Nitrogen-based fertilizers differentially affect protist community composition in paddy field soils
Seda Ozer Bodur, Solomon Oloruntoba Samuel, Kazuki Suzuki, Naoki Harada, Rasit Asiloglu
Nitrogen-based fertilizers differentially affect protist community composition in paddy field soils
● Nitrogen fertilizers’ effects on protists in three paddy field soils were analyzed.
● Different nitrogen fertilizers had distinctive effects on the protist communities.
● The effect of nitrogen fertilizers on protist communities slightly depended on the soil types.
● Predatory protists were the main groups that were affected by nitrogen fertilizers.
Protists are one of the most diverse and dominant microbial groups and they play critical roles in the soil ecosystem. Although nitrogen fertilizers have a profound impact on protist communities, still less is known about how different nitrogen fertilizer types affect protist community composition in different soil types. Here we investigated the effects of six inorganic nitrogen fertilizers (urea, ammonium nitrate, ammonium sulfate, potassium nitrate, ammonium chloride, and diammonium hydrogen phosphate) and an organic fertilizer (a mixture of rice husk and cow manure) on protist community composition in three paddy field soils using a high-throughput sequencing method. The effect of the fertilizers on the functional groups of protists, namely consumers (predators and decomposers), photoautotrophs, and parasites (plant pathogens and animal parasites) was also analyzed. The results showed that nitrogen fertilizers had distinctive effects on the beta diversity of the protists, while we also observed that the same fertilizer had slightly different effects depending on the soil type. Amoebozoa and Rhizaria were the most affected protist taxonomical groups, while predatory protists were the main functional groups that were affected by nitrogen fertilizers. Random forest analysis showed that most of the fertilizer-affected protists were predators, among which Cercozoa was the most affected taxa. In conclusion, our results provide important insights into the impact of nitrogen fertilizers on soil protist communities.
nitrogen fertilizer / bottom-up / paddy field / predatory protist / soil protist community
[1] |
Amaral-Zettler, L.A., McCliment, E.A., Ducklow, H.W., Huse, S.M., 2009. A method for studying protistan diversity using massively parallel sequencing of v9 hypervariable regions of small-subunit ribosomal RNA genes. PLoS One4, e6372.
CrossRef
Google scholar
|
[2] |
Archer, E., 2013. rfPermute: Estimate Permutation p-Values for Random Forest Importance Metrics. R package version. 1.5.2
|
[3] |
Asiloglu, R., 2022. Biochar–microbe interaction: more protist research is needed. Biochar4, 72.
CrossRef
Google scholar
|
[4] |
Asiloglu, R., Honjo, H., Saka, N., Asakawa, S., Murase, J., 2015. Community structure of microeukaryotes in a rice rhizosphere revealed by DNA-based PCR-DGGE. Soil Science and Plant Nutrition61, 761–768.
CrossRef
Google scholar
|
[5] |
Asiloglu, R., Kenya, K., Samuel, S.O., Sevilir, B., Murase, J., Suzuki, K., Harada, N., 2021a. Top-down effects of protists are greater than bottom-up effects of fertilisers on the formation of bacterial communities in a paddy field soil. Soil Biology & Biochemistry156, 108186.
CrossRef
Google scholar
|
[6] |
Asiloglu, R., Murase, J., 2016. Active community structure of microeukaryotes in a rice (Oryza sativa L. ) rhizosphere revealed by RNA-based PCR-DGGE. Soil Science and Plant Nutrition62, 440–446.
CrossRef
Google scholar
|
[7] |
Asiloglu, R., Samuel, S.O., Sevilir, B., Akca, M.O., Acar Bozkurt, P., Suzuki, K., Murase, J., Turgay, O.C., Harada, N., 2021b. Biochar affects taxonomic and functional community composition of protists. Biology and Fertility of Soils57, 15–29.
CrossRef
Google scholar
|
[8] |
Asiloglu, R., Shiroishi, K., Suzuki, K., Turgay, O.C., Harada, N., 2021c. Soil properties have more significant effects on the community composition of protists than the rhizosphere effect of rice plants in alkaline paddy field soils. Soil Biology & Biochemistry161, 108397.
