Anthropogenic land use shapes the composition and phylogenetic structure of soil arbuscular mycorrhizal fungal communities

FEMS Microbiology Ecology

Volumn 90, Issue 3, 2014, Pages 609-621

  Moora, Mari ^a   Davison, John ^a   Öpik, Maarja ^a   Metsis, Madis ^b   Saks, Ülle ^a   Jairus, Teele ^a   Vasar, Martti ^a   Zobel, Martin ^a  

^a UNIVERSITY OF TARTU   (Estonia)

^b TALLINN UNIVERSITY   (Estonia)

Author keywords

454 pyrosequencing; AMF; Disturbance; Habitat types; Soil biodiversity

Indexed keywords

SOIL;

AGRICULTURE; CLASSIFICATION; DNA SEQUENCE; ESTONIA; FOREST; GENETICS; GLOMEROMYCOTA; GRASSLAND; MICROBIAL CONSORTIUM; MICROBIOLOGY; MOLECULAR GENETICS; MYCORRHIZA; NUCLEOTIDE SEQUENCE; PHYLOGENY; SOIL;

AGRICULTURE; BASE SEQUENCE; ESTONIA; FORESTS; GLOMEROMYCOTA; GRASSLAND; MICROBIAL CONSORTIA; MOLECULAR SEQUENCE DATA; MYCORRHIZAE; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SOIL; SOIL MICROBIOLOGY;

EID: 84914810336     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/1574-6941.12420     Document Type: Article

References (87)

