Microhabitat heterogeneity associated with Vanilla spp. and its influences on the microbial community of leaf litter and soil

Abstract

The impact of forest microhabitats on physiochemical properties of the soil and that of microbial communities on tropical soils remain poorly understood. To elucidate the effect of tropical forest stand on leaf litter and soil microbial communities, we studied enzyme activities, microbial biomass, and diversity in three distinct microhabitats in terms of plant richness, diameter at breast height (DBH), and physiochemical properties of soil and litter, each associated with a different Vanilla sp. In the soil, positive correlations were found between electrical conductivity (EC) and total organic carbon (TOC) with phosphatase activity, and between nitrogen (N) and water-soluble carbon (WSC) content with urease activity (UA). In the litter, the water content was positively correlated with bacterial and fungal biomass, and N and WSC contents were positively correlated with fungal biomass. Positive correlations were found between plant richness and UA in the soil, plant richness and fungal biomass in the soil and litter, and DBH and fungal biomass in the litter. Amplicon sequencing revealed differences between microhabitats in the relative abundance of some fungal and bacterial taxa and in the bacterial community composition of both litter and soil. Bacterial richness and diversity were different between microhabitats, and, in litter samples, they were negatively correlated with DBH and plant richness, respectively. By contrast, none of the soil and litter physiochemical properties were significantly correlated with microbial diversity. Our results show that significant shifts in enzyme activity, microbial biomass, and diversity in the microhabitats were driven by key abiotic and biotic factors depending on the soil or litter sample type.

Keywords

Tropical rainforest / Enzyme activity / Microbial community composition / Microbial biomass / Plant richness

References

[1] Allison, S.D., Jastrow, J.D., 2006. Activities of extracellular enzymes in physically isolated fractions of restored grassland soils. Soil Biology & Biochemistry 38, 3245–3256

[2] Alomia, Y.A., Mosquera-Espinosa, A.T., Flanagan, N.S., Otero, J.T., 2017. Seed viability and symbiotic seed germination in Vanilla spp. (Orchidaceae). Research Journal of Seed Science 10, 43–52

[3] Anderson, M.J., 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 32–46.

[4] Aronesty, E., 2013. Comparison of sequencing utility programs. Open Bioinformatics Journal 7, 1–8

[5] Azofeifa-Bolaños, J., Gigant, L.R., Nicolás-García, M., Pignal, M., Tavares-González, F.B., Hágsater, E., Salazar-Chávez, G.A., Reyes-López, D., Archila-Morales, F.L., García-García, J.A., da Silva, D., Allibert, A., Solano-Campos, F., Rodríguez-Jimenes, G. del C., Paniagua-Vásquez, A., Besse, P., Pérez-Silva, A., Grisoni, M., 2017. A new vanilla species from Costa Rica closely related to V. planifolia (Orchidaceae). European Journal of Taxonomy 284, 1–26

[6] Azofeifa-Bolaños, J.B., Paniagua-Vásquez, A., García-García, J.A., 2014. Importancia y desafíos de la conservación de Vanilla spp. (Orchidaceae) en Costa Rica. Agronomía Mesoamericana 25, 189–202

[7] Azofeifa-Bolaños, J.B., Rivera-Coto, G., Paniagua-Vasquez, A., Cordero-Solórzano, R., 2018. Selección cualitativa del esqueje en la sobreviviencia y desarrollo morfogenético de Vanilla planifolia Andrews. Agronomía Mesoamericana 29, 619–627

[8] Bardgett, R.D., Mommer, L., De Vries, F.T., 2014. Going underground: Root traits as drivers of ecosystem processes. Trends in Ecology & Evolution 29, 692–699

[9] Bastida, F., Torres, I.F., Moreno, J.L., Baldrian, P., Ondoño, S., Ruiz-Navarro, A., Hernández, T., Richnow, H.H., Starke, R., García, C., Jehmlich, N., 2016. The active microbial diversity drives ecosystem multifunctionality and is physiologically related to carbon availability in Mediterranean semi-arid soils. Molecular Ecology 25, 4660–4673

