Predicting the structure of soil communities from plant community taxonomy, phylogeny, and traits

ISME Journal - Tập 12 Số 7 - Trang 1794-1805 - 2018
Jonathan W. Leff1,2, Richard D. Bardgett3, Anna Wilkinson3, Benjamin G. Jackson4, William J. Pritchard3, Jonathan R. De Long3, Simon Oakley5, Kelly Mason5, Nick Ostle6, David Johnson3, Elizabeth M. Baggs7, Noah Fierer1,2
1Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, CO, 80309, USA
2Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309, USA
3School of Earth and Environmental Sciences, Michael Smith Building, The University of Manchester, Oxford Road, Manchester, M13 9PT, UK
4School of GeoSciences, Grant Institute, the King's Buildings, James Hutton Road, Edinburgh, EH9 3FE, UK
5Centre for Ecology & Hydrology, Lancaster Environment Centre, Library Avenue, Bailrigg, Lancaster LA1 4AP, UK
6Lancaster Environment Centre, Lancaster University, Lancaster LA1 4YQ, UK
7The Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus Buildings, Midlothian EH25 9RG, UK

Tóm tắt

Abstract

There are numerous ways in which plants can influence the composition of soil communities. However, it remains unclear whether information on plant community attributes, including taxonomic, phylogenetic, or trait-based composition, can be used to predict the structure of soil communities. We tested, in both monocultures and field-grown mixed temperate grassland communities, whether plant attributes predict soil communities including taxonomic groups from across the tree of life (fungi, bacteria, protists, and metazoa). The composition of all soil community groups was affected by plant species identity, both in monocultures and in mixed communities. Moreover, plant community composition predicted additional variation in soil community composition beyond what could be predicted from soil abiotic characteristics. In addition, analysis of the field aboveground plant community composition and the composition of plant roots suggests that plant community attributes are better predictors of soil communities than root distributions. However, neither plant phylogeny nor plant traits were strong predictors of soil communities in either experiment. Our results demonstrate that grassland plant species form specific associations with soil community members and that information on plant species distributions can improve predictions of soil community composition. These results indicate that specific associations between plant species and complex soil communities are key determinants of biodiversity patterns in grassland soils.

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Tài liệu tham khảo

Bates, 2013, Global biogeography of highly diverse protistan communities in soil, ISME J, 7, 652, 10.1038/ismej.2012.147

Fierer, 2009, Global patterns in belowground communities, Ecol Lett., 12, 1238, 10.1111/j.1461-0248.2009.01360.x

Kaiser, 2016, Driving forces of soil bacterial community structure, diversity, and function in temperate grasslands and forests, Sci Rep., 6, 33696, 10.1038/srep33696

Tedersoo, 2014, Global diversity and geography of soil fungi, Science, 346, 1256688, 10.1126/science.1256688

Van der Putten, 2013, Plant-soil feedbacks: the past, the present and future challenges, J Ecol., 101, 265, 10.1111/1365-2745.12054

Wardle, 2004, Ecological linkages between aboveground and belowground biota, Science, 304, 1629, 10.1126/science.1094875

Bardgett, 2010, Aboveground-belowground linkages: biotic interactions, ecosystem processes, and global change

van der Heijden, 1998, Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity, Nature, 396, 69, 10.1038/23932

Hiiesalu, 2014, Species richness of arbuscular mycorrhizal fungi: associations with grassland plant richness and biomass, New Phytol., 203, 233, 10.1111/nph.12765

Singh, 2004, Unravelling rhizosphere–microbial interactions: opportunities and limitations, Trends Microbiol., 12, 386, 10.1016/j.tim.2004.06.008

Berg, 2009, Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere, FEMS Microbiol Ecol., 68, 1, 10.1111/j.1574-6941.2009.00654.x

Grayston, 1998, Selective influence of plant species on microbial diversity in the rhizosphere, Soil Biol Biochem., 30, 369, 10.1016/S0038-0717(97)00124-7

Bardgett, 1999, Plant species and nitrogen effects on soil biological properties of temperate upland grasslands, Funct Ecol., 13, 650, 10.1046/j.1365-2435.1999.00362.x

Grayston, 2001, Accounting for variability in soil microbial communities of temperate upland grassland ecosystems, Soil Biol Biochem., 33, 533, 10.1016/S0038-0717(00)00194-2

de Vries, 2012, Abiotic drivers and plant traits explain landscape-scale patterns in soil microbial communities, Ecol Lett., 15, 1230, 10.1111/j.1461-0248.2012.01844.x

Prober, 2015, Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide, Ecol Lett., 18, 85, 10.1111/ele.12381

