Seasonal dynamics of soil bacterial and fungal communities in Colombian tropical forests and páramo ecosystems

Abstract

Understanding the dynamics of soil microbial communities and their responses to seasonal fluctuations is crucial for maintaining soil health and predicting the effects of climate change. We investigated seasonal impacts on soil microorganisms in tropical dry forests, Andean forests, and páramos. We characterized bacterial and fungal communities using 16S rRNA and ITS gene metabarcoding, complemented by soil chemical analysis. Proteobacteria, Actinobacteriota, Acidobacteriota, and Chloroflexi dominated bacterial communities. Fungi primarily comprised Ascomycota, Basidiomycota, and Mortierellomycota across all ecosystems. Bacterial Shannon diversity was significantly higher during the dry season at all sites, irrespective of ecosystem type. While fungal communities also showed higher species richness in the dry season, these differences were not statistically significant. Correlations between microbial communities and soil properties were generally stronger in the dry season, particularly in tropical dry forests. These findings suggest bacterial communities are more responsive to seasonal environmental shifts, whereas fungal communities exhibit greater structural stability. The páramo notably exhibited the greatest seasonal variability and highest proportion of unclassified reads, underscoring its ecological sensitivity and need for further research and conservation. This study provides valuable insights into the temporal dynamics of microbes in underexplored ecosystems, which are particularly vulnerable to the effects of climate change.

Graphical abstract

Keywords

forest microbiome / metabarcoding / soil ecology / soil microorganisms

Highlight

	● The microbial communities in the forest soils of the studied ecosystems generally demonstrated higher abundances during the dry season sampling event in comparison to the rainy season sampling event.
	● Seasonal climatic variations significantly affected the diversity of soil microbial communities in tropical forests.
	● Soil chemical properties had a more pronounced influence on bacterial communities during the dry season sampling event than in the rainy season sampling event.

References

[1] Andrews, S., 2010. FastQC: a quality control tool for high throughput sequence data [Online]. Available at the website of bioinformatics.babraham.ac.uk/projects/fastqc/.

[2] Bai, Z.Y., Jia, A.M., Li, H.X., Wang, M.J., Qu, S.M., 2023. Explore the soil factors driving soil microbial community and structure in Songnen alkaline salt degraded grassland. Frontiers in Plant Science14, 1110685.

[3] Baldrian, P., 2017. Forest microbiome: diversity, complexity and dynamics. FEMS Microbiology Reviews41, 109–130.

[4] Beidler, K.V., Powers, J.S., Dupuy-Rada, J.M., Hulshof, C., Medvigy, D., Pizano, C., Salgado-Negret, B., Van Bloem, S.J., Vargas, G.G., Waring, B.G., Kennedy, P.G., 2023. Seasonality regulates the structure and biogeochemical impact of ectomycorrhizal fungal communities across environmentally divergent neotropical dry forests. Journal of Ecology111, 1598–1613.

[5] Bellemain, E., Carlsen, T., Brochmann, C., Coissac, E., Taberlet, P., & Kauserud, H., 2010. ITS as an environmental DNA barcode for fungi: An in silico approach reveals potential PCR biases. BMC Microbiology, 10, 189.

[6] Bhardwaj, Y., Reddy, B., Dubey, S.K., 2020. Temporal shift in methanotrophic community and methane oxidation potential in forest soils of dry tropics: high-throughput metagenomic approach. Biology and Fertility of Soils56, 859–867.

[7] Brugnoli, E., Verocai, J., Muniz, P., García-Rodríguez, F., 2017. Weather, hydrological and oceanographic conditions of the northern coast of the Río de la Plata estuary during ENSO 2009–2010. In: Froneman, W., ed. Estuary. London: IntechOpen111, 1598–1613.

[8] Buscardo, E., Geml, J., Nagy, L., 2024. Seasonal dependence of deterministic versus stochastic processes influencing soil fungal community composition in a lowland Amazonian rain forest. Communications Earth & Environment5, 334.

[9] Buscardo, E., Souza, R.C., Meir, P., Geml, J., Schmidt, S.K., da Costa, A.C.L., Nagy, L., 2021. Effects of natural and experimental drought on soil fungi and biogeochemistry in an Amazon rain forest. Communications Earth & Environment2, 55.