CrossRef
Google scholar
|
[9] |
Asiloglu, R., Shiroishi, K., Suzuki, K., Turgay, O.C., Murase, J., Harada, N., 2020. Protist-enhanced survival of a plant growth promoting rhizobacteria, Azospirillum sp. B510, and the growth of rice (Oryza sativa L.) plants. Applied Soil Ecology 154, 103599
|
[10] |
Breiman, L., 2001. Random forests. Machine Learning45, 5–32.
CrossRef
Google scholar
|
[11] |
Burki, F., Roger, A.J., Brown, M.W., Simpson, A.G.B., 2020. The new tree of eukaryotes. Trends in Ecology & Evolution35, 43–55.
CrossRef
Google scholar
|
[12] |
Callahan, B.J., McMurdie, P.J., Rosen, M.J., Han, A.W., Johnson, A.J.A., Holmes, S.P., 2016. DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods13, 581–583.
CrossRef
Google scholar
|
[13] |
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 Journal6, 1621–1624.
CrossRef
Google scholar
|
[14] |
Caron, D.A., Worden, A.Z., Countway, P.D., Demir, E., Heidelberg, K.B., 2009. Protists are microbes too: a perspective. ISME Journal3, 4–12.
CrossRef
Google scholar
|
[15] |
Fiore-Donno, A.M., Human, Z.R., Štursová, M., Mundra, S., Morgado, L., Kauserud, H., Baldrian, P., Bonkowski, M., 2022. Soil compartments (bulk soil, litter, root and rhizosphere) as main drivers of soil protistan communities distribution in forests with different nitrogen deposition. Soil Biology & Biochemistry168, 108628.
CrossRef
Google scholar
|
[16] |
Fujino, M., Suzuki, K., Harada, N., Asiloglu, R., 2023. Protists modulate active bacterial community composition in paddy field soils. Biology and Fertility of Soils59, 709–721.
CrossRef
Google scholar
|
[17] |
Gao, Z., Karlsson, I., Geisen, S., Kowalchuk, G., Jousset, A., 2019. Protists: Puppet masters of the rhizosphere microbiome. Trends in Plant Science24, 165–176.
CrossRef
Google scholar
|
[18] |
Geisen, S., Koller, R., Hünninghaus, M., Dumack, K., Urich, T., Bonkowski, M., 2016. The soil food web revisited: Diverse and widespread mycophagous soil protists. Soil Biology & Biochemistry94, 10–18.
CrossRef
Google scholar
|
[19] |
Geisen, S., Mitchell, E.A.D., Adl, S., Bonkowski, M., Dunthorn, M., Ekelund, F., Fernández, L.D., Jousset, A., Krashevska, V., Singer, D., Spiegel, F.W., Walochnik, J., Lara, E., 2018. Soil protists: A fertile frontier in soil biology research. FEMS Microbiology Reviews42, 293–323.
CrossRef
Google scholar
|
[20] |
Guillou, L., Bachar, D., Audic, S., Bass, D., Berney, C., Bittner, L., Boutte, C., Burgaud, G., de Vargas, C., Decelle, J., del Campo, J., Dolan, J.R., Dunthorn, M., Edvardsen, B., Holzmann, M., Kooistra, W.H.C.F., Lara, E., Le Bescot, N., Logares, R., Mahé, F., Massana, R., Montresor, M., Morard, R., Not, F., Pawlowski, J., Probert, I., Sauvadet, A.L., Siano, R., Stoeck, T., Vaulot, D., Zimmermann, P., Christen, R., 2012. The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Research41, D597–D604.
CrossRef
Google scholar
|
[21] |
Guo, S., Tao, C., Jousset, A., Xiong, W., Wang, Z., Shen, Z., Wang, B., Xu, Z., Gao, Z., Liu, S., Li, R., Ruan, Y., Shen, Q., Kowalchuk, G.A., Geisen, S., 2022. Trophic interactions between predatory protists and pathogen-suppressive bacteria impact plant health. ISME Journal16, 1932–1943.
