Vegetation-associated impacts on Arctic tundra bacterial and microeukaryotic communities

Applied and Environmental Microbiology

Volumn 81, Issue 2, 2015, Pages 492-501

  Shi, Yu ^a,d   Xiang, Xingjia ^a,d   Shen, Congcong ^a,d   Chu, Haiyan ^a   Neufeld, Josh D ^b   Walker, Virginia K ^c   Grogan, Paul ^c  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b UNIVERSITY OF WATERLOO   (Canada)

^c QUEEN S UNIVERSITY   (Canada)

^d UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

LANDFORMS; MICROORGANISMS; MOISTURE; MOISTURE DETERMINATION; RNA; SOILS; VEGETATION;

AMMONIUM CONCENTRATIONS; BIOGEOCHEMICAL PROCESS; DISSOLVED ORGANIC NITROGEN; ENVIRONMENTAL CHARACTERISTIC; MICROBIAL COMMUNITY STRUCTURES; MICROEUKARYOTIC COMMUNITY; OPERATIONAL TAXONOMIC UNITS; PHYLOGENETIC DIVERSITY;

CLIMATE CHANGE;

ARCTIC ENVIRONMENT; ATMOSPHERIC CHEMISTRY; BIOGEOCHEMISTRY; COMMUNITY DYNAMICS; HYDROLOGICAL CHANGE; MICROBIAL COMMUNITY; PHYLOGENETICS; RNA; SPECIES DIVERSITY; TAXONOMY; TUNDRA SOIL; VEGETATION TYPE;

BACTERIA (MICROORGANISMS); EUKARYOTA;

CARBON; NITROGEN; RIBOSOME DNA; SOIL; WATER;

ARCTIC; BACTERIUM; BIOTA; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; EUKARYOTE; GENETICS; MICROBIOLOGY; PLANT DEVELOPMENT; SOIL; TUNDRA;

ARCTIC REGIONS; BACTERIA; BIOTA; CARBON; DNA, RIBOSOMAL; EUKARYOTA; NITROGEN; PLANT DEVELOPMENT; SEQUENCE ANALYSIS, DNA; SOIL; SOIL MICROBIOLOGY; TUNDRA; WATER;

EID: 84920747674     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03229-14     Document Type: Article

References (73)