Lekberg, 2006, What drives differences in arbuscular mycorrhizal fungal communities among plant species?, Fungal Ecol., 24, 135, 10.1016/j.funeco.2016.05.012

Berg, 2009, Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture, Appl Microbiol Biotechnol., 84, 11, 10.1007/s00253-009-2092-7

Bezemer, 2010, Divergent composition but similar function of soil food webs beneath individual plants: plant species and community effects, Ecology, 91, 3027, 10.1890/09-2198.1

St John, 2006, Does plant species co-occurrence influence soil mite diversity?, Ecology, 87, 625, 10.1890/05-0380

Gibbons, 2017, Invasive plants rapidly reshape soil properties in a grassland ecosystem, mSystems, 2, e00178, 10.1128/mSystems.00178-16

Hawkes, 2005, Plant invasion alters nitrogen cycling by modifying the soil nitrifying community, Ecol Lett., 8, 976, 10.1111/j.1461-0248.2005.00802.x

Bezemer, 2006, Plant species and functional group effects on abiotic and microbial soil properties and plant-soil feedback responses in two grasslands, J Ecol., 94, 893, 10.1111/j.1365-2745.2006.01158.x

Carey, 2015, Soil microbial community structure is unaltered by plant invasion, vegetation clipping, and nitrogen fertilization in experimental semi-arid grasslands, Front Microbiol., 6, 10.3389/fmicb.2015.00466

Porazinska, 2003, Relationships at the aboveground-belowground interface: plants, soil biota, and soil processes, Ecol Monogr, 73, 377, 10.1890/0012-9615(2003)073[0377:RATAIP]2.0.CO;2

Tedersoo, 2016, Tree diversity and species identity effects on soil fungi, protists and animals are context dependent, ISME J, 10, 346, 10.1038/ismej.2015.116

Barberán, 2015, Relating belowground microbial composition to the taxonomic, phylogenetic, and functional trait distributions of trees in a tropical forest, Ecol Lett., 18, 1397, 10.1111/ele.12536

De Deyn, 2005, Linking aboveground and belowground diversity, Trends Ecol Evol., 20, 625, 10.1016/j.tree.2005.08.009

Ben-Hur, 2012, Functional trade-offs increase species diversity in experimental plant communities, Ecol Lett., 15, 1276, 10.1111/j.1461-0248.2012.01850.x

Adler, 2013, Trait-based tests of coexistence mechanisms, Ecol Lett., 16, 1294, 10.1111/ele.12157

Cantarel, 2015, Using plant traits to explain plant–microbe relationships involved in nitrogen acquisition, Ecology, 96, 788, 10.1890/13-2107.1

Grigulis, 2013, Relative contributions of plant traits and soil microbial properties to mountain grassland ecosystem services, J Ecol., 101, 47, 10.1111/1365-2745.12014

Legay, 2016, Influence of plant traits, soil microbial properties, and abiotic parameters on nitrogen turnover of grassland ecosystems, Ecosphere, 7, 1, 10.1002/ecs2.1448

Moreau, 2015, Plant traits related to nitrogen uptake influence plant-microbe competition, Ecology, 96, 2300, 10.1890/14-1761.1

Orwin, 2010, Linkages of plant traits to soil properties and the functioning of temperate grassland, J Ecol., 98, 1074, 10.1111/j.1365-2745.2010.01679.x

Legay, 2014, Contribution of above- and below-ground plant traits to the structure and function of grassland soil microbial communities, Ann Bot., 114, 1011, 10.1093/aob/mcu169

Thion, 2016, Plant nitrogen-use strategy as a driver of rhizosphere archaeal and bacterial ammonia oxidiser abundance, FEMS Microbiology Ecology, 92, fiw091, 10.1093/femsec/fiw091

Bardgett, 2014, Going underground: root traits as drivers of ecosystem processes, Trends Ecol Evol., 29, 692, 10.1016/j.tree.2014.10.006

De Deyn, 2011, Additional carbon sequestration benefits of grassland diversity restoration, J Appl Ecol., 48, 600, 10.1111/j.1365-2664.2010.01925.x

Rodwell, 1992, British plant communities. Volume 3. Grassland and montane communities, 3rd

Smith, 2003, Soil microbial community, fertility, vegetation and diversity as targets in the restoration management of a meadow grassland, J Appl Ecol., 40, 51, 10.1046/j.1365-2664.2003.00780.x

Ramirez, 2014, Biogeographic patterns in below-ground diversity in New York City’s Central Park are similar to those observed globally, Proc R Soc B Biol Sci., 281, 1, 10.1098/rspb.2014.1988

