Fungal diversity in permafrost and tallgrass prairie soils under experimental warming conditions

Applied and Environmental Microbiology

Volumn 79, Issue 22, 2013, Pages 7063-7072

  Penton, C Ryan ^a   Louis, Derek St ^a   Cole, James R ^a   Luo, Yiqi ^b   Wu, Liyou ^b   Schuur, E A G ^c   Zhou, Jizhong ^b,d,e   Tiedje, James M ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF OKLAHOMA   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

^d TSINGHUA UNIVERSITY   (China)

^e LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BAYESIAN CLASSIFIER; CLASSIFICATION CONFIDENCE; COMMUNITY STRUCTURES; DATABASE PROJECTS; NUTRIENT CYCLING; OPERATIONAL TAXONOMIC UNITS; TALLGRASS PRAIRIE; TERRESTRIAL ECOSYSTEMS;

CLASSIFICATION (OF INFORMATION); FUNGI; RNA; SOCIAL SCIENCES; SOILS;

PERMAFROST;

DATA SET; DOMINANCE; ECOSYSTEM FUNCTION; EXPERIMENTAL STUDY; FUNGUS; GENETIC ANALYSIS; GLOBAL WARMING; GRASS; NUTRIENT CYCLING; PERMAFROST; PRAIRIE; PREDATION; SOIL MICROORGANISM; SOIL STRUCTURE; SOIL TYPE; SPECIES DIVERSITY; TERRESTRIAL ECOSYSTEM;

FUNGAL DNA; RNA 28S;

ARTICLE; ASCOMYCETES; BASIDIOMYCETES; BAYES THEOREM; BIODIVERSITY; CHYTRIDIOMYCETES; CLASSIFICATION; DNA SEQUENCE; FUNGAL GENE; GENETICS; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; POACEAE; UNITED STATES;

ALASKA; ASCOMYCOTA; BASIDIOMYCOTA; BAYES THEOREM; BIODIVERSITY; CHYTRIDIOMYCOTA; DNA, FUNGAL; GENES, FUNGAL; MOLECULAR SEQUENCE DATA; MYCOLOGICAL TYPING TECHNIQUES; OKLAHOMA; PHYLOGENY; POACEAE; RNA, RIBOSOMAL, 28S; SEQUENCE ANALYSIS, DNA; SOIL MICROBIOLOGY;

EID: 84886697864     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01702-13     Document Type: Article

References (81)

