Cited by 233Soil Carbon and Nitrogen DynamicsEcology and Vegetation Dynamics StudiesMicrobial Community Ecology and Physiology

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Biotic and Abiotic Properties Mediating Plant Diversity Effects on Soil Microbial Communities in an Experimental Grassland

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Lange, Markus, Habekost, Maike, Eisenhauer, Nico, Roscher, Christiane, Bessler, Holger, Engels, Christof, Oelmann, Yvonne, Scheu, Stefan, Wilcke, Wolfgang, Schulze, Ernst-Detlef, Gleixner, Gerd·2014·PLoS ONE

DOI 10.1371/journal.pone.0096182PMC PMC4015938

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Abstract

Plant diversity drives changes in the soil microbial community which may result in alterations in ecosystem functions. However, the governing factors between the composition of soil microbial communities and plant diversity are not well understood. We investigated the impact of plant diversity (plant species richness and functional group richness) and plant functional group identity on soil microbial biomass and soil microbial community structure in experimental grassland ecosystems. Total microbial biomass and community structure were determined by phospholipid fatty acid (PLFA) analysis. The diversity gradient covered 1, 2, 4, 8, 16 and 60 plant species and 1, 2, 3 and 4 plant functional groups (grasses, legumes, small herbs and tall herbs). In May 2007, soil samples were taken from experimental plots and from nearby fields and meadows. Beside soil texture, plant species richness was the main driver of soil microbial biomass. Structural equation modeling revealed that the positive plant diversity effect was mainly mediated by higher leaf area index resulting in higher soil moisture in the top soil layer. The fungal-to-bacterial biomass ratio was positively affected by plant functional group richness and negatively by the presence of legumes. Bacteria were more closely related to abiotic differences caused by plant diversity, while fungi were more affected by plant-derived organic matter inputs. We found diverse plant communities promoted faster transition of soil microbial communities typical for arable land towards grassland communities. Although some mechanisms underlying the plant diversity effect on soil microorganisms could be identified, future studies have to determine plant traits shaping soil microbial community structure. We suspect differences in root traits among different plant communities, such as root turnover rates and chemical composition of root exudates, to structure soil microbial communities.

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Figure 1 Impact of land use and plant diversity soil microbial community. Differences (P<0.05) between experimental plots and control sites (arable land and semi-natural meadows) were analyzed with Tukey's HSD test and indicated by letters. Differences between bare ground vs. vegetated plots and significant effects of plant diversity were tested with ANOVA (Table 1) and indicated by asterisks (P<0.05). Figures show effect of plant species richness on (a) total microbial biomass (b) fungal biomass and the fungal-to-bacterial biomass ratio and (c) number plant functional groups effect on fungal biomass and the fungal-to-bacterial biomass ratio.CC BY · PubMed Central

Figure 2 Minimal parsimonious models, testing direct and indirect effects of plant diversity on soil microbial community. Minimal SEM for a) total soil microbial biomass (MicBM), b) biomass of Gram positive bacteria (Gram+), c) biomass Gram negative bacteria (Gram−), d) fungal biomass (Fungi), and e) fungal-to-bacterial biomass ratio (F:B ratio). Arrows show significant relationships between variables. Numbers next to arrows show standardized parameter estimates (i.e., standardized regression weights). Circles (e1–e6) indicate error terms, and double-headed arrows indicate significant correlations between the error terms. Squared multiple correlations (R2) for the dependent soil microbial biomass are given next to the box of the dependent variable. See the non-standardized estimates of the regression weights in Table S3a-e. Abbreviations are PSR: plant species richness, FG: plant functional group richness, LEG: presence of legumes, GRASS: presence of grasses, RBM: fine root standing biomass, N%: nitrogen concentration of fine roots, LAI: leaf area index, SM: soil moisture, Clay: clay content of soilCC BY · PubMed Central

Figure 3 Summary of non-metric multidimensional scaling (NMDS) of the PLFAs. Differences among bare ground plots and different plant diversity levels are shown for (a) 1 to 60 sown plant species and (b) 1 to 4 functional groups. Bray-Curtis was used as dissimilarity index.CC BY · PubMed Central