1. Intergovernmental Panel on Climate Change. 2013. The physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Intergovernmental Panel on Climate Change, Cambridge, United Kingdom.
2. Rohde R, Muller RA, Jacobsen R, Muller E, Perlmutter S, Rosenfeld A, Wurtele J, Groom D, Wickham C. 2013. A new estimate of the average Earth surface land temperature spanning 1753 to 2011. Geoinfor Geostat Overview 1:1. http://dx.doi.org/10.4172/2327-4581.1000101.
3. Arctic Council and the International Arctic Science Committee. 2004. Arctic climate impact assessment. Cambridge University Press, Cambridge, United Kingdom.
4. Feng S, Ho CH, Hu Q, Oglesby RJ, Jeong SJ, Kim BM. 2012. Evaluating observed and projected future climate changes for the Arctic using the Koppen-Trewartha climate classification. Clim Dynam 38:1359-1373. http://dx.doi.org/10.1007/s00382-011-1020-6.
5. Dufour-Tremblay G, Levesque E, Boudreau S. 2012. Dynamics at the treeline: differential responses of Picea mariana and Larix laricina to climate change in eastern subarctic Quebec. Environ Res Lett 7:044038. http: //dx.doi.org/10.1088/1748-9326/7/4/044038.
6. Tremblay B, Levesque E, Boudreau S. 2012. Recent expansion of erect shrubs in the low Arctic: evidence from eastern Nunavik. Environ Res Lett 7:035501. http://dx.doi.org/10.1088/1748-9326/7/3/035501.
7. Bardgett RD, Wardle DA. 2010. Aboveground-belowground linkages: biotic interactions, ecosystem processes, and global change, p 100-107. In Harvey PH, May RM, Godfray CH, Dunne JA (ed), Oxford University Press, Oxford, United Kingdom.
8. Kowalchuk GA, Buma DS, de Boer W, Klinkhamer PG, van Veen JA. 2002. Effects of above-ground plant species composition and diversity on the diversity of soil-borne microorganisms. Antonie Van Leeuwenhoek 81:509-520. http://dx.doi.org/10.1023/A:1020565523615.
9. Buckeridge KM, Banerjee S, Siciliano SD, Grogan P. 2013. The seasonal pattern of soil microbial community structure in mesic low Arctic tundra. Soil Biol Biochem 65:338-347. http://dx.doi.org/10.1016/j.soilbio.2013.06.012.
10. de la Peña E, Vandegehuchte ML, Bonte D, Moens M. 2011. Nematodes surfing the waves: long-distance dispersal of soil-borne microfauna via sea swept rhizomes. Oikos 120:1649-1656. http://dx.doi.org/10.1111/j.1600 -0706.2011.19540.x.
11. 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. http://dx.doi.org/10.1111/j.1574-6941.2006.00260.x.
12. Wardle DA. 2006. The influence of biotic interactions on soil biodiversity. Ecol Lett 9:870 - 886. http://dx.doi.org/10.1111/j.1461-0248.2006.00931.x.
13. Schimel JP, Gulledge J. 1998. Microbial community structure and global trace gases. Glob Change Biol 4:745-758. http://dx.doi.org/10.1046/j.1365 -2486.1998.00195.x.
14. Fierer N, Jackson RB. 2006. The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626-631. http://dx.doi.org/10.1073/pnas.0507535103.
15. Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL, Horner-Devine MC, Kane M, Krumins JA, Kuske CR, Morin PJ, Naeem S, Ovreas L, Reysenbach AL, Smith VH, Staley JT. 2006. Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102-112. http://dx.doi.org/10.1038/nrmicro1341.
16. Ramette A, Tiedje JM. 2007. Multiscale responses of microbial life to spatial distance and environmental heterogeneity in a patchy ecosystem. Proc Natl Acad Sci U S A 104:2761-2766. http://dx.doi.org/10.1073/pnas.0610671104.
17. Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JBH. 2012. Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol 10:497-506. http://dx.doi.org/10.1038/nrmicro2795.
18. Bartram AK, Jiang X, Lynch MD, Masella AP, Nicol GW, Dushoff J, Neufeld JD. 2014. Exploring links between pH and bacterial community composition in soils from the Craibstone Experimental Farm. FEMS Microbiol Ecol 87:403-415. http://dx.doi.org/10.1111/1574-6941.12231.
19. Miller SR, Strong AL, Jones KL, Ungerer MC. 2009. Bar-coded pyrosequencing reveals shared bacterial community properties along the temperature gradients of two alkaline hot springs in Yellowstone National Park. Appl Environ Microbiol 75:4565-4572. http://dx.doi.org/10.1128 /AEM.02792-08.