[10] Bligh, E.G., Dyer, W.J., 1959. A rapid method for total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37, 911–917

[11] Bradford, M.A., Wieder, W.R., Bonan, G.B., Fierer, N., Raymond, P.A., Crowther, T.W., 2016. Managing uncertainty in soil carbon feedbacks to climate change. Nature Climate Change 6, 751–758

[12] Brant, J.B., Sulzman, E.W., Myrold, D.D., 2006. Microbial community utilization of added carbon substrates in response to long-term carbon input manipulation. Soil Biology & Biochemistry 38, 2219–2232

[13] Burns, J.H., Anacker, B.L., Strauss, S.Y., Burke, D.J., 2015. Soil microbial community variation correlates most strongly with plant species identity, followed by soil chemistry, spatial location and plant genus. AoB Plants 7, 1–10

[14] Cabugao, K.G., Timm, C.M., Carrell, A.A., Childs, J., Lu, T.Y.S., Pelletier, D.A., Weston, D.J., Norby, R.J., 2017. Root and rhizosphere bacterial phosphatase activity varies with tree species and soil phosphorus availability in Puerto Rico tropical forest. Frontiers of Plant Science 8, 1–14

[15] Caporaso, J.G., Lauber, C.L., Walters, W.A., Berg-Lyons, D., Huntley, J., Fierer, N., Owens, S.M., Betley, J., Fraser, L., Bauer, M., Gormley, N., Gilbert, J.A., Smith, G., Knight, R., 2012. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME Journal 6, 1621–1624

[16] Chen, L., Xiang, W., Wu, H., Ouyang, S., Zhou, B., Zeng, Y., Chen, Y., Kuzyakov, Y., 2019. Tree species identity surpasses richness in affecting soil microbial richness and community composition in subtropical forests. Soil Biology & Biochemistry 130, 113–121

[17] Chung, H., Zak, D.R., Reich, P.B., Ellsworth, D.S., 2007. Plant species richness, elevated CO₂, and atmospheric nitrogen deposition alter soil microbial community composition and function. Global Change Biology 13, 980–989

[18] Cole, J.R., Wang, Q., Fish, J.A., Chai, B., McGarrell, D.M., Sun, Y., Brown, C.T., Porras-Alfaro, A., Kuske, C.R., Tiedje, J.M., 2014. Ribosomal Database Project: Data and tools for high throughput rRNA analysis. Nucleic Acids Research 42, 633–642

[19] Dassen, S., Cortois, R., Martens, H., de Hollander, M., Kowalchuk, G.A., van der Putten, W.H., De Deyn, G.B., 2017. Differential responses of soil bacteria, fungi, archaea and protists to plant species richness and plant functional group identity. Molecular Ecology 26, 4085–4098

[20] Dawson, W., Hör, J., Egert, M., van Kleunen, M., Peste, M., 2017. A small number of low-abundance bacteria dominate plant species-specific responses during rhizosphere colonization. Frontiers in Microbiology 8, 1–13

[21] Delgado-Baquerizo, M., Fry, E.L., Eldridge, D.J., de Vries, F.T., Manning, P., Hamonts, K., Kattge, J., Boenisch, G., Singh, B.K., Bardgett, R.D., 2018a. Plant attributes explain the distribution of soil microbial communities in two contrasting regions of the globe. New Phytologist 219, 574–587

[22] Delgado-Baquerizo, M., Oliverio, A.M., Brewer, T.E., Benavent-González, A., Eldridge, D.J., Bardgett, R.D., Maestre, F.T., Singh, B.K., Fierer, N., 2018b. A global atlas of the dominant bacteria found in soil. Science 359, 320–325

[23] Dungait, J.A.J., Kemmitt, S.J., Michallon, L., Guo, S., Wen, Q., Brookes, P.C., Evershed, R.P., 2011. Variable responses of the soil microbial biomass to trace concentrations of ¹³C-labelled glucose, using ¹³C-PLFA analysis. European Journal of Soil Science 62, 117–126