[10] Cai, W.J., Santoso, A., Collins, M., Dewitte, B., Karamperidou, C., Kug, J.S., Lengaigne, M., McPhaden, M.J., Stuecker, M.F., Taschetto, A.S., Timmermann, A., Wu, L.X., Yeh, S.W., Wang, G.J., Ng, B., Jia, F., Yang, Y., Ying, J., Zheng, X.T., Bayr, T., Brown, J.R., Capotondi, A., Cobb, K.M., Gan, B.L., Geng, T., Ham, Y.G., Jin, F.F., Jo, H.S., Li, X.C., Lin, X.P., Mcgregor, S., Park, J.H., Stein, K., Yang, K., Zhang, L., Zhong, W.X., 2021. Changing El Niño–Southern Oscillation in a warming climate. Nature Reviews Earth & Environment2, 628–644.

[11] Chen, L.C., Guan, X., Li, H.M., Wang, Q.K., Zhang, W.D., Yang, Q.P., Wang, S.L., 2019. Spatiotemporal patterns of carbon storage in forest ecosystems in Hunan Province, China. Forest Ecology and Management432, 656–666.

[12] Chen, X., Xu, G.C., Xiong, P., Peng, J.B., Fang, K., Wan, S., Wang, B., Gu, F.Y., Li, J., Xiong, H.J., 2023. Dry and wet seasonal variations of the sediment fungal community composition in the semi-arid region of the Dali River, Northwest China. Environmental Science and Pollution Research30, 123694–123709.

[13] Cresso, M., Clerici, N., Sanchez, A., Jaramillo, F., 2020. Future climate change renders unsuitable conditions for paramo ecosystems in Colombia. Sustainability12, 8373.

[14] Du, C., Xu, C.Y., Jian, J.S., He, W.X., Hou, L., Geng, Z.C., 2018. Seasonal dynamics of bacterial communities in a Betula albosinensis forest. European Journal of Soil Science69, 666–674.

[15] Estrada-Bonilla, G.A., Lopes, C.M., Durrer, A., Alves, P.R.L., Passaglia, N., Cardoso, E.J.B.N., 2017. Effect of phosphate-solubilizing bacteria on phosphorus dynamics and the bacterial community during composting of sugarcane industry waste. Systematic and Applied Microbiology40, 308–313.

[16] Fiore-Donno, A.M., Freudenthal, J., Dahl, M.B., Rixen, C., Urich, T., Bonkowski, M., 2024. Biotic interactions explain seasonal dynamics of the alpine soil microbiome. ISME Communications4, ycae028.

[17] Gao, G.F., Song, L.Y., Zhang, Y.H., Chu, H.Y., 2024. Expedited loss of soil biodiversity in blue carbon ecosystems caused by rising sea levels. Soil Biology and Biochemistry191, 109348.

[18] Gazol, A., González de Andrés, E., Valverde, Á., Igual, J.M., Serrano, A., Camarero, J.J., 2024. The strong seasonality of soil microbial community structure in declining Mediterranean pine forests depends more on soil conditions than on tree vitality. Science of the Total Environment957, 177560.

[19] Gerhard, L., Puhlmann, H., Vogt, M., Luster, J., 2021. Phosphorus leaching from naturally structured forest soils is more affected by soil properties than by drying and rewetting. Frontiers in Forests and Global Change4, 543037.

[20] Grosso, F., Iovieno, P., Alfani, A., De Nicola, F., 2018. Structure and activity of soil microbial communities in three Mediterranean forests. Applied Soil Ecology130, 280–287.

[21] Gschwend, F., Hartmann, M., Mayerhofer, J., Hug, A.S., Enkerli, J., Gubler, A., Meuli, R.G., Frey, B., Widmer, F., 2021. Site and land-use associations of soil bacteria and fungi define core and indicative taxa. FEMS Microbiology Ecology97, fiab165.

[22] Han, W.J., Wang, G.M., Liu, J.L., Ni, J., 2021. Effects of vegetation type, season, and soil properties on soil microbial community in subtropical forests. Applied Soil Ecology158, 103813.

[23] Hasnat, G.N.T., Hossain, M.K., 2020. Global overview of tropical dry forests. In: Bhadouria, R., Tripathi, S., Srivastava, P., Singh, P., eds. Handbook of Research on the Conservation and Restoration of Tropical Dry Forests. Hershey: IGI Global1–23.

[24] Hjelmsø, M. H., Hansen, L. H., Bælum, J., Feld, L., Holben, W. E., & Jacobsen, C. S., 2014. High-Resolution Melt Analysis for Rapid Comparison of Bacterial Community Compositions. Applied and Environmental Microbiology, 80, 3568-3575.