1. Mueller GM, Schmit JP. 2007. Fungal biodiversity. What do we know? What can we predict? Biodivers. Conserv. 16:1-5.
2. Hibbett DS, Ohman A, Glotzer D, Nuhn M, Kirk P, Nilsson RH. 2011. Progress in molecular and morphological taxon discovery in fungi and options for formal classification of environmental sequences. Fungal Biol. Rev. 25:38-47.
3. Deslippe JR, Hartmann M, Simard SW, Mohn WW. 2012. Long-term warming alters the composition of Arctic soil microbial communities. FEMS Microbiol. Ecol. 1:1-13.
4. Bååth E, Anderson AH. 2003. Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLF-based techniques. Soil Biol. Biochem. 35:955-963.
5. Zinger L, Shahnavaz B, Baptis F, Geremia RA, Choler P. 2009. Microbial diversity in alpine tundra soils correlates with snow cover dynamics. ISME J. 3:850-859.
6. Rousk J, Bååth 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.
7. Schadt CW, Martin AP, Lipson DA, Schmidt SK. 2003. Seasonal dynamics of previously unknown fungal lineages in tundra soils. Science 301:1359-1361.
8. Wallenstein MD, McMahon S, Schimel J. 2007. Bacterial and fungal community structure in Arctic tundra tussock and shrub soils. FEMS Microbiol. Ecol. 59:428-435.
9. Toberman H, Freeman C, Evans C, Fenner N, Artz RRE. 2008. Summer drought decreases soil fungal diversity and associated phenol oxidase activity in upland Calluna heathland soil. FEMS Microbiol. Ecol. 66:426- 436.
10. Buée M, Reich M, Murat C, Morin E, Nilsson RH, Uroz S, Martin F. 2009. 454 pyrosequencing analyses of forest soils reveals unexpectedly high fungal diversity. New Phytol. 184:449-456.
11. Liu K-L, Porras-Alfaro A, Kuske CR, Elchorst SA, Xie G. 2012. Accurate, rapid taxonomic classification of fungal large-subunit rRNA genes. Appl. Environ. Microbiol. 78:1523-1533.
12. Eichorst SA, Kuske CR. 2012. Identification of cellulose-responsive bacterial and fungal communities in geographically and edaphically different soils by using stable isotope probing. Appl. Environ. Microbiol. 78:2316- 2327.
13. Krüger D, Kapturska D, Fischer C, Daniel R, Wubet T. 2012. Diversity measures in environmental sequences are highly dependent on alignment quality-data from old and new LSU primers targeting Basidiomycetes. PLoS One 7:e32139 doi:10.1371/journal.pone.0032139.
14. Porter TM, Golding GB. 2012. Factors that affect large subunit ribosomal amplicon sequencing studies of fungal communities: classification method, primer choice, and error. PLoS One 7:e35749. doi:10.1371 /journal.pone.0035749.
15. Lentendu G, Zinger L, Manel S, Coissac E, Choler P, Geremia RA, Melodelima C. 2011. Assessment of soil fungal diversity in different alpine tundra habitats by means of pyrosequencing. Fungal Divers. 49:113-123.
16. Ryberg M, Kristiansson E, Sjökvist E, Nilsson RH. 2009. An outlook on the fungal internal transcribed spacer sequences in GenBank and the introduction of a web-based tool for the exploration of fungal diversity. New Phytol. 181:471-477.
17. Nilsson RH, Ryberg M, Kristiansson E, Abarenkov K, Larsson KH, Koljalg U. 2006. Taxonomic reliability of DNA sequences in public sequence databases: a fungal perspective. PLoS One 1:e59. doi:10.1371 /journal.pone.0000059.
18. Nilsson RH, Bok G, Ryberg M, Kristiansson E, Hallenberg N. 2009. A software pipeline for processing and identification of fungal ITS sequences. Source Code Biol. Med. 4:1-6.
19. Natali SM, Schuur EAG, Trucco C, Pries CEH, Crummer KG, Lopez AFB. 2011. Effects of permafrost warming of air, soil and permafrost on carbon balance in Alaskan tundra. Global Change Biol. 17:1394-1407.
20. Schuur EAG, Crummer KG, Vogel JG, Mack MC. 2007. Plant species composition and productivity following permafrost thaw and thermokarst in Alaskan tundra. Ecosystems 10:280-292.