[24] Edgar, R.C., 2013. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods 10, 996–998

[25] Eisenhauer, N., Lanoue, A., Strecker, T., Scheu, S., Steinauer, K., Thakur, M.P., Mommer, L., 2017. Root biomass and exudates link plant diversity with soil bacterial and fungal biomass. Scientific Reports 7, 1–8

[26] Eivazi, F., Tabatabai, M.A., 1977. Phosphatases in soils. Soil Biology & Biochemistry 9, 167–172

[27] Frostegård, Å., Bååth, E., Tunlio, A., 1993. Shifts in the structure of soil microbial communities in limed forests as revealed by phospholipid fatty acid analysis. Soil Biology & Biochemistry 25, 723–730

[28] Fu, X., Yang, F., Wang, J., Di, Y., Dai, X., Zhang, X., Wang, H., 2015. Understory vegetation leads to changes in soil acidity and in microbial communities 27 years after reforestation. Science of the Total Environment 502, 280–286

[29] García-Franco, N., Martínez-Mena, M., Goberna, M., Albaladejo, J., 2015. Changes in soil aggregation and microbial community structure control carbon sequestration after afforestation of semiarid shrublands. Soil Biology & Biochemistry 87, 110–121

[30] Guangming, L., Xuechen, Z., Xiuping, W., Hongbo, S., Jingsong, Y., Xiangping, W., 2017. Soil enzymes as indicators of saline soil fertility under various soil amendments. Agriculture, Ecosystems & Environment 237, 274–279

[31] Haichar, F., Santaella, C., Heulin, T., Achouak, W., 2014. Root exudates mediated interactions belowground. Soil Biology & Biochemistry 77, 69–80

[32] Hammer, Ø., Harper, D., Ryan, P., 2001. Past: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4, 1–9.

[33] Hartmann, A., Schmid, M., van Tuinen, D., Berg, G., 2009. Plant-driven selection of microbes. Plant and Soil 321, 235–257

[34] Hortal, S., Lozano, Y.M., Bastida, F., Armas, C., Moreno, J.L., Garcia, C., Pugnaire, F.I., 2017. Plant-plant competition outcomes are modulated by plant effects on the soil bacterial community. Scientific Reports 7, 1–9

[35] Huang, X., Liu, S., Wang, H., Hu, Z., Li, Z., You, Y., 2014. Changes of soil microbial biomass carbon and community composition through mixing nitrogen-fixing species with Eucalyptus urophylla in subtropical China. Soil Biology & Biochemistry 73, 42–48

[36] Ihrmark, K., Bödeker, I.T.M., Cruz-Martinez, K., Friberg, H., Kubartova, A., Schenck, J., Strid, Y., Stenlid, J., Brandström-Durling, M., Clemmensen, K.E., Lindahl, B.D., 2012. New primers to amplify the fungal ITS2 region- evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiology Ecology 82, 666–677

[37] IUSS Working Group WRB, 2015. World Reference Base for Soil Resources 2014, update 2015. International soil classification system for naming soils and creating legends for soil maps. FAO, Rome.

[38] Iwaoka, C., Imada, S., Taniguchi, T., Du, S., Yamanaka, N., Tateno, R., 2018. The impacts of soil fertility and salinity on soil nitrogen dynamics mediated by the soil microbial community beneath the halophytic shrub tamarisk. Microbial Ecology 75, 985–996

[39] John, R., Dalling, J.W., Harms, K.E., Yavitt, J.B., Stallard, R.F., Mirabello, M., Hubbell, S.P., Valencia, R., Navarrete, H., Vallejo, M., Foster, R.B., 2007. Soil nutrients influence spatial distributions of tropical trees species. Proceedings of the National Academy of Sciences of the United States of America 104, 864–869

[40] Kandeler, E., Gerber, H., 1988. Short-term assay of soil urease activity using colorimetric determination of ammonium. Biology and Fertility of Soils 6, 68–72

[41] Kardol, P., Wardle, D.A., 2010. How understanding aboveground-belowground linkages can assist restoration ecology. Trends in Ecology & Evolution 25, 670–679

[42] Karremans, A.P., Lehmann, C., 2018. A highly threatened new species of Vanilla from Costa Rica. Lindleyana 87, 304–307.