[25] Huang, H.Y., Zhou, L., Chen, J., Wei, T.Y., 2020. ggcor: Extended Tools for Correlation Analysis and Visualization. R Package Version 0.9.7.

[26] James, J., Harrison, R., 2016. The effect of harvest on forest soil carbon: a meta-analysis. Forests7, 308.

[27] Jansson, J.K., Hofmockel, K.S., 2020. Soil microbiomes and climate change. Nature Reviews Microbiology18, 35–46.

[28] Ji, L., Yang, Y.C., Yang, L.X., 2021. Seasonal variations in soil fungal communities and co-occurrence networks along an altitudinal gradient in the cold temperate zone of China: a case study on Oakley Mountain. CATENA204, 105448.

[29] Jin, Y.Y., Wei, X.K., White, J.F., Chen, T.X., Li, X.Z., Chen, Z.J., Li, C.J., 2022. Soil fungal and bacterial communities are altered by the incorporation of leaf litter containing a fungal endophyte. European Journal of Soil Science73, e13240.

[30] Kačergius, A., Sivojienė, D., Gudiukaitė, R., Bakšienė, E., Masevičienė, A., Žičkienė, L., 2023. Comparison of the structure of soil microbial communities of different ecosystems using the microbiome sequencing approach. Soil Systems7, 70.

[31] Kõljalg, U., Nilsson, H.R., Schigel, D., Tedersoo, L., Larsson, K.H., May, T.W., Taylor, A.F.S., Jeppesen, T.S., Frøslev, T.G., Lindahl, B.D., Põldmaa, K., Saar, I., Suija, A., Savchenko, A., Yatsiuk, I., Adojaan, K., Ivanov, F., Piirmann, T., Pöhönen, R., Zirk, A., Abarenkov, K., 2020. The taxon hypothesis paradigm—on the unambiguous detection and communication of taxa. Microorganisms8, 1910.

[32] Lahti, L., Shetty, S., 2019. Microbiome R package. Bioconductor.

[33] Lepcha, N.T., Devi, N.B., 2020. Effect of land use, season, and soil depth on soil microbial biomass carbon of Eastern Himalayas. Ecological Processes9, 65.

[34] Li, G.L., Kim, S., Han, S.H., Chang, H.N., Du, D.L., Son, Y., 2018. Precipitation affects soil microbial and extracellular enzymatic responses to warming. Soil Biology and Biochemistry120, 212–221.

[35] Li, X.L., Qu, Z.L., Zhang, Y.M., Ge, Y., Sun, H., 2022a. Soil fungal community and potential function in different forest ecosystems. Diversity14, 520.

[36] Li, X.P., Kong, P., Daughtrey, M., Kosta, K., Schirmer, S., Howle, M., Likins, M., Hong, C.X., 2022b. Characterization of the soil bacterial community from selected boxwood gardens across the United States. Microorganisms10, 1514.

[37] Li, Y.Q., Ma, J.W., Li, Y.J., Shen, X.Y., Xia, X.H., 2024. Microbial community and enzyme activity respond differently to seasonal and edaphic factors in forest and grassland ecosystems. Applied Soil Ecology194, 105167.

[38] Lin, Y.B., Yang, L., Chen, Z.T., Gao, Y.Q., Kong, J.J., He, Q., Su, Y., Li, J.Y., Qiu, Q., 2023. Seasonal variations of soil bacterial and fungal communities in a subtropical Eucalyptus plantation and their responses to throughfall reduction. Frontiers in Microbiology14, 1113616.

[39] Lu, J., Rincon, N., Wood, D.E., Breitwieser, F.P., Pockrandt, C., Langmead, B., Salzberg, S.L., Steinegger, M., 2022. Metagenome analysis using the Kraken software suite. Nature Protocols17, 2815–2839.

[40] Luo, S.P., He, B.H., Zeng, Q.P., Li, N.J., Yang, L., 2020. Effects of seasonal variation on soil microbial community structure and enzyme activity in a Masson pine forest in Southwest China. Journal of Mountain Science17, 1398–1409.

[41] Luo, X.H., Wang, M.K., Hu, G.P., Weng, B.Q., 2019. Seasonal change in microbial diversity and its relationship with soil chemical properties in an orchard. PLoS One14, e0215556.

[42] Ma, W.X., Yang, Z., Liang, L.S., Ma, Q.H., Wang, G.X., Zhao, T.T., 2021. Seasonal changes in soil microbial community and co-occurrence network of species of the genus Corylus. Microorganisms9, 2228.