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Background
Dryland soil mycobiome response to long‐term precipitation variability depends on host type
Louw, N. L., Gherardi, L., Sala, O. E., & Chung, Y. A. (2022) · Journal of Ecology · doi:10.1111/1365-2745.14006 · Cited by 9
“In experimental grassland ecosystems in Europe, Lange et al. (2014) and Bartelt- Ryser et al. (2005) found that the presence of legumes generally decreased the biomass of soil fungi.”
Background
Short‐term responses of soil carbon, nitrogen, and microbial biomass to cover crop mixtures and monocultures
de Souza, I. A., Daly, A. B., Schnecker, J., Warren, N. D., Lobo-Jr, A. R., Smith, R. G., Brito, A. F., & Grandy, A. S. (2023) · Agrosystems Geosciences & Environment · doi:10.1002/agg2.20395 · Cited by 11
Plant diversity is coupled with soil fungal diversity in a natural temperate steppe of northeastern China
Liu, D., Liu, G., Chen, L., Han, W., & Wang, D. (2021) · Soil Ecology Letters · doi:10.1007/s42832-021-0113-3 · Cited by 9
“Lange et al. (2014) manipulated a gradient in sown plant species next to a river in Germany, and they reported that there was no significant trend between soil fungal biomass and PSR.”
Background
Taxonomical and functional responses of microbial communities from forest soils of differing tree species diversity to drying-rewetting cycles
Gillespie, L. M., Prada‐Salcedo, L. D., Shihan, A., Fromin, N., Goldmann, K., Milcu, A., Buscot, F., Buatois, B., & Hättenschwiler, S. (2023) · Pedobiologia · doi:10.1016/j.pedobi.2023.150875 · Cited by 14
Contrasting effects of two phenotypes of an alpine cushion plant on understory species drive community assembly
Liu, Z., Michalet, R., Wang, C., Wang, Y., Chen, J., Cui, H., Song, H., Wang, J., Yang, Z., An, L., et al. (2022) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2022.160154 · Cited by 8
Grasses mixture-planting rather than fertilization depresses soil microbial diversity in an alpine artificial grassland
Li, J., Jiang, X. P., Zhou, X., Yin, X., & Niu, K. (2023) · Plant and Soil · doi:10.1007/s11104-023-06395-8 · Cited by 8
“…(SOC) Vol.: (0123456789) more pronouncedly consumed by biomass production of two-grasses mixtures due to complementary uptake and utilization (Lange et al. 2014); (ii) the lowered soil available nitrogen and disadvantageous effect of mixture-planting on some infrequent taxa of soil microbes…”
Effects of experimental warming on soil microbial communities in two contrasting subalpine forest ecosystems, eastern Tibetan Plateau, China
Sun, D.-D., Li, Y.-J., Zhao, W., Zhang, Z., Li, D., Zhao, C., & Liu, Q. (2016) · Journal of Mountain Science · doi:10.1007/s11629-015-3733-1 · Cited by 8
Forest humus forms as a playground for studying aboveground-belowground relationships: Part 1, theoretical backgrounds
Aubert, M., & Bureau, F. (2017) · Applied Soil Ecology · doi:10.1016/j.apsoil.2017.09.004 · Cited by 8
Abiotic and plant gender effects on the structure and function of soil microbial communities associated with Acanthosicyos horridus (Nara) in the Namibian sand-dune desert ecosystem
Sherman, C., Marais, E., Maggs‐Kölling, G., Adams, J. M., & Steinberger, Y. (2019) · Journal of Arid Environments · doi:10.1016/j.jaridenv.2019.01.009 · Cited by 8
Contrasting regulating effects of soil available nitrogen, carbon, and critical functional genes on soil N2O emissions between two rice-based rotations
Xu, P., Jiang, M., Khan, I., Zhou, M., Shaaban, M., & Hu, R. (2024) · Plant and Soil · doi:10.1007/s11104-024-06731-6 · Cited by 8
“S3) which were based on the theoretical knowledge derived from the some reported literature (Lange et al. 2014, 2015; Zhou et al. 2017, 2020; Xu et al. 2022b, 2023, 2024; Wu et al. 2023), the SEM was accordingly modified to reflect the direct and indirect effects of several key components on soil N…”