[43] Khlifa, R., Paquette, A., Messier, C., Reich, P.B., Munson, A.D., 2017. Do temperate tree species diversity and identity influence soil microbial community function and composition? Ecology and Evolution 7, 7965–7974

[44] Kivlin, S.N., Hawkes, C.V., 2016. Temporal and spatial variation of soil bacteria richness, composition, and function in a neotropical rainforest. PLoS One 11, 1–17

[45] Koljalg, U., Nilsson, R.H., Abarenkov, K., Tedersoo, L., Taylor, A.F.S., Bahram, M., Bates, S.T., Bruns, T.D., Bengtsson-Palme, J., Callaghan, T.M., Douglas, B., Drenkhan, T., Eberhardt, U., Dueñas, M., Grebenc, T., Griffith, G.W., Hartmann, M., Kirk, P.M., Kohout, P., Larsson, E., Lindahl, B.D., Lücking, R., Martín, M.P., Matheny, P.B., Nguyen, N.H., Niskanen, T., Oja, J., Peay, K.G., Peintner, U., Peterson, M., Põldmaa, K., Saag, L., Saar, I., Schüßler, A., Scott, J.A., Senés, C., Smith, M.E., Suija, A., Taylor, D.L., Telleria, M.T., Weiss, M., Larsson, K.H., 2014. Towards a unified paradigm for sequence-based identification of fungi. Molecular Ecology 22, 5271–5277

[46] Korthou, H., Verpoorte, R., 2007. Vanilla. In: Berger, R.G., ed. Flavours and fragrances: Chemistry, bioprocessing and sustainability. Berlin: Springer-Verlag, 203–217.

[47] Landesman, W.J., Nelson, D.M., Fitzpatrick, M.C., 2014. Soil properties and tree species drive b-diversity of soil bacterial communities. Soil Biology & Biochemistry 76, 201–209

[48] Lange, M., Habekost, M., Eisenhauer, N., Roscher, C., Bessler, H., Engels, C., Oelmann, Y., Scheu, S., Wilcke, W., Schulze, E.D., Gleixner, G., 2014. Biotic and abiotic properties mediating plant diversity effects on soil microbial communities in an experimental grassland. PLoS One 9, e96182

[49] Leff, J.W., Nemergut, D.R., Grandy, A.S., O’Neill, S.P., Wickings, K., Townsend, A.R., Cleveland, C.C., 2012. The effects of soil bacterial community structure on decomposition in a tropical rain forest. Ecosystems (New York, N.Y.) 15, 284–298

[50] Lemanowicz, J., 2018. Dynamics of phosphorus content and the activity of phosphatase in forest soil in the sustained nitrogen compounds emissions zone. Environmental Science and Pollution Research International 25, 33773–33782

[51] Lemanowicz, J., Bartkowiak, A., 2016. Changes in the activity of phosphatase and the content of phosphorus in salt-affected soils grassland habitat natura 2000. Polish Journal of Soil Science 49, 149–165

[52] Liu, X., Liang, M., Etienne, R.S., Wang, Y., Staehelin, C., Yu, S., 2012. Experimental evidence for a phylogenetic Janzen-Connell effect in a subtropical forest. Ecology Letters 15, 111–118

[53] Liu, Y., Sun, X., Li, S., Li, S., Zhou, W., Ma, Q., Zhang, J., 2019. Influence of green waste compost on Pb-polluted soil remediation, soil quality improvement, and uptake by Pakchoi cabbage (Brassica campestris L. ssp). Environmental Science and Pollution Research International.