20. Goldfarb KC, Karaoz U, Hanson CA, Santee CA, Bradford MA, Treseder KK, Wallenstein MD, Brodie EL. 2011. Differential growth responses of soil bacterial taxa to carbon substrates of varying chemical recalcitrance. Front Microbiol 2:94. http://dx.doi.org/10.3389/fmicb.2011.00094.
21. Angel R, Soares MIM, Ungar ED, Gillor O. 2010. Biogeography of soil archaea and bacteria along a steep precipitation gradient. ISME J 4:553- 563. http://dx.doi.org/10.1038/ismej.2009.136.
22. Orwin KH, Wardle DA, Greenfield LG. 2006. Context-dependent changes in the resistance and resilience of soil microbes to an experimental disturbance for three primary plant chronosequences. Oikos 112:196- 208. http://dx.doi.org/10.1111/j.0030-1299.2006.13813.x.
23. 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 40:2407-2415. http://dx.doi.org /10.1016/j.soilbio.2008.05.021.
24. Wu TH, Ayres E, Bardgett RD, Wall DH, Garey JR. 2011. Molecular study of worldwide distribution and diversity of soil animals. Proc Natl Acad Sci U S A 108:17720-17725. http://dx.doi.org/10.1073/pnas.1103824108.
25. Tsyganov AN, Milbau A, Beyens L. 2013. Environmental factors influencing soil testate amoebae in herbaceous and shrubby vegetation along an altitudinal gradient in subarctic tundra (Abisko, Sweden). Eur J Protistol 49:238-248. http://dx.doi.org/10.1016/j.ejop.2012.08.004.
26. Shen CC, Liang WJ, Shi Y, Lin XG, Zhang HY, Wu X, Xie G, Chain P, Grogan P, Chu HY. 21 May 2014. Contrasting elevational diversity patterns between eukaryotic soil microbes and plants. Ecology. http://dx.doi.org/10.1890/14-0310.1.
27. Bjork RG, Klemedtsson L, Molau U, Harndorf J, Odman A, Giesler R. 2007. Linkages betweenNturnover and plant community structure in a tundra landscape. Plant Soil 294:247-261. http://dx.doi.org/10.1007/s11104-007 -9250-4.
28. Walker DA. 2000. Hierarchical subdivision of Arctic tundra based on vegetation response to climate, parent material and topography. Glob Change Biol 6:19-34. http://dx.doi.org/10.1046/j.1365-2486.2000.06010.x.
29. Buckeridge KM, Zufelt E, Chu HY, Grogan P. 2010. Soil nitrogen cycling rates in low Arctic shrub tundra are enhanced by litter feedbacks. Plant Soil 330:407-421. http://dx.doi.org/10.1007/s11104-009-0214-8.
30. McMahon SK, Wallenstein MD, Schimel JP. 2011. A cross-seasonal comparison of active and total bacterial community composition in Arctic tundra soil using bromodeoxyuridine labeling. Soil Biol Biochem 43:287- 295. http://dx.doi.org/10.1016/j.soilbio.2010.10.013.
31. Chu HY, Neufeld JD, Walker VK, Grogan P. 2011. The influence of vegetation type on the dominant soil bacteria, archaea, and fungi in a low Arctic tundra landscape. Soil Sci Soc Am J 75:1756-1765. http://dx.doi.org/10.2136/sssaj2011.0057.
32. Xu M, Cai XB, Gai JP, Li XL, Christie P, Zhang JL. 2014. Soil microbial community structure and activity along a montane elevational gradient on the Tibetan Plateau. Eur J Soil Biol 64:6-14. http://dx.doi.org/10.1016/j.ejsobi.2014.06.002.
33. Zhang XF, Zhao L, Xu SJ, Jr, Liu YZ, Liu HY, Cheng GD. 2013. Soil moisture effect on bacterial and fungal community in Beilu River (Tibetan Plateau) permafrost soils with different vegetation types. J Appl Microbiol 114:1054-1065. http://dx.doi.org/10.1111/jam.12106.
34. Zhang XF, Xu SJ, Li CM, Zhao L, Feng HY, Yue GY, Ren ZW, Cheng GD. 2014. The soil carbon/nitrogen ratio and moisture affect microbial community structures in alkaline permafrost-affected soils with different vegetation types on the Tibetan Plateau. Res Microbiol 165:128-139. http: //dx.doi.org/10.1016/j.resmic.2014.01.002.
35. Jassey VEJ, Chiapusio G, Binet P, Buttler A, Laggoun-Defarge F, Delarue F, Bernard N, Mitchell EAD, Toussaint ML, Francez AJ, Gilbert D. 2013. Above- and belowground linkages in sphagnum peatland: climate warming affects plant-microbial interactions. Glob Change Biol 19: 811-823. http://dx.doi.org/10.1111/gcb.12075.