Tree Diversity Determines the Diversity of the Taxonomic and Functional Structure of the Fungal Community in Forest Litter in Southern China
Xiao, W., Zhao, J., Yan, X., & Guan, Q. (2018) · Forest Science · doi:10.1093/forsci/fxy037 · Cited by 7
“First, plant diversity can affect the fungal community directly through abiotic changes; such changes are mainly mediated by changes in the leaf area index, which affect the moisture in the litter layer (Allison et al. 2013, Lange et al. 2014).”
Effects of Tillage and Winter Cover Management in a Maize Soybean Rotation on Soil Bacterial and Fungal Community Composition
Narayana, N. K., Kingery, W. L., Jacobs, A. A., Allison, J., & Shanmugam, S. G. (2022) · Land · doi:10.3390/land11122259 · Cited by 7
Distribution of microbial communities in seasonally frozen soil layers on the Tibetan Plateau and the driving environmental factors
Wang, X., Yu, Z., Shen, G., Cheng, H., & Tao, S. (2022) · Environmental Science and Pollution Research · doi:10.1007/s11356-022-22283-7 · Cited by 7
Community composition and catabolic functional diversity of soil microbes affected by Hedysarum scoparium in arid desert regions of northwest China
Xue, Z., He, X., & Zuo, Y. (2019) · Arid Land Research and Management · doi:10.1080/15324982.2019.1637968 · Cited by 6
“Numerous studies have demonstrated that soil microorganisms have profound effects on plant performance and composition (Heijden, Bardgett, and Straalen 2008; Lange et al. 2014).”
Background
Tillage and Residue Management Impact on Microbial and Nematode Abundance Under Diverse Rice-Based Cropping Systems in Calcareous and Non-calcareous Floodplain Soils
Sarker, R. R., Rashid, M. H., Islam, M. A., Jahiruddin, M., Islam, K. R., & Jahangir, M. M. R. (2023) · Journal of soil science and plant nutrition · doi:10.1007/s42729-023-01168-9 · Cited by 5
“The higher diversity of crop species caused higher fungal-to-bacterial ratios of the microbial community due to available source of labile C and nutrient stock for microbial growth (Lange et al. 2014).”
Background
Response of soil bacteria on habitat-specialization and abundance gradient to different afforestation types
Qiu, Z., Li, J., Wang, P., Wang, D., Li, H., Gao, X., & Shu, J. (2023) · Scientific Reports · doi:10.1038/s41598-023-44468-x · Cited by 5
Soil Bacterial Diversity Responds to Long-Term Establishment of Perennial Legumes in Warm-Season Grassland at Two Soil Depths
Erhunmwunse, A. S., Guerra, V., Liu, J.-C., Mackowiak, C. L., Blount, A. R. S., Dubeux, J. C. B., & Liao, H. (2023) · Microorganisms · doi:10.3390/microorganisms11123002 · Cited by 5
“However, the association between introduced plant species and soil bacteria may change over time within the same ecosystem as plant growth and development advances [40,41].”
Background
Effects of plant species richness on 13C assimilate partitioning in artificial grasslands of different established ages
Xu, L., Yao, B., Wang, W., Wang, F., Zhou, H., Shi, J., & Zhao, X. (2017) · Scientific Reports · doi:10.1038/srep40307 · Cited by 5
Baseline status of microbial activity on gold tailings facilities in South Africa
Schimmer, C., & van Deventer, P. W. (2017) · Applied Soil Ecology · doi:10.1016/j.apsoil.2017.10.020 · Cited by 5
Testing the effects of plant species loss on multiple ecosystem functions based on extinction scenarios
Yoshihara, Y., Sasaki, T., Nyambayar, D., Matsuki, Y., Baba, Y., & Suyama, Y. (2019) · Basic and Applied Ecology · doi:10.1016/j.baae.2019.05.005 · Cited by 5