[54] Lladó S., López-Mondéjar, R., Baldrian, P., 2017. Forest soil bacteria: Diversity, involvement in ecosystem processes, and response to global change. Microbiology and Molecular Biology Reviews 81, e00063–e16

[55] Looby, C.I., Treseder, K.K., 2018. Shifts in soil fungi and extracellular enzyme activity with simulated climate change in a tropical montane cloud forest. Soil Biology & Biochemistry 117, 87–96

[56] Loranger-Merciris, G., Barthes, L., Gastine, A., Leadley, P., 2006. Rapid effects of plant species diversity and identity on soil microbial communities in experimental grassland ecosystems. Soil Biology & Biochemistry 38, 2336–2343

[57] Lozano, Y.M., Armas, C., Hortal, S., Casanoves, F., Pugnaire, F.I., 2017. Disentangling above- and below-ground facilitation drivers in arid environments: the role of soil microorganisms, soil properties and microhabitat. New Phytologist 216, 1236–1246

[58] Luo, X., Fu, X., Yang, Y., Cai, P., Peng, S., Chen, W., Huang, Q., 2016. Microbial communities play important roles in modulating paddy soil fertility. Scientific Reports 6, 1–12

[59] Margalef, O., Sardans, J., Fernández-Martínez, M., Molowny-Horas, R., Janssens, I.A., Ciais, P., Goll, D., Richter, A., Obersteiner, M., Asensio, D., Peñuelas, J., 2017. Global patterns of phosphatase activity in natural soils. Scientific Reports 7, 1–13

[60] Maruenda, H., Vico, M.D.L., Householder, J.E., Janovec, J.P., Cañari, C., Naka, A., Gonzalez, A.E., 2013. Exploration of Vanilla pompona from the Peruvian Amazon as a potential source of vanilla essence: Quantification of phenolics by HPLC-DAD. Food Chemistry 138, 161–167

[61] Mazzon, M., Cavani, L., Margon, A., Sorrenti, G., Ciavatta, C., Marzadori, C., 2018. Changes in soil phenol oxidase activities due to long-term application of compost and mineral N in a walnut orchard. Geoderma 316, 70–77

[62] McCarthy-Neumann, S., Kobe, R.K., 2010. Conspecific plant-soil feedbacks reduce survivorship and growth of tropical tree seedlings. Journal of Ecology 98, 396–407

[63] McGee, K.M., Eaton, W.D., Shokralla, S., Hajibabaei, M., 2018. Determinants of soil bacterial and fungal community composition toward carbon-use efficiency across primary and secondary forests in a Costa Rican conservation area. Microbial Ecology 77, 148–167

[64] Nemergut, D.R., Cleveland, C.C., Wieder, W.R., Washenberger, C.L., Townsend, A.R., 2010. Plot-scale manipulations of organic matter inputs to soils correlate with shifts in microbial community composition in a lowland tropical rain forest. Soil Biology & Biochemistry 42, 2153–2160

[65] Nicolai, V., 1988. Phenolic and mineral content of leaves influences decomposition in European Forest Ecosystems. Oecologia 75, 575–579

[66] Nielsen, U.N., Osler, G.H.R., Campbell, C.D., Burslem, D.F.R.P., van der Wal, R., 2010. The influence of vegetation type, soil properties and precipitation on the composition of soil mite and microbial communities at the landscape scale. Journal of Biogeography 37, 1317–1328

[67] Ochoa-Hueso, R., Eldridge, D.J., Delgado-Baquerizo, M., Soliveres, S., Bowker, M.A., Gross, N., Le Bagousse-Pinguet, Y., Quero, J.L., García-Gómez, M., Valencia, E., Arredondo, T., Beinticinco, L., Bran, D., Cea, A., Coaguila, D., Dougill, A.J., Espinosa, C.I., Gaitán, J., Guuroh, R.T., Guzman, E., Gutiérrez, J.R., Hernández, R.M., Huber-Sannwald, E., Jeffries, T., Linstädter, A., Mau, R.L., Monerris, J., Prina, A., Pucheta, E., Stavi, I., Thomas, A.D., Zaady, E., Singh, B.K., Maestre, F.T., 2018. Soil fungal abundance and plant functional traits drive fertile island formation in global drylands. Journal of Ecology 106, 242–253

[68] Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P.R., O’Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.H., Szoecs, E., Wagner, H., 2019. vegan: Community Ecology Package. R package version2.5–6.