[43] Mabagala, F.S., Mng’ong’o, M.E., 2022. On the tropical soils; the influence of organic matter (OM) on phosphate bioavailability. Saudi Journal of Biological Sciences29, 3635–3641.

[44] Maurice, K., Bourceret, A., Youssef, S., Boivin, S., Laurent-Webb, L., Damasio, C., Boukcim, H., Selosse, M.A., Ducousso, M., 2024. Anthropic disturbances impact the soil microbial network structure and stability to a greater extent than natural disturbances in an arid ecosystem. Science of the Total Environment907, 167969.

[45] Oksanen, J., Simpson, G.L., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O’Hara, R.B., Solymos, P., Stevens, M.H.H., Szoecs, E., Wagner, H., Barbour, M., Bedward, M., Bolker, B., Borcard, D., Borman, T., Carvalho, G., Chirico, M., De Caceres, M., Durand, S., Evangelista, H.B.A., Fitzjohn, R., Friendly, M., Furneaux, B., Hannigan, G., Hill, M.O., Lahti, L., Martino, C., Mcglinn, D., Ouellette, M.H., Ribeiro Cunha, E., Smith, T., Stier, A., Ter Braak, C.J.F., Weedon, J., 2024. Vegan: Community Ecology Package Version 2.7-0. .

[46] Onyango, L.A., Ngonga, F.A., Karanja, E.N., Kuja, J.O., Boga, H.I., Cowan, D.A., Mwangi, K.W., Maghenda, M.W., Marinho Lebre, P.B.N., Kambura, A.K., 2023. The soil microbiomes of forest ecosystems in Kenya: their diversity and environmental drivers. Scientific Reports13, 7156.

[47] Palácios, R., Castagna, D., Barbosa, L., Souza, A.P., Imbiriba, B., Zolin, C.A., Nassarden, D., Duarte, L., Morais, F.G., Franco, M.A., Cirino, G., Kuhn, P., Sodré, G., Curado, L., Basso, J., Roberto de Paulo, S., Rodrigues, T., 2024. ENSO effects on the relationship between aerosols and evapotranspiration in the south of the Amazon biome. Environmental Research250, 118516.

[48] Pan, Y.Q., Kang, P., Qu, X., Zhang, H.X., Li, X.R., 2024. Response of the soil bacterial community to seasonal variations and land reclamation in a desert grassland. Ecological Indicators165, 112227.

[49] Pardo-Esté, C., Leiva, S.G., Remonsellez, F., Castro-Nallar, E., Castro-Severyn, J., Saavedra, C.P., 2023. Exploring the influence of small-scale geographical and seasonal variations over the microbial diversity in a poly-extreme Athalosaline wetland. Current Microbiology80, 297.

[50] Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., Glöckner, F.O., 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research41, D590–D596.

[51] Reyes-Ardila, W.L., Vélez-Martínez, G.A., Duque-Zapata, J.D., Rugeles-Silva, P.A., Muñoz Flórez, J.E., López-Álvarez, D., 2024. Exploring soil bacterial and fungal communities in colombian terrestrial ecosystems modulated by altitude-influenced factors. PLoS One19, e0312842.

[52] Sánchez-Galindo, L.M., Sandmann, D., Marian, F., Krashevska, V., Maraun, M., Scheu, S., 2021. Leaf litter identity rather than diversity shapes microbial functions and microarthropod abundance in tropical montane rainforests. Ecology and Evolution11, 2360–2374.

[53] Shigyo, N., Umeki, K., Hirao, T., 2019. Seasonal dynamics of soil fungal and bacterial communities in cool-temperate montane forests. Frontiers in Microbiology10, 1944.

[54] Solanki, A.C., Gurjar, N.S., Sharma, S., Wang, Z., Kumar, A., Solanki, M.K., Kumar Divvela, P., Yadav, K., Kashyap, B.K., 2024. Decoding seasonal changes: soil parameters and microbial communities in tropical dry deciduous forests. Frontiers in Microbiology15, 1258934.

[55] Sun, F., Fan, L.N., Deng, G.Y., Kuzyakov, Y., Zhang, Y., Wang, J.C., Li, Y.W., Wang, F.M., Li, Z.A., Tariq, A., Sardans, J., Penuelas, J., Wang, M., Peng, C.L., 2024. Responses of tropical forest soil organic matter pools to shifts in precipitation patterns. Soil Biology and Biochemistry197, 109530.