21. Schuur EAG, Vogel JG, Crummer KG, Lee H, Sickman JO, Osterkamp TE. 2009. The effect of permafrost thaw on old carbon release and net carbon exchange from tundra. Nature 459:556-559.
22. Luo T, Wan S, Hui D, Wallace LL. 2001. Acclimatization of soil respiration to warming in tallgrass prairie. Nature 413:622-625.
23. Wan S, Luo Y, Wallace LL. 2002. Change in microclimate induced by experimental warming and clipping in tallgrass prairie. Glob. Change Biol. 8:754-768.
24. Wan S, Yuan T, Bowdish S, Wallace L, Russell SD, Luo Y. 2002. Response of an allergenic species, Ambrosia psilostachya (Asteraceae), to experimental warming and clipping: implications for public health. Am. J. Bot. 89:1843-1846.
25. Zhang W, Parker KM, Luo Y, Wan S, Wallace LL, Hu S. 2005. Soil microbial responses to experiment warming and clipping in a tallgrass prairie. Glob. Change Biol. 11:266-277.
26. Zhou J, Wan S, Luo Y. 2007. Source components and interannual variability of soil CO2 efflux under experimental warming and clipping in a grassland ecosystem. Glob. Change Biol. 13:761-775.
27. Zhou J, Xue K, Xie J, Deng Y, Wu L, Cheng X, Fei S, Deng S, He Z, Van Nostrand JD, Luo Y. 2012. Microbial mediation of carbon-cycle feedbacks to climate warming. Nat. Climate Change 2:106-110.
28. Zhou JZ, Bruns MA, Tiedje JM. 1996. DNA recovery from soils of diverse composition. Appl. Environ. Microbiol. 62:316-322.
29. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200.
30. Wright ES, Yilmaz LS, Noguera DR. 2012. DECIPHER, a search-based approach to chimera identification for 16S rRNA sequences. Appl. Environ. Microbiol. 78:717-725.
31. Clarke KR. 1993. Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18:117-143.
32. Anderson MJ. 2001. A new method for non-parametric multivariate analysis of variance. Aust. Ecol. 26:32-46.
33. Clarke RK, Somerfield PJ, Gorley RN. 2008. Testing of null hypotheses in exploratory community analyses: similarity profiles and biotaenvironment linkage. J. Exp. Mar. Biol. Ecol. 366:57-69.
34. Warwick RM, Platt HM, Clarke KR, Agard J, Gobin J. 1990. Analysis of macrobenthic and meiobenthic community structure in relationship to pollution and disturbance in Hamilton Harbour, Bermuda. J. Exp. Mar. Biol. Ecol. 138:119-142.
35. Anderson MJ, Ellingsen KE, McArdle BH. 2006. Multivariate dispersion as a measure of beta diversity. Ecol. Lett. 9:683-693.
36. Clarke KR, Gorley RN. 2006. PRIMER v6: user manual/tutorial. PRIMER-E, Plymouth, United Kingdom.
37. O'Brien HE, Parrent JL, Jackson JA, Moncalvo JM, Vilfalys R. 2005. Fungal community analysis by large-scale sequencing of environmental samples. Appl. Environ. Microbiol. 71:5544-5550.
38. Xu L, Ravnskov S, Larson J, Nicolaisen M. 2012. Linking fungal communities in roots, rhizosphere, and soil to the health status of Pisum sativum. FEMS Microbiol. Ecol. 82:736-745.
39. Xu L, Ravnskov S, Larson J, Nicolaisen M. 2012. Soil fungal community structure along a soil health gradient in pea fields examined using deep amplicon sequencing. Soil Biol. Biochem. 46:26-32.
40. Gottel NR, Castro HF, Kerley M, Yang Z, Pelletier DA, Podar M, Karpinets T, Uberbacher E, Tuskan GA, Vilgalys R, Doktycz MJ, Schadt CW. 2011. Distinct microbial communities within the endosphere and rhizosphere of Populus deltoids roots across contrasting soil types. Appl. Environ. Microbiol. 77:5934-5944.
41. Orgiazzi A, Lumini E, Nilsson RH, Girlanda M, Vizzini A, Bonfante P, Bianciotto V. 2012. Unravelling soil fungal communities from different Mediterranean land-use backgrounds. PLoS One 7:e34847. doi:10.1371 /journal.pone.0034847.