Loquat-tea intercropping enhances rhizosphere microbial diversity and functional profiles in tea soil ecosystems
Zou, C., Dai, T., Liang, Z., Li, M., Meng, L., Xianming, Z., Li, N., Wei, Q., Elhamid, M. A. A., Atif, A. M., et al. (2025) · Frontiers in Microbiology · doi:10.3389/fmicb.2025.1651997 · Cited by 4
“Increasingly, studies have shown that the relationship between soil nutrient factors and soil microorganisms can provide a deeper understanding of the ecological processes and mechanisms underlying soil microorganisms’ role in promoting normal plant growth (Lange et al., 2014).”
Methods of Assessments of Microbial Diversity and Their Functional Role in Soil Fertility and Crop Productivity
Reddy, B., Kumar, A., Mehta, S., & Sahu, K. P. (2021) · Rhizosphere biology · doi:10.1007/978-981-16-3364-5_14 · Cited by 4
Interannual Variation and Control Factors of Soil Respiration in Xeric Shrubland and Agricultural Sites from the Chihuahuan Desert, Mexico
Guillén-Cruz, G., Campuzano, E. F., Juárez-Altamirano, R., López-García, K. L., Torres-Arreola, R., & Flores‐Rentería, D. (2023) · Land · doi:10.3390/land12111961 · Cited by 4
“On the other hand, the concentration of TC in the soil of the agricultural plots is related to a higher content of SOC, and precisely, we can conﬁrm it with the percentages of SOM in both land uses since, as is well known, the SOM contains about 58% organic carbon [29].”
Background
Soil Ecoenzymatic Stoichiometry Reveals Microbial Metabolic Limitations in Apple Orchards with Cover Crop and Organic Fertilizer Incorporation
Cai, S., Zheng, B., Zhao, Z., Zheng, Z., Yang, N., & Zhai, B. (2024) · Agronomy · doi:10.3390/agronomy14030581 · Cited by 4
Enhancing soil carbon in solar farms through active land management: a systematic review of the available evidence
Carvalho, F., Healing, S., & Armstrong, A. (2024) · Environmental Research Ecology · doi:10.1088/2752-664x/ad8ce4 · Cited by 6
“For instance, diverse grasslands are thought to promote ecological complementarity among species and result in higher productivity and a more diverse supply of plant-derived resources for soil microorganisms compared to less diverse grasslands [58, 60].”
Microhabitat heterogeneity associated with Vanilla spp. and its influences on the microbial community of leaf litter and soil
de Oca-Vásquez, G. M., Solano-Campos, F., Bolaños, B. A., Vásquez, A. P., Vega‐Baudrit, J. R., Ruiz‐Navarro, A., López‐Mondéjar, R., & Bastida, F. (2020) · Soil Ecology Letters · doi:10.1007/s42832-020-0041-7 · Cited by 4
DELINEATING THE DYNAMIC INTERACTION OF VEGETATION AND SOIL PROPERTIES IN CONTROLLING CUT SLOPE SOIL EROSION
HALIM, A., Yusoff, I., Osman, N., & Mohamed, N. A. (2021) · Applied Ecology and Environmental Research · doi:10.15666/aeer/1904_27612778 · Cited by 4
“As such, the higher number of plants in the dense plot (D) could enhance the F/B ratio through ecological complementarity effects such as a higher supply of resources for microorganisms (Lange et al., 2014).”
Background
POSITIVE EFFECTS OF LEGUMES ON SOIL ORGANIC CARBON STORAGE DISAPPEAR AT HIGH LEGUME PROPORTION ACROSS A WIDE RANGE OF ENVIRONMENTAL CONDITIONS IN GRASSLANDS IN THE PYRENEESPreprint
guez, A. R., Canals, R. M., & Sebastià, M. (2020) · doi:10.22541/au.158930956.66985695 · Cited by 4
Long‐Term Grazing Altered Soil Phosphorus Fractions via Inorganic Phosphorus Solubilisation in a Semi‐Arid Grassland
Wang, S., Li, Y., Hu, H., Ding, X., Lin, Q., Li, G., & Xiao-rong, Z. (2025) · European Journal of Soil Science · doi:10.1111/ejss.70176 · Cited by 3
“In this study, the negative correlation between grazing intensity and soil PLFAs (Figure 3 and Figure S3) could be due to the altered soil structure and environment under long-term grazing (Lange et al. 2014; Li et al. 2018; Pan, Liu, et al. 2018).”