36. Dredge L, Kerr D, Wolfe S. 1999. Surficial materials and related ground ice conditions, Slave Province, NWT, Canada. Can J Earth Sci 36:1227- 1238. http://dx.doi.org/10.1139/e98-087.
37. Nobrega S, Grogan P. 2008. Landscape and ecosystem-level controls on net carbon dioxide exchange along a natural moisture gradient in Canadian low Arctic tundra. Ecosystems 11:377-396. http://dx.doi.org/10.1007 /s10021-008-9128-1.
38. Chu HY, Grogan P. 2010. Soil microbial biomass, nutrient availability and nitrogen mineralization potential among vegetation-types in a low Arctic tundra landscape. Plant Soil 329:411-420. http://dx.doi.org/10.1007/s11104-009-0167-y.
39. Diez B, Pedros-Alio C, Marsh TL, Massana R. 2001. Application of denaturing gradient gel electrophoresis (DGGE) to study the diversity of marine picoeukaryotic assemblages and comparison of DGGE with other molecular techniques. Appl Environ Microbiol 67:2942-2951. http://dx.doi.org/10.1128/AEM.67.7.2942-2951.2001.
40. Hamady M, Walker JJ, Harris JK, Gold NJ, Knight R. 2008. Errorcorrecting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat Methods 5:235-237. http://dx.doi.org/10.1038 /nmeth.1184.
41. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335-336. http://dx.doi.org/10.1038/nmeth.f.303.
42. Huse SM, Huber JA, Morrison HG, Sogin ML, Welch DM. 2007. Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biol 8:R143. http://dx.doi.org/10.1186/gb-2007-8-7-r143.
43. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200. http://dx.doi.org/10.1093/bioinformatics/btr381.
44. 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 3:442-453. http://dx.doi.org/10.1038/ismej.2008.127.
45. Lauber CL, Hamady M, Knight R, Fierer N. 2009. Pyrosequencingbased assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111-5120. http://dx.doi.org/10.1128/AEM.00335-09.
46. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460 -2461. http://dx.doi.org/10.1093 /bioinformatics/btq461.
47. DeSantis TZ, Hugenholtz P, Keller K, Brodie EL, Larsen N, Piceno YM, Phan R, Andersen GL. 2006. NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucleic Acids Res 34:W394- W399. http://dx.doi.org/10.1093/nar/gkl244.
48. Bray JR, Curtis JT. 1957. An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr 27:326-349.
49. R Development Core Team. 2006. R, a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
50. Faith DP. 1992. Conservation evaluation and phylogenetic diversity. Biol Conservation 61:1-10. http://dx.doi.org/10.1016/0006-3207(92)91201-3.
51. Dixon P. 2003. VEGAN, a package of R functions for community ecology. J Veg Sci 14:927-930. http://dx.doi.org/10.1111/j.1654-1103.2003.tb02228.x.
52. Anderson MJ, Ford RB, Feary DA, Honeywill C. 2004. Quantitative measures of sedimentation in an estuarine system and its relationship with intertidal soft-sediment in fauna. Mar Ecol Prog Ser 272:33-48. http://dx.doi.org/10.3354/meps272033.
53. Chu HY, Fierer N, Lauber CL, Caporaso JG, Knight R, Grogan P. 2010. Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes. Environ Microbiol 12:2998-3006. http://dx.doi.org/10.1111/j.1462-2920.2010.02277.x.
54. Shen CC, Xiong JB, Zhang HY, Feng YZ, Lin XG, Li XY, Liang WJ, Chu HY. 2013. Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain. Soil Biol Biochem 57:204-211. http://dx.doi.org/10.1016/j.soilbio.2012.07.013.
55. Ludley KE, Robinson CH. 2008. 'Decomposer' Basidiomycota in Arctic and Antarctic ecosystems. Soil Biol Biochem 40:11-29. http://dx.doi.org /10.1016/j.soilbio.2007.07.023.
56. Coolen MJ, van de Giessen J, Zhu EY, Wuchter C. 2011. Bioavailability of soil organic matter and microbial community dynamics upon permafrost thaw. Environ Microbiol 13:2299-2314. http://dx.doi.org/10.1111/j.1462-2920.2011.02489.x.