1. Alguacil MM, Lumini E, Roldan A, Salinas-Garcia JR, Bonfante P & Bianciotto V (2008) The impact of tillage practices on arbuscular mycorrhizal fungal diversity in subtropical crops. Ecol Appl 18: 527-536.
2. Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62: 245-253.
3. Augusto L, Dupouey JL & Ranger J (2003) Effects of tree species on understory vegetation and environmental conditions in temperate forests. Ann For Sci 60: 823-831.
4. Bainard LD, Koch AM, Gordon AM & Klironomos JN (2012) Temporal and compositional differences of arbuscular mycorrhizal fungal communities in conventional monocropping and tree-based intercropping systems. Soil Biol Biochem 45: 172-180.
5. Bainard LD, Bainard JD, Hamel C & Gan Y (2014) Spatial and temporal structuring of arbuscular mycorrhizal communities is differentially influenced by abiotic factors and host crop in a semi-arid prairie agroecosystem. FEMS Microbiol Ecol 88: 333-344.
6. Becklin KM, Pallo ML & Galen C (2012) Willows indirectly reduce arbuscular mycorrhizal fungal colonization in understorey communities. J Ecol 100: 343-351.
7. Bennett AE, Daniell TJ, Öpik M, Davison J, Moora M, Zobel M, Selosse MA & Evans D (2013) Arbuscular mycorrhizal fungal networks vary throughout the growing season and between successional stages. PLoS One 8: e83241.
8. Boddington CL & Dodd JC (2000) The effect of agricultural practices on the development of indigenous arbuscular mycorrhizal fungi. II. Studies in experimental microcosms. Plant Soil 218: 145-157.
9. Busby RR, Stromberger ME, Rodriguez G, Gebhart DL & Paschke MW (2013) Arbuscular mycorrhizal fungal community differs between a coexisting native shrub and introduced annual grass. Mycorrhiza 23: 129-141.
10. Chagnon PL, Bradley RL, Maherali H & Klironomos JN (2013) A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci 18: 484-491.
11. Corkidi L, Rowland D, Johnson NC & Allen EB (2002) Nitrogen fertilization alters the functioning of arbuscular mycorrhizas at two semiarid grassland. Plant Soil 240: 299-310.
12. Cumming JR & Kelly CN (2007) Pinus virginiana invasion influences soils and arbuscular mycorrhizae of a serpentine grassland. J Torrey Bot Soc 134: 63-73.
13. Daniell TJ, Husband R, Fitter AH & Young JPW (2001) Molecular diversity of arbuscular mycorrhizal fungi colonising arable crops. FEMS Microbiol Ecol 36: 203-209.
14. Davison J, Öpik M, Daniell TJ, Moora M & Zobel M (2011) Arbuscular mycorrhizal fungal communities in plant roots are not random assemblages. FEMS Microbiol Ecol 78: 103-115.
15. Davison J, Öpik M, Zobel M, Vasar M, Metsis M & Moora M (2012) Communities of arbuscular mycorrhizal fungi detected in forest soil are spatially heterogeneous but do not vary throughout the growing season. PLoS One 7: e41938.
16. de Cárcer DA, Denman SE, McSweeney C & Morrison M (2011) Evaluation of subsampling-based normalization strategies for tagged high-throughput sequencing data sets from gut microbiomes. Appl Environ Microbiol 77: 8795-8798.
17. Dufrene M & Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67: 345-366.
18. Dumbrell AJ, Nelson M, Helgason T, Dytham C & Fitter AH (2010) Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 4: 337-345.
19. Edgar RC, Haas BJ, Clemente JC, Quince C & Knight R (2011) uchime improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200.
20. Fitzsimons M, Miller R & Jastrow J (2008) Scale-dependent niche axes of arbuscular mycorrhizal fungi. Oecologia 158: 117-127.
21. Galvan GA, Paradi I, Burger K, Baar J, Kuyper TW, Scholten OE & Kik C (2009) Molecular diversity of arbuscular mycorrhizal fungi in onion roots from organic and conventional farming systems in the Netherlands. Mycorrhiza 19: 317-328.
22. Graham CH & Fine PVA (2008) Phylogenetic beta diversity: linking ecological and evolutionary processes across space in time. Ecol Lett 11: 1265-1277.
23. Hart MM & Reader RJ (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 153: 335-344.
24. Hart MM & Reader RJ (2004) Do arbuscular mycorrhizal fungi recover from soil disturbance differently? Tropic Ecol 45: 97-111.
25. Haug I, Wubet T, Weiss M, Aguirre N, Weber M, Gunter S & Kottke I (2010) Species-rich but distinct arbuscular mycorrhizal communities in reforestation plots on degraded pastures and in neighboring pristine tropical mountain rain forest. Tropic Ecol 51: 125-148.
26. Haug I, Setaro S & Suarez JP (2013) Reforestation sites show similar and nested AMF communities to an adjacent pristine forest in a tropical mountain area of South Ecuador. PLoS One 8: e63524.
27. Helgason T, Daniell TJ, Husband R, Fitter AH & Young JPW (1998) Ploughing up the wood-wide web? Nature 394: 431.
28. Hempel S, Renker C & Buscot F (2007) Differences in the species composition of arbuscular mycorrhizal fungi in spore, root and soil communities in a grassland ecosystem. Environ Microbiol 9: 1930-1938.
29. Hijri I, Sykorova Z, Oehl F, Ineichen K, Mader P, Wiemken A & Redecker D (2006) Communities of arbuscular mycorrhizal fungi in arable soils are not necessarily low in diversity. Mol Ecol 15: 2277-2289.
30. Horn S, Caruso T, Verbruggen E, Rillig MC & Hempel S (2014) Arbuscular mycorrhizal fungal communities are phylogenetically clustered at small scales. ISME J. DOI: 10.1038/ismej.2014.72. [Epub ahead of print]