42. McGuire KL, Fierer N, Bateman C, Treseder KK, Turner BL. 2012. Fungal community composition in neotropical rain forests: the influence of tree diversity and precipitation. Microb. Ecol. 63:804-812.
43. Schmidt SK, Naff CS, Lynch RC. 2012. Fungal communities at the edge: ecological lessons from high alpine fungi. Fungal Ecol. 5:443-452.
44. Gibbons SM, Caporaso JG, Pirrung M, Field D, Knight R, Gilbert JA. 2013. Evidence for a persistent microbial seed bank throughout the global ocean. Proc. Natl. Acad. Sci. U. S. A. 110:4651-4655.
45. Khidir HH, Eudy DM, Porras-Alfaro A, Herrea J, Natvig DO, Sinsabaugh RL. 2010. A general suite of fungal endophytes dominate the roots of two dominant grasses in a semiarid grassland. J. Arid Environ. 74:35-42.
46. Porras-Alfaro A, Herrera J, Sinsabaugh RL, Odenback KJ, Lowrey T, Natvig DO. 2008. Novel root fungal consortium associated with a dominant desert grass. Environ. Microbiol. 74:2805-2813.
47. Aime MC, Phillips-Mora W. 2005. The causal agents of witches' broom and frosty pod rot of cacao (chocolate, Theobroma cacao) form a new lineage of Marasmiaceae. Mycologia 97:1012-1022.
48. Calvert EL, Muskett AE. 1944. Blind-seed disease of rye-grass. Nature 153:287-288.
49. Santos-González JC, Finlay RD, Tehler A. 2007. Seasonal dynamics of arbuscular mycorrhizal fungal communities in roots in a seminatural grassland. Appl. Environ. Microbiol. 73:5613-5623.
50. Öpik M, Moora Liira M, Zobel JM. 2006. Composition of rootcolonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J. Ecol. 94:778-790.
51. Malloch D, Cain RF. 1970. The genus Arachnomyces. Can. J. Bot. 48:839- 845.
52. Gibas CF, Sigler L, Summerbell RC, Hofstader SL, Gupta AK. 2002. Arachnomyces kanei (anamorph Onychocola kanei) sp. nov., from human nails. Med. Mycol. 40:573-580.
53. Tedersoo L, May TW, Smite ME. 2010. Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20:217-263.
54. Deslippe JR, Hartmann M, Mohn WW, Simard SW. 2011. Long-term experimental manipulation of climate alters the ectomycorrhizal community of Betula nana in Arctic tundra. Glob. Change Biol. 17:1625-1636.
55. Wang Z, Binder M, Schoch GL, Johnston PR, Spatafora JW, Hibbett DS. 2006. Evolution of helotialean fungi (Leotiomycetes, Pezizomycotina): a nuclear rDNA phylogeny. Mol. Phylogenet. Evol. 41:295-312.
56. Freeman KR, Martin AP, Karki D, Lynch RC, Mitter MS, Meyer AF, Longcore JE, Simmons DR, Schmidt SK. 2009. Evidence that chytrids dominate fungal communities in high-elevation soils. Proc. Natl. Acad. Sci. U. S. A. 106:18315-18320.
57. Simmons DR, James TY, Meyer AF, Longcore JE. 2009. Lobulomycetales, a new order in the Chytridiomycota. Mycol. Res. 113:450-460.
58. Anderson OR. 2012. The role of bacterial-based protist communities in aquatic and soil ecosystems and the carbon biogeochemical cycle, with emphasis on naked amoebae. Acta Protozool. 51:209-221.
59. Blackwell WH, Letcher PM, Powell MJ. 2004. Synopsis and systematic reconsideration of Karlingiomyces (Chytridiomycota). Mycotaxon 89: 259-276.
60. Massee G. 1895. British fungus-flora, vol IV. William Clowes and Sons, New York, NY.
61. Wang Z, Johnston PR, Takamatsu S, Spatafora JW, Hibbett DS. 2006. Towards a phylogenetic classification of the Leotiomycetes based on rDNA data. Mycologia 98:1065-1075.
62. Baral H-O, de Sloover JR, Huhtinen S, Laukka T, Stenroos S. 2009. An emendation of the genus Hyaloscypha to include Fuscoscypha (Hyaloscyphaceae, Helotiales, Ascomycotina). Karstenia 49:1-17.
63. Geml J, Laursen GA, Herriott IC, McFarland JM, Booth MG, Lennon N, Nusbaum HC, Taylor DL. 2010. Phylogenetic and ecological analyses of soil and sporocarp DNA sequences reveal high diversity and strong habitat partitioning in the boreal ectomycorrhizal genus Russula (Russulales; Basidiomycota). New Phytol. 187:494-507.
64. Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, Wallander H, Stenlid J, Finlay RD, Wardle DA, Lindahl BD. 2013. Roots and associated fungi drive carbon sequestration in boreal forest. Science 339:1615-1618.
65. Weber CF, Vilgalys R, Kuske CR. 2013. Changes in fungal community composition in response to elevated atmospheric CO2 and nitrogen fertilization varies with soil horizon. Front. Microbiol. 4:78. doi:10.3389/fmicb .2013.00078.
66. Kotiaho M, Fritze H, Merilä P, Tuomivirta T, Väliranta M, Korhola A, Karofeld E, Tuittila E-S. 2012. Actinobacteria community structure in the peat profile of boreal bogs follows a variation in the microtopographical gradient similar to vegetation. Plant Soil doi:10.1007/s11104-012-1546-3.
67. Staddon PL, Thompson K, Jakobsen I, Grime JP, Askew AP, Fitter AH. 2003. Mycorrhizal fungal abundance is affected by long-term climatic manipulations in the field. Glob. Change Biol. 9:186-194.
68. Clemmensen KE, Michelsen A, Jonasson S, Shaver GR. 2006. Increased ectomycorrhizal fungal abundance after long-term fertilization and warming of two Arctic tundra ecosystems. New Phytol. 171:391-404.
69. Zhou JZ, Wu LY, Deng Y, Zhi XY, Jiang YH, Tu QC, Xie JP, Van Nostrand JD, He ZH, Yang YF. 2011. Reproducibility and quantitation of amplicon sequencing-based detection. ISME J. 5:1303-1313.
70. Sherry RA, Weng E, Arnone JA, III, Johnson DW, Schimel DS, Verburg PS, Wallace LL, Luo Y. 2008. Lagged effects of experimental warming and doubled precipitation on annual and seasonal aboveground biomass production in a tallgrass prairie. Glob. Change Biol. 14:2923-2936.
71. Sheik CS, Beasley WH, Elshahed MS, Zhou X, Luo Y, Krunholz LR. 2011. Effect of warming and drought on grassland microbial communities. ISME J. 5:1692-1700.
72. Walker JF, Miller OK, Jr, Horton JL. 2008. Seasonal dynamics of ectomycorrhizal fungus assemblages on oak seedlings in the southeastern Appalachian Mountains. Mycorrhiza 18:123-132.
73. Jumpponen A, Jones KL, Mattox JD, Yaege C. 2010. Massively parallel 454-sequencing of fungal communities in Quercus spp. ectomycorrhizas indicates seasonal dynamics in urban and rural sites. Mol. Ecol. 19:S41- S53.
74. Dumbrell AJ, Ashton PD, Aziz N, Feng G, Nelson M, Dytham C, Fitter AH, Helgason T. 2011. Distinct seasonal assemblages of arbuscular mycorrhizal fungi revealed by massively parallel pyrosequencing. New Phytol. 190:794-804.
75. Davey ML, Heegaard E, Halvorsen R, Ohlson M, Kauserud H. 2012. Seasonal trends in the biomass and structure of bryophyte associated fungal communities explored by 454 pyrosequencing. New Phytol. 195:844- 856.
76. Schmit JP, Mueller GM. 2007. An estimate of the lower limit of global fungal diversity. Biodivers. Conserv. 16:99-111.
77. Kirk PM, Cannon PF, Minter DW, Stalpers JA. 2008. Dictionary of the fungi, 10th ed. CAB International, Wallingford, United Kingdom.
78. Hawksworth DL. 2001. The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycol. Res. 105:1422-1432.
79. Vilgays R. 2003. Taxonomic misidentification in public DNA databases. New Phytol. 160:4-5.
80. Nilsson RH, Kristiansson E, Ryberg M, Hallenberg N, Larsson KH. 2008. Intraspecific ITS variability in the kingdom Fungi as expressed in the international sequence database and its implications for molecular species identification. Evol. Bioinform. 4:193-201.
81. Hibbett DS, Thorn RG. 2001. Basidiomycota: Homobasidiomycetes, p 121-128. In McLaughlin DJ, McLaughlin EG, Lemke PA (ed), The Mycota: systematics and evolution, vol 7. Springer-Verlag, Berlin, Germany.