Fungal communities respond to long-term CO2 elevation by community reassembly

Applied and Environmental Microbiology

Volumn 81, Issue 7, 2015, Pages 2445-2454

  Tu, Qichao ^a   Yuan, Mengting ^a   He, Zhili ^a   Deng, Ye ^b   Xue, Kai ^a   Wu, Liyou ^a   Hobbie, Sarah E ^c   Reich, Peter B ^c,d   Zhou, Jizhong ^a,e,f  

^a UNIVERSITY OF OKLAHOMA   (United States)

^b RESEARCH CENTER FOR ECO ENVIRONMENTAL SCIENCES   (China)

^c UNIVERSITY OF MINNESOTA   (United States)

^d WESTERN SYDNEY UNIVERSITY   (Australia)

^e LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^f TSINGHUA UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BIODIVERSITY; CARBON DIOXIDE; COMPLEX NETWORKS; ECOLOGY; ELECTRIC NETWORK TOPOLOGY; FORESTRY; FUNGI; RNA; SOILS;

CO-OCCURRENCE NETWORKS; ECOLOGICAL NETWORK ANALYSIS; ECOLOGICAL NETWORKS; GEODESIC DISTANCES; GLOBAL CHANGE FACTORS; GRASSLAND ECOSYSTEMS; OPERATIONAL TAXONOMIC UNITS; SOIL FUNGAL COMMUNITIES;

ECOSYSTEMS;

ABUNDANCE; BIOMASS; CARBON DIOXIDE; COEXISTENCE; DOMINANCE; ECOSYSTEM RESPONSE; FUNGUS; GENE EXPRESSION; GEODESY; GRASSLAND; RELATIVE ABUNDANCE; RNA; SOIL BIOTA; TAXONOMY;

MINNESOTA; UNITED STATES;

ASCOMYCOTA; BASIDIOMYCOTA;

CARBON DIOXIDE; FUNGAL DNA; RIBOSOME DNA; RNA 28S;

BIOTA; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; DRUG EFFECTS; FUNGUS; GENETICS; METABOLISM; MICROBIOLOGY; MINNESOTA; MOLECULAR GENETICS;

BIOTA; CARBON DIOXIDE; DNA, FUNGAL; DNA, RIBOSOMAL; FUNGI; MINNESOTA; MOLECULAR SEQUENCE DATA; RNA, RIBOSOMAL, 28S; SEQUENCE ANALYSIS, DNA; SOIL MICROBIOLOGY;

EID: 84925358080     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.04040-14     Document Type: Article

References (72)

