and fungal community structure in Arctic tundra tussock and shrub soils. FEMS Microbiology Ecology 2007, 59:428-435.
76. Wardle D.A. Controls of temporal variability of the soil microbial biomass: a global-scale synthesis. Soil Biology and Biochemistry 1998, 30:1627-1637.
77. Wardle D.A. Communities and Ecosystems: Linking the Aboveground and Belowground Components 2002, Princetown University Press, Princetown, N.J.
78. White D.C., Davis W.M., Nickels J.S., King J.D., Bobbie R.J. Determination of the sedimentary microbial biomass by extractable lipid phosphate. Oecologia 1979, 40:51-62.
79. Zelles L. Phospholipid fatty acid profiles in selected members of soil microbial communities. Chemosphere 1997, 35:275-294.
80. Zelles L. Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biology and Fertility of Soils 1999, 29:111-129.
81. Zelles L., Bai Q.Y., Beck T., Beese F. Signature fatty-acids in phospholipids and lipopolysaccharides as indicators of microbial biomass and community structure in agricultural soils. Soil Biology and Biochemistry 1992, 24:317-323.
82. Zogg G.P., Zak D.R., Ringelberg D.B., MacDonald N.W., Pregitzer K.S., White D.C. Compositional and functional shifts in microbial communities due to soil warming. Soil Science Society of America Journal 1997, 61:475-481.