57. Myers-Smith IH, Forbes BC, Wilmking M, Hallinger M, Lantz T, Blok D, Tape KD, Macias-Fauria M, Sass-Klaassen U, Levesque E, Boudreau S, Ropars P, Hermanutz L, Trant A, Collier LS, Weijers S, Rozema J, Rayback SA, Schmidt NM, Schaepman-Strub G, Wipf S, Rixen C, Menard CB, Venn S, Goetz S, Andreu-Hayles L, Elmendorf S, Ravolainen V, Welker J, Grogan P, Epstein HE, Hik DS. 2011. Shrub expansion in tundra ecosystems: dynamics, impacts and research priorities. Environ Res Lett 6:045509. http://dx.doi.org/10.1088 /1748-9326/6/4/045509.
58. Serreze MC, Walsh JE, Chapin FS, Osterkamp T, Dyurgerov M, Romanovsky V, Oechel WC, Morison J, Zhang T, Barry RG. 2000. Observational evidence of recent change in the northern high-latitude environment. Climatic Change 46:159 -207. http://dx.doi.org/10.1023 /A:1005504031923.
59. Hinzman LD, Bettez ND, Bolton WR, Chapin FS, Dyurgerov MB, Fastie CL, Griffith B, Hollister RD, Hope A, Huntington HP, Jensen AM, Jia GJ, Jorgenson T, Kane DL, Klein DR, Kofinas G, Lynch AH, Lloyd AH, McGuire AD, Nelson FE, Oechel WC, Osterkamp TE, Racine CH, Romanovsky VE, Stone RS, Stow DA, Sturm M, Tweedie CE, Vourlitis GL, Walker MD, Walker DA, Webber PJ, Welker JM, Winker K, Yoshikawa K. 2005. Evidence and implications of recent climate change in northern Alaska and other Arctic regions. Climatic Change 72:251-298. http://dx.doi.org/10.1007/s10584-005-5352-2.
60. Hinzman LD, Destouni G, Woo MK. 2013. Preface: hydrogeology of cold regions. Hydrogeol J 21:1-4. http://dx.doi.org/10.1007/s10040-012 -0943-2.
61. Bliss LC, Matveyeva NV. 1992. Circumpolar arctic vegetation, p 59-68. In Chapin FS, Jefferies RL, Reynolds JF, Shaver GR, Svodboda J (ed), Arctic ecosystems in a changing environment: an ecophysiological perspective. Academic Press, New York, NY.
62. Oechel WC. 1989. Nutrient and water flux in a small arctic watershed: an overview. Holararctic Ecol 12:229-237.
63. Chapin FS, Miller PC, Billings WD, Coyne PI. 1980. Carbon and nutrient budgets and their control in coastal tundra, p 458-482. In Brown J, Miller PC, Tieszen LL, Bunnell FL (ed), An Arctic tundra ecosystem. The coastal tundra at Barrow, Alaska. Dowden, Hutchinson and Ross, Stroudsburg, PA.
64. Heal GR, Mcewen IJ. 1981. The effect of water on the characteristics of the flow micro-calorimeter. Powder Technol 30:243-254. http://dx.doi.org /10.1016/0032-5910(81)80018-6.
65. Davis TH. 2004. Biography of David Tilman. Proc Natl Acad Sci U S A 101:10851-10853. http://dx.doi.org/10.1073/pnas.0404605101.
66. Griffiths RI, Thomson BC, James P, Bell T, Bailey M, Whiteley AS. 2011. The bacterial biogeography of British soils. Environ Microbiol 13: 1642-1654. http://dx.doi.org/10.1111/j.1462-2920.2011.02480.x.
67. Rousk J, Baath 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. http://dx.doi.org/10.1038/ismej.2010.58.
68. Fujimura KE, Egger KN. 2012. Host plant and environment influence community assembly of high Arctic root-associated fungal communities. Fungal Ecol 5:409-418. http://dx.doi.org/10.1016/j.funeco.2011.12.010.
69. Bates ST, Clemente JC, Flores GE, Walters WA, Parfrey LW, Knight R, Fierer N. 2013. Global biogeography of highly diverse protistan communities in soil. ISME J 7:652- 659. http://dx.doi.org/10.1038 /ismej.2012.147.
70. Mack MC, Schuur EAG, Bret-Harte MS, Shaver GR, Chapin FS. 2004. Ecosystem carbon storage in Arctic tundra reduced by long-term nutrient fertilization. Nature 43:440-443. http://dx.doi.org/10.1038/nature02887.
71. Wardle DA, Bardgett RD, Klironomos JN, Setala H, van der Putten WH, Wall DH. 2004. Ecological linkages between aboveground and belowground biota. Science 304:1629 -1633. http://dx.doi.org/10.1126 /science.1094875.
72. Wallenstein MD, McMahon SK, Schimel JP. 2009. Seasonal variation in enzyme activities and temperature sensitivities in Arctic tundra soils. Glob Change Biol 15:1631-1639. http://dx.doi.org/10.1111/j.1365-2486.2008.01819.x.
73. 15N in symbiotic fungi and plants estimates nitrogen and carbon flux rates in Arctic tundra. Ecology 87:816-822. http: //dx.doi.org/10.1890/0012-9658(2006)87[816:NISFAP]2.0.CO;2.