1. Hawksworth DL. 2001. The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycol Res 105:1422-1432. http://dx.doi.org/10.1017/S0953756201004725.
2. O'Brien HE, Parrent JL, Jackson JA, Moncalvo J-M, Vilgalys R. 2005. Fungal community analysis by large-scale sequencing of environmental samples. Appl Environ Microbiol 71:5544-5550. http://dx.doi.org/10.1128/AEM.71.9.5544-5550.2005.
3. Webster J, Weber R. 2007. Introduction to fungi. Cambridge University Press, Cambridge, United Kingdom.
4. Bridge P, Spooner B. 2001. Soil fungi: diversity and detection. Plant Soil 232:147-154. http://dx.doi.org/10.1023/A:1010346305799.
5. 2. Ecol Lett 14:349-357. http://dx.doi.org/10.1111/j.1461-0248.2011.01593.x.
6. 2. Ecol Lett 13:564-575. http://dx.doi.org/10.1111/j.1461-0248.2010.01453.x.
7. 2 levels limited by nitrogen-induced plant species shift. Nature 466:96-99. http://dx.doi.org/10.1038/nature09176.
8. 2 fertilization of plant biomass. Nat Clim Change 3:278-282.
9. 2 and nitrogen deposition. Nature 410:809-810. http://dx.doi.org/10.1038/35071062.
10. 2. Ecol Lett 14:1220-1226. http://dx.doi.org/10.1111/j.1461-0248.2011.01692.x.
11. 2 enrichment experiments. Global Change Biol 16:836-848. http://dx.doi.org/10.1111/j.1365-2486.2009.02006.x.
12. Castro HF, Classen AT, Austin EE, Norby RJ, Schadt CW. 2010. Soil microbial community responses to multiple experimental climate change drivers. Appl Environ Microbiol 76:999-1007. http://dx.doi.org/10.1128 /AEM.02874-09.
13. Deng Y, He Z, Xu M, Qin Y, Van Nostrand JD, Wu L, Roe BA, Wiley G, Hobbie SE, Reich PB, Zhou J. 2012. Elevated carbon dioxide alters the structure of soil microbial communities. Appl Environ Microbiol 78: 2991-2995. http://dx.doi.org/10.1128/AEM.06924-11.
14. 2 on rhizosphere carbon flow and microbial community dynamics. Global Change Biol 19:621-636. http://dx.doi.org/10.1111/gcb.12045.
15. 2. Proc Natl Acad Sci USA 107:10938-10942. http://dx.doi.org/10.1073/pnas.0912421107.
16. 2. ISME J 3:1204-1217. http://dx.doi.org/10.1038/ismej.2009.65.
17. 2 and N fertilization in the duke forest. Global Change Biol 16:2104-2116. http://dx.doi.org/10.1111/j.1365-2486.2009.02080.x.
18. 2 and warming in an Australian native grassland soil. Environ Microbiol 14:3081-3096. http://dx.doi.org/10.1111/j.1462-2920.2012.02855.x.
19. He Z, Piceno Y, Deng Y, Xu M, Lu Z, DeSantis T, Andersen G, Hobbie SE, Reich PB, Zhou J. 2012. The phylogenetic composition and structure of soil microbial communities shifts in response to elevated carbon dioxide. ISME J 6:259-272. http://dx.doi.org/10.1038/ismej.2011.99.
20. 2 affects soil microbial diversity associated with trembling aspen. Environ Microbiol 10:926-941. http://dx.doi.org/10.1111/j.1462-2920.2007.01512.x.
21. 2, and atmospheric nitrogen deposition alter soil microbial community composition and function. Global Change Biol 13:980-989. http://dx.doi.org/10.1111/j.1365-2486.2007.01313.x.
22. 2 on microbial community structure and activities in the rhizosphere. Biol Fertil Soils 44:667-679. http://dx.doi.org/10.1007/s00374-008-0277-3.
23. 2 and nitrogen fertilization. New Phytol 176:164-174. http://dx.doi.org/10.1111/j.1469-8137.2007.02155.x.
24. 2. New Phytol 167:859-868. http://dx.doi.org/10.1111/j.1469-8137.2005.01458.x.
25. Antoninka A, Reich PB, Johnson NC. 2011. Seven years of carbon dioxide enrichment, nitrogen fertilization and plant diversity influence arbuscular mycorrhizal fungi in a grassland ecosystem. New Phytol 192: 200-214. http://dx.doi.org/10.1111/j.1469-8137.2011.03776.x.
26. 2. Science 337:1084-1087. http://dx.doi.org/10.1126/science.1224304.
27. van der Heijden MG, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR. 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69-72. http://dx.doi.org/10.1038/23932.
28. 2. Ecol Lett 15:1042-1049. http://dx.doi.org/10.1111/j.1461-0248.2012.01827.x.