Ecological signals of arctic plant-microbe associations are consistent across eDNA and vegetation surveys
Parisy, B., Schmidt, N. M., Wirta, H., Stewart, L., Pellissier, L., Holben, W. E., Pannoni, S. B., Somervuo, P. J., Jones, M. M., Sirén, J., et al. (2023) · Metabarcoding and Metagenomics · doi:10.3897/mbmg.7.99979 · Cited by 3
The content and quality of soil carbon and nitrogen as well as enzymatic activity in soils with diverse texture following different land use and management practices
Dębska, B., Długosz, J., & Piotrowska‐Długosz, A. (2024) · Soil Use and Management · doi:10.1111/sum.13106 · Cited by 3
“…permanent, dense plant cover performs a protective function by preventing the leaching of organic C and nutrients (e.g. nitrogen) from the soil (Burzyńska, 2012) as well as by reducing evaporation, which in turn positively affects soil microbial and enzymatic properties (Lange et al., 2014).”
The interplay between host plants and priority effects in community assembly processes of arbuscular mycorrhizal fungi
Lewe, N. (2023) · doi:10.26686/wgtn.21974357 · Cited by 3
Impact of plant diversity in potato-ley strip-cropping systems on soil microbial communities
Riggi, L. G. A., Sveen, T. R., Castaño, C., Onorati, P., van Apeldoorn, D. F., Berri, M., Mommer, L., Clemmensen, K. E., & Bahram, M. (2024) · Applied Soil Ecology · doi:10.1016/j.apsoil.2024.105777 · Cited by 2
“…yield, but also impact microbial communities (e.g. generally decreasing biomass of soil fungi and benefits saprotrophs (Bartelt-Ryser et al., 2005; Lange et al., 2014; Yu et al., 2022)) and interactions between microbes (e.g. promoting interactions between Rhizobium and AMF, Hnini et al., 2024).”
Differences in nutrient content between heterospecific plant neighbours affect respiration rates of rhizosphere microbiota
Jimeno‐Alda, J., Navarro‐Cano, J. A., Goberna, M., & Verdú, M. (2025) · Plant and Soil · doi:10.1007/s11104-025-07419-1 · Cited by 2
“Despite its subtle influence, it remains significant, as plant functional diversity is a key factor mediating plant–soil microorganism feedback, which in turn influence ecosystem processes (e.g., Sardans 2013; Kardol et al. 2013; Lange et al. 2014).”
Soil health indicators for water-limited regions: Evaluating relative sensitivity to compost and cropping intensification
Strohm, T. N., Fonte, S. J., Ghimire, R., Mikha, M. M., Adebayo, O., Bista, P., Acosta‐Martínez, V., Angadi, S. V., & Schipanski, M. E. (2025) · Journal of Soil and Water Conservation · doi:10.1080/00224561.2025.2477320 · Cited by 2
The shifts in the structure of the prokaryotic community of mountain-grassland soil under the influence of artificial larch plantations
Ivanova, E. A., Abakumov, E. V., Vasilyeva, N., Zverev, A. O., Vladimirov, A., Ksenofontova, N. A., Andronov, E. E., & Kostenko, I. V. (2022) · PLoS ONE · doi:10.1371/journal.pone.0263135 · Cited by 2
Effect of maize and peanut crops on Ivory Coast northern soil biological activities and their response to arbuscular mycorrhizal fungi inoculation
Gisele, A. K., Ndoye, F., Dabonné, S., Bakhoum, N., Faye, M. N., Dioumacor, F., & Diegane, D. (2018) · African Journal of Microbiology Research · doi:10.5897/ajmr2017.8775 · Cited by 2
Microbial Profile of a Calcareous Soil of South Tamil Nadu, India
Maheshwari, P., & Raj, S. A. (2020) · International Journal of Current Microbiology and Applied Sciences · doi:10.20546/ijcmas.2020.910.449 · Cited by 2
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Díaz, J. M. F., González, J. M. F., Calvo, T. G., Becerra, A. T., Pérez, M. S., & Bravo, X. B. L. (2021) · Geoderma · doi:10.1016/j.geoderma.2021.115525 · Cited by 2