31. Jansa J, Mozafar A, Anken T, Ruh R, Sanders IR & Frossard E (2002) Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza 12: 225-234.
32. Jansa J, Mozafar A, Kuhn G, Anken T, Ruh R, Sanders IR & Frossard E (2003) Soil tillage affects the community structure of mycorrhizal fungi in maize roots. Ecol Appl 13: 1164-1176.
33. Johnson NC (1993) Can fertilization of soil select less mutualistic mycorrhizae? Ecol Appl 3: 749-757.
34. Johnson NC, Rowland DL, Corkidi L & Allen EB (2008) Plant winners and losers during grassland N-eutrophication differ in biomass allocation and mycorrhizas. Ecology 89: 2868-2878.
35. Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP & Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26: 1463-1464.
36. Kindt R & Coe R (2005) Tree Diversity Analysis. A Manual and Software for Common Statistical Methods for Ecological and Biodiversity Studies. World Agroforestry Centre (ICRAF), Nairobi.
37. Kivlin SN, Hawkes CV & Treseder KK (2011) Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biol Biochem 43: 2294-2303.
38. Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84: 2292-2301.
39. Koorem K & Moora M (2010) Positive association between understory species richness and a dominant shrub species (Corylus avellana) in a boreonemoral spruce forest. Forest Ecol Manag 260: 1407-1413.
40. Koorem K, Price JN & Moora M (2011) Species-specific effects of woody litter on seedling emergence and growth of herbaceous plants. PLoS One 6: e26505.
41. Lee J, Lee S & Young JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65: 339-349.
42. Lekberg Y, Meadow J, Rohr JR, Redecker D & Zabinski CA (2011) Importance of dispersal and thermal environment for mycorrhizal communities: lessons from Yellowstone National Park. Ecology 92: 1292-1302.
43. Lekberg Y, Gibbons SM, Rosendahl S & Ramsey PW (2013) Severe plant invasions can increase mycorrhizal fungal abundance and diversity. ISME J 7: 1424-1433.
44. Li LF, Li T, Zhang Y & Zhao ZW (2010) Molecular diversity of arbuscular mycorrhizal fungi and their distribution patterns related to host-plants and habitats in a hot and arid ecosystem, southwest China. FEMS Microbiol Ecol 71: 418-427.
45. Lumini E, Orgiazzi A, Borriello R, Bonfante P & Bianciotto V (2010) Disclosing arbuscular mycorrhizal fungal biodiversity in soil through a land-use gradient using a pyrosequencing approach. Environ Microbiol 12: 2165-2179.
46. Lumini E, Vallino M, Alguacil MM, Romani M & Bianciotto V (2011) Different farming and water regimes in Italian rice fields affect arbuscular mycorrhizal fungal soil communities. Ecol Appl 21: 1696-1707.
47. Maherali H & Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316: 1746-1748.
48. Maherali H & Klironomos JN (2012) Phylogenetic and trait-based assembly of arbuscular mycorrhizal fungal communities. PLoS One 7: e36695.
49. Martinez TN & Johnson NC (2010) Agricultural management influences propagule densities and functioning of arbuscular mycorrhizas in low- and high-input agroecosystems in arid environments. Appl Soil Ecol 46: 300-306.
50. Mathimaran N, Ruh R, Jama B, Verchot L, Frossard E & Jansa J (2007) Impact of agricultural management on arbuscular mycorrhizal fungal communities in Kenyan ferralsol. Agric Ecosyst Environ 119: 22-32.
51. Meadow JF & Zabinski CA (2012) Linking symbiont community structures in a model arbuscular mycorrhizal system. New Phytol 194: 800-809.
52. Miras-Avalos JM, Antunes PM, Koch A, Khosla K, Klironomos JN & Dunfield KE (2011) The influence of tillage on the structure of rhizosphere and root-associated arbuscular mycorrhizal fungal communities. Pedobiologia 54: 235-241.
53. Moebius-Clune DJ, Anderson ZU & Pawlowska TE (2013) Arbuscular mycorrhizal fungi associated with a single agronomic plant host across the landscape: the structure of an assemblage. Soil Biol Biochem 64: 181-190.
54. Moora M, Öpik M, Sen R & Zobel M (2004) Native arbuscular mycorrhizal fungal communities differentially influence the seedling performance of rare and common Pulsatilla species. Funct Ecol 18: 554-562.
55. Moora M, Daniell T, Kalle H, Liira J, Püssa K, Roosaluste E, Öpik M, Wheatley R & Zobel M (2007) Spatial pattern and species richness of boreonemoral forest understorey and its determinants - A comparison of differently managed forests. Forest Ecol Manag 250: 64-70.
56. Moora M, Öpik M, Zobel K & Zobel M (2009) Understory plant diversity is related to higher variability of vegetative mobility of coexisting species. Oecologia 159: 355-361.
57. Mummey DL, Clarke JT, Cole CA, O'Connor BG, Gannon JE & Ramsey PW (2010) Spatial analysis reveals differences in soil microbial community interactions between adjacent coniferous forest and clearcut ecosystems. Soil Biol Biochem 42: 1138-1147.
58. Oehl F, Sieverding E, Ineichen K, Mader P, Boller T & Wiemken A (2003) Impact of land use intensity on the species diversity of arbuscular mycorrhizal fungi in agroecosystems of Central Europe. Appl Environ Microbiol 69: 2816-2824.
59. Oehl F, Sieverding E, Mader P, Dubois D, Ineichen K, Boller T & Wiemken A (2004) Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia 138: 574-583.
60. Oehl F, Laczko E, Bogenrieder A, Stahr K, Bösch R, van der Heijden M & Sieverding E (2010) Soil type and land use intensity determine the composition of arbuscular mycorrhizal fungal communities. Soil Biol Biochem 42: 724-738.
