Gravesoil fungi are more sensitive than bacteria in response to precipitation

Abstract

● Fungi are more sensitive to precipitation than bacteria.

● The susceptibility of abundant and rare bacteria to precipitation has no difference.

● Abundant taxa of fungi are more vulnerable to precipitation than rare ones.

Precipitation scenario alteration leads to grievous ecological consequences in ecosystems, especially on the Qinghai-Tibet Plateau. Bacterial and fungal community and their abundant and rare taxa in soil ecosystems may respond differently to the changed precipitation. Therefore, more attention needs to be paid to the sensitivity of bacteria and fungi and their abundant and rare taxa to precipitation shifts. The responses of bacterial and fungal populations and their abundant and rare taxa concerning diversity, assembly, and interactions to manipulative changes of precipitation were explored via imitating no precipitation, little precipitation, and medium precipitation using 16S rRNA gene and ITS amplicon sequencing. The results indicated that the change rate of fungal Simpson diversity with precipitation was higher than that of bacteria. The slope of the modified stochasticity ratio (MST) value of fungi to precipitation was steeper than that of bacteria. The Simpson diversity and the MST value of abundant and rare taxa within bacteria had no difference with precipitation. In contrast, those of abundant taxa within fungi varied more than rare ones with precipitation. By unveiling the differential responses of microbial populations with discrepant characteristics, this study allowed us to understand the different microbial communities responding to rainfall on the Qinghai-Tibet Plateau.

Graphical abstract

Keywords

Qinghai-Tibet Plateau / sensitivity / precipitation / assembly / co-occurrence networks

References

[1] Bahram, M., Kohout, P., Anslan, S., Harend, H., Abarenkov, K., Tedersoo, L., 2016. Stochastic distribution of small soil eukaryotes resulting from high dispersal and drift in a local environment. The ISME Journal10, 885–896.

[2] Bastian, M., Heymann, S., Jacomy, M., 2009. Gephi: An open source software for exploring and manipulating networks. Proceedings of the International AAAI Conference on Web and Social Media3, 361–362.

[3] Campbell, B.J., Yu, L.Y., Heidelberg, J.F., Kirchman, D.L., 2011. Activity of abundant and rare bacteria in a coastal ocean. Proceedings of the National Academy of Sciences of the United States of America108, 12776–12781.

[4] Carter, D.O., Yellowlees, D., Tibbett, M., 2006. Cadaver decomposition in terrestrial ecosystems. Naturwissenschaften94, 12–24.

[5] Carter, D.O., Yellowlees, D., Tibbett, M., 2010. Moisture can be the dominant environmental parameter governing cadaver decomposition in soil. Forensic Science International200, 60–66.

[6] Chen, J., Wang, P., Wang, C., Wang, X., Miao, L., Liu, S., Yuan, Q., Sun, S., 2020. Fungal community demonstrates stronger dispersal limitation and less network connectivity than bacterial community in sediments along a large river. Environmental Microbiology22, 832–849.

[7] Chen, Q.L., Hu, H.W., Yan, Z.Z., Li, C.Y., Nguyen, B.A.T., Sun, A.Q., Zhu, Y.G., He, J.Z., 2021. Deterministic selection dominates microbial community assembly in termite mounds. Soil Biology & Biochemistry152, 108073.

[8] Cleland, E.E., Collins, S.L., Dickson, T.L., Farrer, E.C., Gross, K.L., Gherardi, L.A., Hallett, L.M., Hobbs, R.J., Hsu, J.S., Turnbull, L., Suding, K.N., 2013. Sensitivity of grassland plant community composition to spatial vs. temporal variation in precipitation. Ecology94, 1687–1696.

[9] de Vries, F.T., Shade, A., 2013. Controls on soil microbial community stability under climate change. Frontiers in Microbiology 4, 265.

[10] Feng, W., Zhang, Y., Lai, Z., Qin, S., Yan, R., Sun, Y., She, W., 2021. Soil bacterial and eukaryotic co-occurrence networks across a desert climate gradient in northern China. Land Degradation & Development32, 1938–1950.

[11] Fierer, N., Schimel, J.P., Holden, P.A., 2003. Influence of drying-rewetting frequency on soil bacterial community structure. Microbial Ecology45, 63–71.

[12] Freilich, S., Kreimer, A., Meilijson, I., Gophna, U., Sharan, R., Ruppin, E., 2010. The large-scale organization of the bacterial network of ecological co-occurrence interactions. Nucleic Acids Research38, 3857–3868.