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Soil total carbon as a key factor affects soil biota attributes in plant mixtures over time: A meta-analysis
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“We expected to find an indirect positive relationship between plant community diversity and abundance and taxon richness of microbial feeding nematodes, via increased microbial biomass (Lange et al. 2014) and increased organic matter content of the soil (Steinbeiss et al.”
Background
Diversity of Forest Genes: Impacts on the Structure and Function of Soil Ecosystems Under Changing Climate
Dhyani, P., Sati, P., Rawat, S., Tripathi, L. K., Dhyani, S., & Pande, V. (2022) · Springer eBooks · doi:10.1007/978-981-19-0071-6_7 · Cited by 1
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Authors: Lange, M., Habekost, M., Eisenhauer, N., Roscher, C., Bessler, H., Engels, C., Oelmann, Y., Scheu, S., Wilcke, W., Schulze, E.-D., & Gleixner, G.
Affiliations: Max Planck Society (DE)
Friedrich Schiller University Jena (DE)
Helmholtz Centre for Environmental Research (DE)
Humboldt-Universität zu Berlin (DE)
University of Tübingen (DE)
University of Göttingen (DE)
University of Bern (CH)
Corresponding author: Gleixner, Gerd
ORCID: Lange, Markus
Eisenhauer, Nico
Roscher, Christiane
Oelmann, Yvonne
Scheu, Stefan
Wilcke, Wolfgang
Schulze, Ernst-Detlef
Gleixner, Gerd
Venue: PLoS ONE
Publisher: Public Library of Science (PLoS)
Published: 2014-05-09
Volume: 9
Issue: 5
Pages: e96182
ISSN: 1932-6203 (ISSN-L)
DOI: 10.1371/journal.pone.0096182
PMC: PMC4015938
OpenAlex: W2045806593
Cited by: 233
References: 56
Citations by year: 2026: 4 · 2025: 8 · 2024: 19 · 2023: 26 · 2022: 21 · 2021: 30 · 2020: 23 · 2019: 30 · 2018: 21 · 2017: 21 · 2016: 10 · 2015: 16 · 2014: 4
FWCI: 23.98
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: PLoS ONE (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, other-oa)
PubMed Central (publishedVersion, cc-by)
Repository KITopen (Karlsruhe Institute of Technology) (publishedVersion, cc-by)
PubMed (publishedVersion)
BORIS (University Library Bern) (submittedVersion, cc-by)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Max Planck Digital Library (submittedVersion, other-oa)
Figshare (submittedVersion, cc-by)
GoeScholar The Publication Server of the Georg-August-Universität Göttingen (Georg-August-Universität Göttingen) (submittedVersion, cc-by)
GRO (submittedVersion, cc-by)
MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
KITopen (cc-by)
Funders: Johns Hopkins University
Friedrich-Schiller-Universität Jena
Deutsche Forschungsgemeinschaft (FOR 456)
Max-Planck-Gesellschaft
Topics: Life Sciences › Agricultural and Biological Sciences › Soil Science › Soil Carbon and Nitrogen Dynamics
Physical Sciences › Environmental Science › Nature and Landscape Conservation › Ecology and Vegetation Dynamics Studies
Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
Keywords: plant diversity, soil microbial communities, plant functional groups, plant species richness, soil microbial biomass, leaf area index, soil moisture, fungal to bacterial ratio, Fabaceae, plant-derived organic matter, root exudates, phospholipid fatty acids, grassland
MeSH terms: Bacteria, Chromatography, Gas, Fatty Acids, Fungi, Gas Chromatography-Mass Spectrometry, Models, Theoretical, Phospholipids, Plants, Soil, Soil Microbiology, Water, Plant Roots, Biomass, Biodiversity, Grassland

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Biotic and Abiotic Properties Mediating Plant Diversity Effects on Soil Microbial Communities in an Experimental Grassland

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