Callahan, 2016, DADA2: high resolution sample inference from amplicon data, Nat Methods, 13, 581, 10.1038/nmeth.3869

Abarenkov, 2010, The UNITE database for molecular identification of fungi—recent updates and future perspectives, New Phytol., 186, 281, 10.1111/j.1469-8137.2009.03160.x

McDonald, 2012, An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea, ISME J, 6, 610, 10.1038/ismej.2011.139

Guillou, 2013, The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote Small Sub-Unit rRNA sequences with curated taxonomy, Nucleic Acids Res., 41, 597, 10.1093/nar/gks1160

Spatafora, 2016, A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data, Mycologia, 108, 1028, 10.3852/16-042

Nguyen, 2015, FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild, Fungal Ecol., 20, 241, 10.1016/j.funeco.2015.06.006

Kartzinel, 2015, DNA metabarcoding illuminates dietary niche partitioning by African large herbivores, Proc Natl Acad Sci USA, 112, 8019, 10.1073/pnas.1503283112

Cornelissen, 2003, A handbook of protocols for standardised and easy measurement of plant functional traits worldwide, Aust J Bot., 51, 335, 10.1071/BT02124

Bardgett, 2003, Soil microbes compete effectively with plants for organic-nitrogen inputs to temperate grasslands, Ecology, 84, 1277, 10.1890/0012-9658(2003)084[1277:SMCEWP]2.0.CO;2

R Core Team R, 2016, A language and environment for statistical computing

Dufrêne, 1997, Species assemblages and indicator species: The need for a flexible asymmetrical approach, Ecol Monogr, 67, 345

Durka, 2012, Daphne: a dated phylogeny of a large European flora for phylogenetically informed ecological analyses, Ecology, 93, 2297, 10.1890/12-0743.1

Blomberg, 2003, Testing for phylogenetic signal in comparative data: behavioral traits are more labile, Evolution, 57, 717, 10.1111/j.0014-3820.2003.tb00285.x

Lozupone, 2011, UniFrac: an effective distance metric for microbial community comparison, ISME J, 5, 169, 10.1038/ismej.2010.133

Leff, 2015, Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe, Proc Natl Acad Sci USA, 112, 10967, 10.1073/pnas.1508382112

Wu, 2011, Molecular study of worldwide distribution and diversity of soil animals, Proc Natl Acad Sci USA, 108, 17720, 10.1073/pnas.1103824108

Lennon, 2012, Mapping the niche space of soil microorganisms using taxonomy and traits, Ecology, 93, 1867, 10.1890/11-1745.1

Peay, 2013, Strong coupling of plant and fungal community structure across western Amazonian rainforests, ISME J, 7, 1852, 10.1038/ismej.2013.66

Anacker, 2014, Phylogenetic conservatism in plant-soil feedback and its implications for plant abundance, Ecol Lett., 17, 1613, 10.1111/ele.12378

Mehrabi, 2015, Relatedness is a poor predictor of negative plant-soil feedbacks, New Phytol., 205, 1071, 10.1111/nph.13238

Lavorel, 2002, Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail, Funct Ecol., 16, 545, 10.1046/j.1365-2435.2002.00664.x

Roumet, 2016, Root structure-function relationships in 74 species: evidence of a root economics spectrum related to carbon economy, New Phytologist, 210, 815, 10.1111/nph.13828

Barberán, 2015, The ecology of microscopic life in household dust, Proc R Soc B, 282, 1, 10.1098/rspb.2015.1139

Haichar, 2008, Plant host habitat and root exudates shape soil bacterial community structure, ISME J, 2, 1221, 10.1038/ismej.2008.80

Carini, 2016, Relic DNA is abundant in soil and obscures estimates of soil microbial diversity, Nat Microbiol, 2, 10.1038/nmicrobiol.2016.242

Yoccoz, 2012, DNA from soil mirrors plant taxonomic and growth form diversity, Mol Ecol., 21, 3647, 10.1111/j.1365-294X.2012.05545.x

Hiiesalu, 2012, Plant species richness belowground: higher richness and new patterns revealed by next-generation sequencing, Mol Ecol., 21, 2004, 10.1111/j.1365-294X.2011.05390.x

Harrison, 2010, Influence of plant species and soil conditions on plant-soil feedback in mixed grassland communities, J Ecol., 98, 384, 10.1111/j.1365-2745.2009.01614.x

Laliberté, 2017, Below-ground frontiers in trait-based plant ecology, New Phytol., 213, 1597, 10.1111/nph.14247