[13] Fuhrman, J.A., 2009. Microbial community structure and its functional implications. Nature459, 193–199.

[14] Gilbert, J.A., Neufeld, J.D., 2014. Life in a world without microbes. PLoS Biology12, e1002020.

[15] Hawkes, C.V., Kivlin, S.N., Rocca, J.D., Huguet, V., Thomsen, M.A., Suttle, K.B., 2011. Fungal community responses to precipitation. Global Change Biology17, 1637–1645.

[16] He, D., Guo, Z., Shen, W., Ren, L., Sun, D., Yao, Q., Zhu, H., 2023. Fungal communities are more sensitive to the simulated environmental changes than bacterial communities in a subtropical forest: the single and interactive effects of nitrogen addition and precipitation seasonality change. Microbial Ecology86, 521–535.

[17] He, D., Shen, W., Eberwein, J., Zhao, Q., Ren, L., Wu, Q.L., 2017. Diversity and co-occurrence network of soil fungi are more responsive than those of bacteria to shifts in precipitation seasonality in a subtropical forest. Soil Biology & Biochemistry115, 499–510.

[18] Held, I.M., Soden, B.J., 2000. Water vapor feedback and global warming. Annual Review of Energy and the Environment25, 441–475.

[19] Izabel-Shen, D., Höger, A.L., Jürgens, K., 2021. Abundance-occupancy relationships along taxonomic ranks reveal a consistency of niche differentiation in marine bacterioplankton with distinct lifestyles. Frontiers in Microbiology12, 690712.

[20] Ji, M., Kong, W., Stegen, J., Yue, L., Wang, F., Dong, X., Cowan, D.A., Ferrari, B.C., 2020. Distinct assembly mechanisms underlie similar biogeographical patterns of rare and abundant bacteria in Tibetan Plateau grassland soils. Environmental Microbiology22, 2261–2272.

[21] Jiao, S., Chen, W., Wang, J., Du, N., Li, Q., Wei, G., 2018. Soil microbiomes with distinct assemblies through vertical soil profiles drive the cycling of multiple nutrients in reforested ecosystems. Microbiome6, 146.

[22] Jiao, S., Lu, Y., 2020. Soil pH and temperature regulate assembly processes of abundant and rare bacterial communities in agricultural ecosystems. Environmental Microbiology22, 1052–1065.

[23] Jiao, S., Yang, Y., Xu, Y., Zhang, J., Lu, Y., 2020. Balance between community assembly processes mediates species coexistence in agricultural soil microbiomes across eastern China. The ISME Journal14, 202–216.

[24] Kaisermann, A., Maron, P.A., Beaumelle, L., Lata, J.C., 2015. Fungal communities are more sensitive indicators to non-extreme soil moisture variations than bacterial communities. Applied Soil Ecology86, 158–164.

[25] Kivlin, S.N., Winston, G.C., Goulden, M.L., Treseder, K.K., 2014. Environmental filtering affects soil fungal community composition more than dispersal limitation at regional scales. Fungal Ecology12, 14–25.

[26] Kooijman, A.M., Bloem, J., van Dalen, B.R., Kalbitz, K., 2016. Differences in activity and N demand between bacteria and fungi in a microcosm incubation experiment with selective inhibition. Applied Soil Ecology99, 29–39.

[27] Koutnikova, H., Genser, B., Monteiro-Sepulveda, M., Faurie, J.M., Rizkalla, S., Schrezenmeir, J., Clément, K., 2019. Impact of bacterial probiotics on obesity, diabetes and non-alcoholic fatty liver disease related variables: a systematic review and meta-analysis of randomised controlled trials. BMJ Open9, e017995.

[28] Li, C., Jin, L., Zhang, C., Li, S., Zhou, T., Hua, Z., Wang, L., Ji, S., Wang, Y., Gan, Y., Liu, J., 2023a. Destabilized microbial networks with distinct performances of abundant and rare biospheres in maintaining networks under increasing salinity stress. iMeta2, e79.

[29] Li, J., Benti, G., Wang, D., Yang, Z., Xiao, R., 2022. Effect of alteration in precipitation amount on soil microbial community in a semi-arid grassland. Frontiers in Microbiology13, 842446.

[30] Li, L., Nijs, I., De Boeck, H., Vinduskova, O., Reynaert, S., Donnelly, C., Zi, L., Verbruggen, E., 2023b. Longer dry and wet spells alter the stochasticity of microbial community assembly in grassland soils. Soil Biology & Biochemistry178, 108969.