[69] Ondoño, S., Bastida, F., Moreno, J.L., 2014. Microbiological and biochemical properties of artificial substrates: A preliminary study of its application as Technosols or as a basis in Green Roof Systems. Ecological Engineering 70, 189–199

[70] Pind, A., Freeman, C., Lock, M.A., 1994. Enzymic degradation of phenolic materials in peatlands-measurement of phenol oxidase activity. Plant and Soil 159, 227–231

[71] Prather, C., Strickland, M.S., Laws, A., Branson, D., 2017. Herbivore species identity and composition affect soil enzymatic activity through altered plant composition in a coastal tallgrass prairie. Soil Biology & Biochemistry 112, 277–280

[72] Prober, S.M., Leff, J.W., Bates, S.T., Borer, E.T., Firn, J., Harpole, W.S., Lind, E.M., Seabloom, E.W., Adler, P.B., Bakker, J.D., Cleland, E.E., Decrappeo, N.M., Delorenze, E., Hagenah, N., Hautier, Y., Hofmockel, K.S., Kirkman, K.P., Knops, J.M.H., La Pierre, K.J., Macdougall, A.S., Mcculley, R.L., Mitchell, C.E., Risch, A.C., Schuetz, M., Stevens, C.J., Williams, R.J., Fierer, N., 2015. Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide. Ecology Letters 18, 85–95

[73] R Core Team, (2019). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL

[74] Ramirez, K.S., Knight, C.G., De Hollander, M., Brearley, F.Q., Constantinides, B., Cotton, A., Creer, S., Crowther, T.W., Davison, J., Delgado-Baquerizo, M., Dorrepaal, E., Elliott, D.R., Fox, G., Griffiths, R.I., Hale, C., Hartman, K., Houlden, A., Jones, D.L., Krab, E.J., Maestre, F.T., Mcguire, K.L., Monteux, S., Orr, C.H., Van Der Putten, W.H., Roberts, I.S., Singh, B.K., Straathof, A.L., Bhatnagar, J.M., Thion, C., 2017. Detecting macroecological patterns in bacterial communities across independent studies of global soils. Nature Microbiology 3, 189–196

[75] Ranadive, A., 2011. Quality control of vanilla beans and extracts. In: Havkin-Frenkel, D., Belanger, F., eds. Handbook of Vanilla Science and Technology. New Jersey: Wiley-Blackwell, 141–161.

[76] Rinnan, R., Bååth, E., 2009. Differential utilization of carbon substrates by bacteria and fungi in tundra soil. Applied and Environmental Microbiology 75, 3611–3620

[77] Saetre, P., 1999. Spatial patterns of ground vegetation, soil microbial biomass and activity in a mixed spruce-birch stand. Ecography 22, 183–192

[78] Saha, S., Gopinath, K.A., Mina, B.L., Gupta, H.S., 2008. Influence of continuous application of inorganic nutrients to a Maize-Wheat rotation on soil enzyme activity and grain quality in a rainfed Indian soil. European Journal of Soil Biology 44, 521–531

[79] Schilling, E.M., Waring, B.G., Schilling, J.S., Powers, J.S., 2016. Forest composition modifies litter dynamics and decomposition in regenerating tropical dry forest. Oecologia 182, 287–297

[80] Schlatter, D.C., Bakker, M.G., Bradeen, J.M., Kinkel, L.L., 2015. Plant community richness and microbial interactions structure bacterial communities in soil. Ecology 96, 134–142

[81] Si, P., Shao, W., Yu, H., Yang, X., Gao, D., Qiao, X., Wang, Z., Wu, G., 2018. Rhizosphere microenvironments of eight common deciduous fruit trees were shaped by microbes in northern China. Frontiers in Microbiology 9, 1–17

[82] Singh, K., 2016. Microbial and enzyme activities of saline and sodic soils. Land Degradation & Development 27, 706–718.