61. Oksanen J, Blanchet GF, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH & Wagner H (2013) vegan: Community Ecology Package. R package version 2.0-10. http://CRAN.R-project.org/package=vegan.
62. Öpik M, Moora M, Liira J & Zobel M (2006) Composition of root-colonising arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J Ecol 94: 778-790.
63. Öpik M, Moora M, Zobel M, Saks Ü, Wheatley R, Wright F & Daniell T (2008) High diversity of arbuscular mycorrhizal fungi in a boreal, herb rich, coniferous forest. New Phytol 179: 867-876.
64. Öpik M, Metsis M, Daniell TJ, Zobel M & Moora M (2009) Large-scale parallel 454 sequencing reveals host ecological group specificity of arbuscular mycorrhizal fungi in a boreonemoral forest. New Phytol 184: 424-437.
65. Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij JM, Reier Ü & Zobel M (2010) The online database MaarjAM reveals global and ecosystem distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188: 223-241.
66. Öpik M, Zobel M, Cantero J et al. (2013) Global sampling of plant roots expands the described molecular diversity of arbuscular mycorrhizal fungi. Mycorrhiza 23: 411-430.
67. Öpik M, Davison J, Moora M & Zobel M (2014) DNA-based detection and identificaton of Glomeromycota: the virtual taxonomy of environmental sequences. Botany 92: 1-13.
68. Pinheiro J, Bates D, DebRoy S, Sarkar D & the R Development Core Team (2013) nlme: linear and nonlinear mixed effects models. R package version 3.1-113.
69. Powell JR, Parrent JL, Hart MM, Klironomos JN, Rillig MC & Maherali H (2009) Phylogenetic trait conservatism and the evolution of functional tradeoffs in arbuscular mycorrhizal fungi. Proc Biol Sci 276: 4237-4245.
70. Reintam L, Sepp R & Zobel M (1987) Ecological and genetical diagnostics of surface gleyic soils. Degradation and Restoration Diagnostics of Forest Soils (Reintam L, Ed), pp. 29-32. Estonian Agricultural Academy Press, Tartu.
71. Roberts DW (2012) labdsv: ordination and multivariate analysis for ecology, package version 1.5-0. http://CRAN.R-project.org/package=labdsv.
72. Saito K, Suyama Y, Sato S & Sugawara K (2004) Defoliation effects on the community structure of arbuscular mycorrhizal fungi based on 18S rDNA sequences. Mycorrhiza 14: 363-373.
73. Saks Ü, Davison J, Öpik M, Vasar M, Moora M & Zobel M (2014) Root-colonizing and soil-borne communities of arbuscular mycorrhizal fungi in a temperate forest understorey. Botany 92: 277-285.
74. Schnoor TK, Lekberg Y, Rosendahl S & Olsson PA (2011) Mechanical soil disturbance as a determinant of arbuscular mycorrhizal fungal communities in semi-natural grassland. Mycorrhiza 21: 211-220.
75. Sikes BA, Maherali HZ & Klironomos JN (2012) Arbuscular mycorrhizal fungal communities change among three stages of primary sand dune succession but do not alter plant growth. Oikos 121: 1791-1800.
76. Simon L, Lalonde M & Bruns TD (1992) Specific amplification of 18S fungal ribosomal genes from VA endomycorrhizal fungi colonizing roots. Appl Environ Microbiol 58: 291-295.
77. Smith SE & Read DJ (2008) Mycorrhizal Symbiosis, 3rd edn. Academic Press, New York.
78. Tyndall RW (2005) Twelve years of herbaceous vegetation change in oak savanna habitat on a Maryland serpentine barren after Virginia pine removal. Castanea 70: 287-297.
79. Uibopuu A, Moora M, Saks Ü, Daniell T, Zobel M & Öpik M (2009) Differential effect of arbuscular mycorrhizal fungal communities from ecosystems along management gradient on the growth of forest understorey plant species. Soil Biol Biochem 41: 2141-2146.
80. Uibopuu A, Moora M, Öpik M & Zobel M (2012) Temperate forest understorey species performance is altered by local arbuscular mycorrhizal fungal communities from stands of different successional stages. Plant Soil 356: 331-339.
81. van der Heijden MGA & Scheublin TR (2007) Functional traits in mycorrhizal ecology: their use for predicting the impact of arbuscular mycorrhizal fungal communities on plant growth and ecosystem functioning. New Phytol 174: 244-250.
82. van der Heijden MGA, Boller T, Wiemken A & Sanders IR (1998) Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79: 2082-2091.
83. Vandenkoornhuyse P, Baldauf SL, Leyval C, Straczek J & Young JPW (2002a) Extensive fungal diversity in plant roots. Science 295: 2051.
84. Vandenkoornhuyse P, Husband R, Daniell TJ, Watson IJ, Duck JM, Fitter AH & Young JP (2002b) Arbuscular mycorrhizal community composition associated with two plant species in a grassland ecosystem. Mol Ecol 11: 1555-1564.
85. Verbruggen E, van der Heijden MGA, Weedon JT, Kowalchuk GA & Roling WFM (2012) Community assembly, species richness and nestedness of arbuscular mycorrhizal fungi in agricultural soils. Mol Ecol 21: 2341-2353.
86. Wetzel K, Silva G, Matczinski U, Oehl F & Fester T (2014) Superior differentiation of arbuscular mycorrhizal fungal communities from till and no-till plots by morphological spore identification when compared to T-RFLP. Soil Biol Biochem 72: 88-96.
87. Williams A, Ridgway HJ & Norton DA (2011) Growth and competitiveness of the New Zealand tree species Podocarpus cunninghamii is reduced by ex-agricultural AMF but enhanced by forest AMF. Soil Biol Biochem 43: 339-345.