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

Gabriela Montes de Oca-Vásquez, Frank Solano-Campos, Bernal Azofeifa-Bolaños, Amelia Paniagua-Vasquez, José Vega-Baudrit, Antonio Ruiz-Navarro, Rubén López-Mondéjar, Felipe Bastida

PDF(652 KB)
PDF(652 KB)
Soil Ecology Letters ›› 2020, Vol. 2 ›› Issue (3) : 195-208. DOI: 10.1007/s42832-020-0041-7
RESEARCH ARTICLE
RESEARCH ARTICLE

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

Author information +
History +

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

Cite this article

Download citation ▾
Gabriela Montes de Oca-Vásquez, Frank Solano-Campos, Bernal Azofeifa-Bolaños, Amelia Paniagua-Vasquez, José Vega-Baudrit, Antonio Ruiz-Navarro, Rubén López-Mondéjar, Felipe Bastida. Microhabitat heterogeneity associated with Vanilla spp. and its influences on the microbial community of leaf litter and soil. Soil Ecology Letters, 2020, 2(3): 195‒208 https://doi.org/10.1007/s42832-020-0041-7

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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[24]
Edgar, R.C., 2013. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods 10, 996–998
CrossRef Google scholar
[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
CrossRef Google scholar
[26]
Eivazi, F., Tabatabai, M.A., 1977. Phosphatases in soils. Soil Biology & Biochemistry 9, 167–172
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[31]
Haichar, F., Santaella, C., Heulin, T., Achouak, W., 2014. Root exudates mediated interactions belowground. Soil Biology & Biochemistry 77, 69–80
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[41]
Kardol, P., Wardle, D.A., 2010. How understanding aboveground-belowground linkages can assist restoration ecology. Trends in Ecology & Evolution 25, 670–679
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[65]
Nicolai, V., 1988. Phenolic and mineral content of leaves influences decomposition in European Forest Ecosystems. Oecologia 75, 575–579
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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. https://CRAN.R-project.org/package=vegan.
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[73]
R Core Team, (2019). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/.
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[77]
Saetre, P., 1999. Spatial patterns of ground vegetation, soil microbial biomass and activity in a mixed spruce-birch stand. Ecography 22, 183–192
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar

Acknowledgments

The authors are grateful to the Osa Conservation Organization for allowing access for sampling at Piro Biological Station. They are also grateful to the Spanish Ministry of Science and the Spanish Research Council (CSIC) call “I-COOP Suelos y Legumbres 2016” for the funded project (2016SU0013). This work was supported by the Universidad Nacional, Costa Rica (grant number SIA-0249-18). This study was performed with permission from Costa Rica’s Ministry of Environment and Energy (R-002-2019-OT-CONAGEBIO).

Electronic supplementary material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s42832-020-0041-7 and is accessible for authorized users.

RIGHTS & PERMISSIONS

2020 Higher Education Press
AI Summary AI Mindmap
PDF(652 KB)

Accesses

Citations

Detail

Sections
Recommended

/