29. Verbruggen E, Veresoglou SD, Anderson IC, Caruso T, Hammer EC, Kohler J, Rillig MC. 2013. Arbuscular mycorrhizal fungi-short-term liability but long-term benefits for soil carbon storage? New Phytol 197: 366-368. http://dx.doi.org/10.1111/nph.12079.
30. 3. Global Change Biol 17:2184-2195. http://dx.doi.org/10.1111/j.1365-2486.2010.02376.x.
31. 2 and nitrogen fertilization varies with soil horizon. Front Microbiol 4:78. http://dx.doi.org/10.3389/fmicb.2013.00078.
32. Faust K, Raes J. 2012. Microbial interactions: from networks to models. Nat Rev Microbiol 10:538-550. http://dx.doi.org/10.1038/nrmicro2832.
33. Barberan A, Bates ST, Casamayor EO, Fierer N. 2012. Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J 6:343-351. http://dx.doi.org/10.1038/ismej.2011.119.
34. Faust K, Sathirapongsasuti JF, Izard J, Segata N, Gevers D, Raes J, Huttenhower C. 2012. Microbial co-occurrence relationships in the human microbiome. PLoS Comput Biol 8:e1002606. http://dx.doi.org/10.1371/journal.pcbi.1002606.
35. Steele JA, Countway PD, Xia L, Vigil PD, Beman JM, Kim DY, Chow C-ET, Sachdeva R, Jones AC, Schwalbach MS, Rose JM, Hewson I, Patel A, Sun F, Caron DA, Fuhrman JA. 2011. Marine bacterial, archaeal and protistan association networks reveal ecological linkages. ISME J 5:1414-1425. http://dx.doi.org/10.1038/ismej.2011.24.
36. Zhou J, Deng Y, Luo F, He Z, Tu Q, Zhi X. 2010. Functional molecular ecological networks. mBio 1(4):e00169-10. http://dx.doi.org/10.1128 /mBio.00169-10.
37. 2. mBio 2:e00122-11. http://dx.doi.org/10.1128/mBio.00122-11.
38. Deng Y, Jiang Y-H, Yang Y, He Z, Luo F, Zhou J. 2012. Molecular ecological network analyses. BMC Bioinformatics 13:113. http://dx.doi.org/10.1186/1471-2105-13-113.
39. Zhou J, Bruns MA, Tiedje JM. 1996. DNA recovery from soils of diverse composition. Appl Environ Microbiol 62:316-322.
40. Ahn SJ, Costa J, Rettig Emanuel J. 1996. PicoGreen quantitation of DNA: effective evaluation of samples pre-or post-PCR. Nucleic Acids Res 24: 2623-2625. http://dx.doi.org/10.1093/nar/24.13.2623.
41. Liu K-L, Porras-Alfaro A, Kuske CR, Eichorst SA, Xie G. 2012. Accurate, rapid taxonomic classification of fungal large-subunit rRNA genes. Appl Environ Microbiol 78:1523-1533. http://dx.doi.org/10.1128/AEM.06826-11.
42. Edgar RC. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996-998. http://dx.doi.org/10.1038 /nmeth.2604.
43. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO. 2007. SILVA: a comprehensive online resource for quality checked and aligned rRNA sequence data compatible with ARB. Nucleic Acids Res 35:7188-7196. http://dx.doi.org/10.1093/nar/gkm864.
44. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792-1797. http://dx.doi.org/10.1093/nar/gkh340.
45. Price MN, Dehal PS, Arkin AP. 2009. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26:1641-1650. http://dx.doi.org/10.1093/molbev/msp077.
46. Hedges LV, Gurevitch J, Curtis PS. 1999. The meta-analysis of response ratios in experimental ecology. Ecology 80:1150-1156. http://dx.doi.org /10.1890/0012-9658(1999)080[1150:TMAORR]2.0.CO;2.
47. Hamady M, Lozupone C, Knight R. 2009. Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4:17-27. http: //dx.doi.org/10.1038/ismej.2009.97.
48. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537-7541. http://dx.doi.org/10.1128/AEM.01541-09.
49. Lin L, Ji Y, Tu Q, Huang R, Teng L, Zeng X, Song H, Wang K, Zhou Q, Li Y. 2013. Microevolution from shock to adaptation revealed strategies improving ethanol tolerance and production in Thermoanaerobacter. Biotechnol Biofuels 6:103. http://dx.doi.org/10.1186/1754-6834-6-103.
50. Lin L, Song H, Tu Q, Qin Y, Zhou A, Liu W, He Z, Zhou J, Xu J. 2011. The Thermoanaerobacter glycobiome reveals mechanisms of pentose and hexose co-utilization in bacteria. PLoS Genet 7:e1002318. http://dx.doi.org/10.1371/journal.pgen.1002318.