[83] Sinsabaugh, R.L., 2010. Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biology & Biochemistry 42, 391–404

[84] Smith, A.P., Marín-Spiotta, E., Balser, T., 2015. Successional and seasonal variations in soil and litter microbial community structure and function during tropical postagricultural forest regeneration: A multiyear study. Global Change Biology 21, 3532–3547

[85] Song, Y., Song, C., Shi, F., Wang, M., Ren, J., Wang, X., Jiang, L., 2019. Linking plant community composition with the soil C pool, N availability and enzyme activity in boreal peatlands of Northeast China. Applied Soil Ecology 140, 144–154

[86] Steinauer, K., Tilman, D., Wragg, P.D., Cesarz, S., Cowles, J.M., Pritsch, K., Reich, P.B., Weisser, W.W., Eisenhauer, N., 2015. Plant diversity effects on soil microbial functions and enzymes are stronger than warming in a grassland experiment. Ecology 96, 99–112

[87] Štursova, M., Bárta, J., Šantručková H., Baldrian, P., 2016. Small-scale spatial heterogeneity of ecosystem properties, microbial community composition and microbial activities in a temperate mountain forest soil. FEMS Microbiology Ecology 92, 1–10

[88] Tabatabai, M.A., Bremner, J.M., 1969. Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biology & Biochemistry 1, 301–307

[89] Tedersoo, L., Bahram, M., Põlme, S., Kõljalg, U., Yorou, N.S., Wijesundera, R., Ruiz, L.V., Vasco-Palacios, A.M., Thu, P.Q., Suija, A., Smith, M.E., Sharp, C., Saluveer, E., Saitta, A., Rosas, M., Riit, T., Ratkowsky, D., Pritsch, K., Põldmaa, K., Piepenbring, M., Phosri, C., Peterson, M., Parts, K., Pärtel, K., Otsing, E., Nouhra, E., Njouonkou, A.L., Nilsson, R.H., Morgado, L.N., Mayor, J., May, T.W., Majuakim, L., Lodge, D.J., Lee, S.S., Larsson, K.H., Kohout, P., Hosaka, K., Hiiesalu, I., Henkel, T.W., Harend, H., Guo, L., Greslebin, A., Grelet, G., Geml, J., Gates, G., Dunstan, W., Dunk, C., Drenkhan, R., Dearnaley, J., De Kesel, A., Dang, T., Chen, X., Buegger, F., Brearley, F.Q., Bonito, G., Anslan, S., Abell, S., Abarenkov, K., 2014. Global diversity and geography of soil fungi. Science 346, 1256688

[90] Tianzhu, L., Guicai, S., Jian, W., Gengxin, Z., 2017. Microbial communities and associated enzyme activities in alpine wetlands with increasing altitude on the Tibetan Plateau. Wetlands 37, 401–412

[91] Torres, P.A., Abril, A.B., Bucher, E.H., 2005. Microbial succession in litter decomposition in the semi-arid Chaco woodland. Soil Biology & Biochemistry 37, 49–54

[92] Van Nuland, M.E., Wooliver, R.C., Pfennigwerth, A.A., Read, Q.D., Ware, I.M., Mueller, L., Fordyce, J.A., Schweitzer, J.A., Bailey, J.K., 2016. Plant–soil feedbacks: connecting ecosystem ecology and evolution. Functional Ecology 30, 1032–1042

[93] Větrovský T., Baldrian, P., Morais, D., 2018. SEED 2: A user-friendly platform for amplicon high-throughput sequencing data analyses. Bioinformatics (Oxford, England) 34, 2292–2294

[94] Wakelin, S.A., Gerard, E., van Koten, C., Banabas, M., O’Callaghan, M., Nelson, P.N., 2016. Soil physicochemical properties impact more strongly on bacteria and fungi than conversion of grassland to oil palm. Pedobiologia 59, 83–91