[31] Liu, S., Yu, H., Yu, Y., Huang, J., Zhou, Z., Zeng, J., Chen, P., Xiao, F., He, Z., Yan, Q., 2022. Ecological stability of microbial communities in Lake Donghu regulated by keystone taxa. Ecological Indicators136, 108695.

[32] Luo, Y., Gao, W., Gao, Y., Tang, S., Huang, Q., Tan, X., Chen, J., Huang, T., 2008. Mitochondrial genome analysis of Ochotona curzoniae and implication of cytochrome c oxidase in hypoxic adaptation. Mitochondrion8, 352–357.

[33] Lynch, M.D.J., Neufeld, J.D., 2015. Ecology and exploration of the rare biosphere. Nature Reviews Microbiology13, 217–229.

[34] MacArthur, R., 1955. Fluctuations of animal populations and a measure of community stability. Ecology36, 533–536.

[35] Magoč T., Salzberg, S.L., 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics (Oxford, England)27, 2957–2963.

[36] Markham, K., 2015. Tutorials for the dplyr package in R. available at the GitHub website

[37] McHugh, T.A., Schwartz, E., 2016. A watering manipulation in a semiarid grassland induced changes in fungal but not bacterial community composition. Pedobiologia59, 121–127.

[38] Mougi, A., Kondoh, M., 2012. Diversity of interaction types and ecological community stability. Science337, 349–351.

[39] Nemergut, D.R., Schmidt, S.K., Fukami, T., O’Neill, S.P., Bilinski, T.M., Stanish, L.F., Knelman, J.E., Darcy, J.L., Lynch, R.C., Wickey, P., Ferrenberg, S., 2013. Patterns and processes of microbial community assembly. Microbiology and Molecular Biology Reviews77, 342–356.

[40] Neutel, A.M., Heesterbeek, J.A.P., de Ruiter, P.C., 2002. Stability in real food webs: Weak links in long loops. Science296, 1120–1123.

[41] Ning, D., Deng, Y., Tiedje, J.M., Zhou, J., 2019. A general framework for quantitatively assessing ecological stochasticity. Proceedings of the National Academy of Sciences of the United States of America116, 16892–16898.

[42] Ning, D., Yuan, M., Wu, L., Zhang, Y., Guo, X., Zhou, X., Yang, Y., Arkin, A.P., Firestone, M.K., Zhou, J., 2020. A quantitative framework reveals ecological drivers of grassland microbial community assembly in response to warming. Nature Communications11, 4717.

[43] Parton, W.J., Schimel, D.S., Cole, C.V., Ojima, D.S., 1987. Analysis of factors controlling soil organic matter levels in great plais grasslands. Soil Science Society of America Journal51, 1173–1179.

[44] Pedrós-Alió C., 2012. The rare bacterial biosphere. Annual Review of Marine Science4, 449–466.

[45] Ren, Z., Gao, H., 2022. Abundant and rare soil fungi exhibit distinct succession patterns in the forefield of Dongkemadi glacier on the central Qinghai-Tibet Plateau. Science of the Total Environment828, 154563.

[46] Ritz, K., McNicol, W., Nunan, N., Grayston, S., Millard, P., Atkinson, D., Gollotte, A., Habeshaw, D., Boag, B., Clegg, C.D., Griffiths, B.S., Wheatley, R.E., Glover, L.A., McCaig, A.E., Prosser, J.I., 2004. Spatial structure in soil chemical and microbiological properties in an upland grassland. FEMS Microbiology Ecology49, 191–205.

[47] Schimel, J.P., Gulledge, J.M., Clein-Curley, J.S., Lindstrom, J.E., Braddock, J.F., 1999. Moisture effects on microbial activity and community structure in decomposing birch litter in the Alaskan taiga. Soil Biology & Biochemistry31, 831–838.

[48] Siciliano, S.D., Palmer, A.S., Winsley, T., Lamb, E., Bissett, A., Brown, M.V., van Dorst, J., Ji, M., Ferrari, B.C., Grogan, P., Chu, H., Snape, I., 2014. Soil fertility is associated with fungal and bacterial richness, whereas pH is associated with community composition in polar soil microbial communities. Soil Biology & Biochemistry78, 10–20.

[49] Singh, D., Gupta, R.D., Jain, S.K., 2015. Assessment of impact of climate change on water resources in a hilly river basin. Arabian Journal of Geosciences8, 10625–10646.