[56] Uroz, S., Buée, M., Deveau, A., Mieszkin, S., Martin, F., 2016. Ecology of the forest microbiome: highlights of temperate and boreal ecosystems. Soil Biology and Biochemistry103, 471–488.

[57] Vélez-Martínez, G.A., Reyes-Ardila, W.L., Duque-Zapata, J.D., Rugeles-Silva, P.A., Muñoz Flórez, J.E., López-Álvarez, D., 2023. Soil bacteria and fungi communities are shaped by elevation influences in Colombian forest and páramo natural ecosystems. International Microbiology27, 377–391.

[58] Voříšková, J., Brabcová, V., Cajthaml, T., Baldrian, P., 2014. Seasonal dynamics of fungal communities in a temperate oak forest soil. New Phytologist201, 269–278.

[59] Wei, Y.Q., Quan, F., Lan, G.Y., Wu, Z.X., Yang, C., 2022. Space rather than seasonal changes explained more of the spatiotemporal variation of tropical soil microbial communities. Microbiology Spectrum10, e0184622.

[60] Wickham, H., 2016. ggplot2: Elegant Graphics for Data Analysis. Cham: Springer.

[61] Wood, D.E., Lu, J., Langmead, B., 2019. Improved metagenomic analysis with Kraken 2. Genome Biology20, 257.

[62] Wright, I.J., Dong, N., Maire, V., Prentice, I.C., Westoby, M., Díaz, S., Gallagher, R.V., Jacobs, B.F., Kooyman, R., Law, E.A., Leishman, M.R., Niinemets, Ü., Reich, P.B., Sack, L., Villar, R., Wang, H., Wilf, P., 2017. Global climatic drivers of leaf size. Science357, 917–921.

[63] Xu, A.X., Li, L.L., Xie, J.H., Zhang, R.Z., Luo, Z.Z., Cai, L.Q., Liu, C., Wang, L.L., Anwar, S., Jiang, Y.J., 2022a. Bacterial diversity and potential functions in response to long-term nitrogen fertilizer on the semiarid loess plateau. Microorganisms10, 1579.

[64] Xu, B., Wang, J.N., Wu, N., Wu, Y., Shi, F.S., 2018. Seasonal and interannual dynamics of soil microbial biomass and available nitrogen in an alpine meadow in the eastern part of Qinghai–Tibet Plateau, China. Biogeosciences15, 567–579.

[65] Xu, T.L., Shen, Y.W., Ding, Z.J., Zhu, B., 2023. Seasonal dynamics of microbial communities in rhizosphere and bulk soils of two temperate forests. Rhizosphere25, 100673.

[66] Xu, Y.Z., Liu, K., Yao, S.H., Zhang, Y.L., Zhang, X.D., He, H.B., Feng, W.T., Ndzana, G.M., Chenu, C., Olk, D.C., Mao, J.D., Zhang, B., 2022b. Formation efficiency of soil organic matter from plant litter is governed by clay mineral type more than plant litter quality. Geoderma412, 115727.

[67] Zhang, J.J., Liang, M.X., Tong, S., Qiao, X.T., Li, B.H., Yang, Q., Chen, T., Hu, P., Yu, S.X., 2023a. Response of leaf functional traits to soil nutrients in the wet and dry seasons in a subtropical forest on an island. Frontiers in Plant Science14, 1236607.

[68] Zhang, K.P., Delgado-Baquerizo, M., Zhu, Y.G., Chu, H.Y., 2020. Space is more important than season when shaping soil microbial communities at a large spatial scale. MSystems5( 3), e00783-19.

[69] Zhang, X.Y., Zeng, H., Wang, W., 2018. Two contrasting seasonal patterns in microbial nitrogen immobilization from temperate ecosystems. Ecological Indicators93, 164–172.

[70] Zhang, Z.Y., Qiang, F.F., Liu, G.Q., Liu, C.H., Ai, N., 2023b. Distribution characteristics of soil microbial communities and their responses to environmental factors in the sea buckthorn forest in the water-wind erosion crisscross region. Frontiers in Microbiology13, 1098952.

[71] Zhu, B.L., Karwautz, C., Andrei, S., Klingl, A., Pernthaler, J., Lueders, T., 2022. A novel Methylomirabilota methanotroph potentially couples methane oxidation to iodate reduction. mLife1, 323–328.

[72] Zhuang, J.J., Tian, Y., 2023. Effects of precipitation on forestry soil microorganisms. Polish Journal of Environmental Studies32, 5923–5931.

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The Author(s) 2025. This article is published with open access at link.springer.com and journal.hep.com.cn