[95] Wang, X.Y., Ge, Y., Wang, J., 2017. Positive effects of plant diversity on soil microbial biomass and activity are associated with more root biomass production. Journal of Plant Interactions 12, 533–541

[96] Waring, B.G., 2013. Exploring relationships between enzyme activities and leaf litter decomposition in a wet tropical forest. Soil Biology & Biochemistry 64, 89–95

[97] Waring, B.G., Adams, R., Branco, S., Powers, J.S., 2016. Scale-dependent variation in nitrogen cycling and soil fungal communities along gradients of forest composition and age in regenerating tropical dry forests. New Phytologist 209, 845–854

[98] Watteyn, C., Fremout, T., Karremans, A.P., Huarcaya, R.P., Azofeifa, J.B., Reubens, B., Muys, B., 2020. Vanilla distribution modeling for conservation and sustainable cultivation in a joint land sparing/sharing concept. Ecosphere 11, e03056

[99] Wei, K., Sun, T., Tian, J., Chen, Z., Chen, L., 2018. Soil microbial biomass, phosphatase and their relationships with phosphorus turnover under mixed inorganic and organic nitrogen addition in a Larix gmelinii plantation. Forest Ecology and Management 422, 313–322

[100] Wu, N., Li, Z., Wu, F., Tang, M., 2019. Microenvironment and microbial community in the rhizosphere of dioecious Populus cathayana at Chaka Salt Lake. Journal of Soils and Sediments 19, 2740–2751

[101] Xie, E., Ding, A., Zheng, L., Lu, C., Wang, J., Huang, B., Xiu, H., 2016. Seasonal variation in populations of nitrogen-transforming bacteria and correlation with nitrogen removal in a full-scale horizontal flow constructed wetland treating polluted river water. Geomicrobiology Journal 33, 338–346

[102] Xiong, W., Zhao, Q., Xue, C., Xun, W., Zhao, J., Wu, H., Li, R., Shen, Q., 2016. Comparison of fungal community in black pepper-vanilla and vanilla monoculture systems associated with vanilla Fusarium wilt disease. Frontiers in Microbiology 7, 1–8

[103] Yao, Q., Li, Z., Song, Y., Wright, S.J., Guo, X., Tringe, S.G., Tfaily, M.M., Paša-Tolić L., Hazen, T.C., Turner, B.L., Mayes, M.A., Pan, C., 2018. Community proteogenomics reveals the systemic impact of phosphorus availability on microbial functions in tropical soil. Nature Ecology & Evolution 2, 499–509

[104] Zhang, C., Wang, J., Liu, G., Song, Z., Fang, L., 2019. Impact of soil leachate on microbial biomass and diversity affected by plant diversity. Plant and Soil 439, 505–523

[105] Zhang, C.B., Wang, J., Liu, W.L., Zhu, S.X., Liu, D., Chang, S.X., Chang, J., Ge, Y., 2010. Effects of plant diversity on nutrient retention and enzyme activities in a full-scale constructed wetland. Bioresource Technology 101, 1686–1692

[106] Zhang, Q., Wu, J., Yang, F., Lei, Y., Zhang, Q., Cheng, X., 2016a. Alterations in soil microbial community composition and biomass following agricultural land use change. Scientific Reports 6, 1–10

[107] Zhang, T., Zhang, J., Wang, T., Tian, X., Ge, H., Ma, Y., Wang, K., 2016b. Effects of organic matter on Leymus chinensis germination, growth, and urease activity and available nitrogen in coastal saline soil. Toxicological and Environmental Chemistry 98, 623–629

[108] Zhang, W., Qiao, W., Gao, D., Dai, Y., Deng, J., Yang, G., Han, X., Ren, G., 2018. Relationship between soil nutrient properties and biological activities along a restoration chronosequence of Pinus tabulaeformis plantation forests in the Ziwuling Mountains, China. Catena 161, 85–95

[109] Žifčáková L., Větrovský T., Howe, A., Baldrian, P., 2016. Microbial activity in forest soil reflects the changes in ecosystem properties between summer and winter. Environmental Microbiology 18, 288–301

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