[50] Sloan, W.T., Lunn, M., Woodcock, S., Head, I.M., Nee, S., Curtis, T.P., 2006. Quantifying the roles of immigration and chance in shaping prokaryote community structure. Environmental Microbiology8, 732–740.

[51] Smith, A.T., Badingqiuying, Wilson, M.C., Hogan, B.W., 2019. Functional-trait ecology of the plateau pika Ochotona curzoniae in the Qinghai-Tibetan Plateau ecosystem. Integrative Zoology14, 87–103.

[52] Stegen, J.C., Lin, X., Fredrickson, J.K., Chen, X., Kennedy, D.W., Murray, C.J., Rockhold, M.L., Konopka, A., 2013. Quantifying community assembly processes and identifying features that impose them. The ISME Journal7, 2069–2079.

[53] Stegen, J.C., Lin, X., Fredrickson, J.K., Konopka, A.E., 2015. Estimating and mapping ecological processes influencing microbial community assembly. Frontiers in Microbiology 6, 370.

[54] Stegen, J.C., Lin, X., Konopka, A.E., Fredrickson, J.K., 2012. Stochastic and deterministic assembly processes in subsurface microbial communities. ISME Journal6, 1653–1664.

[55] Steinberger, Y., Zelles, L., Bai, Q.Y., von Lutzow, M., Munch, J.C., 1999. Phospholipid fatty acid profiles as indicators for the microbial community structure in soils along a climatic transect in the Judean Desert. Biology and Fertility of Soils28, 292–300.

[56] Su, W., Han, Q., Yang, J., Yu, Q., Wang, S., Wang, X., Qu, J., Li, H., 2022. Heavy rainfall accelerates the temporal turnover but decreases the deterministic processes of buried gravesoil bacterial communities. Science of the Total Environment836, 155732.

[57] Wang, X. and Smith, A.T., 1988. On the natural winter mortality of the plateau pika (Ochotona curzoniae). Acta Theriologica Sinica 8, 152–156.

[58] Wang, Z., Qi, W., Zhao, L., 2022. Analysis of precipitation characteristics during main flood season in Haibei region drom 1976 to 2017. Qinghai Prataculture31, 64–70.

[59] Wu, J., Barahona, M., Tan, Y.J., Deng, H.Z., 2010. Natural connectivity of complex networks. Chinese Physics Letters27, 078902.

[60] Xu, Z.X., Gong, T.L., Li, J.Y., 2008. Decadal trend of climate in the Tibetan Plateau - regional temperature and precipitation. Hydrological Processes22, 3056–3065.

[61] Yachi, S., Loreau, M., 1999. Biodiversity and ecosystem productivity in a fluctuating environment: The insurance hypothesis. Proceedings of the National Academy of Sciences of the United States of America96, 1463–1468.

[62] Yao, T.D., Liu, X.D., Wang, N.L., Shi, Y.F., 2000. Amplitude of climatic changes in Qinghai-Tibetan Plateau. Chinese Science Bulletin45, 1236–1243.

[63] Zhang, J., 2016. Spaa: Species Association Analysis. R package version 0.2.2. 2016. available at the website CRAN.R-project.org

[64] Zhang, J., Liu, S., Liu, C., Wang, H., Luan, J., Liu, X., Guo, X., Niu, B., 2021. Soil bacterial and fungal richness and network exhibit different responses to long-term throughfall reduction in a warm-temperate oak forest. Forests12, 165.

[65] Zhao, Z., Ma, Y., Feng, T., Kong, X., Wang, Z., Zheng, W., Zhai, B., 2022. Assembly processes of abundant and rare microbial communities in orchard soil under a cover crop at different periods. Geoderma406, 115543.

[66] Zhong, Y., Liu, J., Jia, X., Tang, Z., Shangguan, Z., Wang, R., Yan, W., 2022. Environmental stress-discriminatory taxa are associated with high C and N cycling functional potentials in dryland grasslands. Science of the Total Environment817, 152991.

[67] Zou, D., Zhao, L., Sheng, Y., Chen, J., Hu, G., Wu, T., Wu, J., Xie, C., Wu, X., Pang, Q., Wang, W., Du, E., Li, W., Liu, G., Li, J., Qin, Y., Qiao, Y., Wang, Z., Shi, J., Cheng, G., 2017. A new map of permafrost distribution on the Tibetan Plateau. Cryosphere11, 2527–2542.

RIGHTS & PERMISSIONS

Higher Education Press