51. Luo F, Yang Y, Zhong J, Gao H, Khan L, Thompson DK, Zhou J. 2007. Constructing gene coexpression networks and predicting functions of unknown genes by random matrix theory. BMC Bioinformatics 8:299. http: //dx.doi.org/10.1186/1471-2105-8-299.
52. Yang Y, Harris DP, Luo F, Wu L, Parsons AB, Palumbo AV, Zhou J. 2008. Characterization of the Shewanella oneidensis Fur gene: roles in iron and acid tolerance response. BMC Genomics 9:S11. http://dx.doi.org/10.1186/1471-2164-9-S2-S11.
53. Zhou A, He Z, Redding-Johanson AM, Mukhopadhyay A, Hemme CL, Joachimiak MP, Luo F, Deng Y, Bender KS, He Q. 2010. Hydrogen peroxide-induced oxidative stress responses in Desulfovibrio vulgaris Hildenborough. Environ Microbiol 12:2645-2657. http://dx.doi.org/10.1038/ismej.2009.97.
54. Smoot ME, Ono K, Ruscheinski J, Wang P-L, Ideker T. 2011. Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27:431-432. http://dx.doi.org/10.1093/bioinformatics/btq675.
55. Hill MO. 1973. Diversity and evenness: a unifying notation and its consequences. Ecology 54:427-432. http://dx.doi.org/10.2307/1934352.
56. Vane-Wright RI, Humphries CJ, Williams PH. 1991. What to protect? Systematics and the agony of choice. Biol Conserv 55:235-254. http://dx.doi.org/10.1016/0006-3207(91)90030-D.
57. 2-Enrichment and nutrient availability alter ectomycorrhizal fungal communities. Ecology 87:2278-2287. http://dx.doi.org/10.1890/0012-9658(2006)87[2278:CANAAE]2.0.CO;2.
58. Buée M, Reich M, Murat C, Morin E, Nilsson RH, Uroz S, Martin F. 2009. 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol 184:449-456. http://dx.doi.org/10.1111 /j.1469-8137.2009.03003.x.
59. Jumpponen A, Jones KL, Blair J. 2010. Vertical distribution of fungal communities in tallgrass prairie soil. Mycologia 102:1027-1041. http://dx.doi.org/10.3852/09-316.
60. Penton CR, St Louis D, Cole JR, Luo Y, Wu L, Schuur EA, Zhou J, Tiedje JM. 2013. Fungal diversity in permafrost and tallgrass prairie soils under experimental warming. Appl Environ Microbiol 79:7063-7072. http://dx.doi.org/10.1128/AEM.01702-13.
61. Xu L, Ravnskov S, Larsen 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. http://dx.doi.org/10.1111/j.1574-6941.2012.01445.x.
62. Toju H, Tanabe AS, Yamamoto S, Sato H. 2012. High-coverage ITS primers for the DNA-based identification of ascomycetes and basidiomycetes in environmental samples. PLoS One 7:e40863. http://dx.doi.org/10.1371/journal.pone.0040863.
63. 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. http://dx.doi.org/10.1128/AEM.00262-07.
64. Öpik M, Moora M, Liira J, Zobel M. 2006. Composition of rootcolonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J Ecol 94:778-790. http://dx.doi.org/10.1111/j.1365-2745.2006.01136.x.
65. Fath BD, Scharler UM, Ulanowicz RE, Hannon B. 2007. Ecological network analysis: network construction. Ecol Modeling 208:49-55. http: //dx.doi.org/10.1016/j.ecolmodel.2007.04.029.
66. Kareiva PM, Kingsolver JG, Huey RB. 1993. Biotic interactions and global change. Sinauer Associates, Sunderland, MA.
67. Tylianakis JM, Didham RK, Bascompte J, Wardle DA. 2008. Global change and species interactions in terrestrial ecosystems. Ecol Lett 11: 1351-1363. http://dx.doi.org/10.1111/j.1461-0248.2008.01250.x.
68. 3. Oecologia 147:143-154. http: //dx.doi.org/10.1007/s00442-005-0249-3.
69. 2. Nature 409:188-191. http://dx.doi.org/10.1038/35051576.
70. 2 stimulates net accumulations of carbon and nitrogen in land ecosystems: a meta-analysis. Ecology 87:53-63. http://dx.doi.org/10.1890/04-1724.
71. Luo Y, Su BO, Currie WS, Dukes JS, Finzi A, Hartwig U, Hungate B, Murtrie REM, Oren RAM, Parton WJ, Pataki DE, Shaw MR, Zak DR, Field CB. 2004. Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54:731-739. http://dx.doi.org/10.1641/0006-3568(2004)054[0731:PNLOER]2.0.CO;2.
72. 2. Nature 440:922-925. http://dx.doi.org/10.1038/nature04486.