CrossRef
Google scholar
|
[22] |
Guo, S., Xiong, W., Hang, X., Gao, Z., Jiao, Z., Liu, H., Mo, Y., Zhang, N., Kowalchuk, G.A., Li, R., Shen, Q., Geisen, S., 2021. Protists as main indicators and determinants of plant performance. Microbiome9, 64.
CrossRef
Google scholar
|
[23] |
Guo, S., Xiong, W., Xu, H., Hang, X., Liu, H., Xun, W., Li, R., Shen, Q., 2018. Continuous application of different fertilizers induces distinct bulk and rhizosphere soil protist communities. European Journal of Soil Biology88, 8–14.
CrossRef
Google scholar
|
[24] |
Huang, X., Wang, J., Dumack, K., Liu, W., Zhang, Q., He, Y., Di, H., Bonkowski, M., Xu, J., Li, Y., 2021. Protists modulate fungal community assembly in paddy soils across climatic zones at the continental scale. Soil Biology & Biochemistry160, 108358.
CrossRef
Google scholar
|
[25] |
Hultberg, M., Alsberg, T., Khalil, S., Alsanius, B., 2010. Suppression of disease in tomato infected by Pythium ultimum with a biosurfactant produced by Pseudomonas koreensis. BioControl55, 435–444.
CrossRef
Google scholar
|
[26] |
Jassey, V.E.J., Signarbieux, C., Hättenschwiler, S., Bragazza, L., Buttler, A., Delarue, F., Fournier, B., Gilbert, D., Laggoun-Défarge, F., Lara, E., Mills, R.T.E., Mitchell, E.A.D., Payne, R.J., Robroek, B.J.M., 2015. An unexpected role for mixotrophs in the response of peatland carbon cycling to climate warming. Scientific Reports5, 16931.
CrossRef
Google scholar
|
[27] |
Jassey, V.E.J., Walcker, R., Kardol, P., Geisen, S., Heger, T., Lamentowicz, M., Hamard, S., Lara, E., 2022. Contribution of soil algae to the global carbon cycle. New Phytologist234, 64–76.
CrossRef
Google scholar
|
[28] |
Kirk, G., 2004. The biogeochemistry of submerged soils. Wiley, Chichester
|
[29] |
Kononov, A., Hishida, M., Suzuki, K., Harada, N., 2022. Microplastic extraction from agricultural soils using canola oil and unsaturated sodium chloride solution and evaluation by incineration method. Soil Systems6, 54.
CrossRef
Google scholar
|
[30] |
Krashevska, V., Sandmann, D., Maraun, M., Scheu, S., 2014. Moderate changes in nutrient input alter tropical microbial and protist communities and belowground linkages. ISME Journal8, 1126–1134.
CrossRef
Google scholar
|
[31] |
Lentendu, G., Wubet, T., Chatzinotas, A., Wilhelm, C., Buscot, F., Schlegel, M., 2014. Effects of long-term differential fertilization on eukaryotic microbial communities in an arable soil: a multiple barcoding approach. Molecular Ecology23, 3341–3355.
CrossRef
Google scholar
|
[32] |
Li, F., Sun, A., Jiao, X., Bi, L., Zheng, Y., He, J.Z., Hu, H.W., 2021. Specific protistan consumers and parasites are responsive to inorganic fertilization in rhizosphere and bulk soils. Journal of Soils and Sediments21, 3801–3812.
CrossRef
Google scholar
|
[33] |
Murase, J., Asiloglu, R., 2023. Protists: the hidden ecosystem players in a wetland rice field soil. Biology and Fertility of Soils. https://doi.org/10.1007/s00374-023-01705-9
|
[34] |
Murase, J., Hida, A., Ogawa, K., Nonoyama, T., Yoshikawa, N., Imai, K., 2015. Impact of long-term fertilizer treatment on the microeukaryotic community structure of a rice field soil. Soil Biology & Biochemistry80, 237–243.
CrossRef
Google scholar
|
[35] |
Nakamura, A., Tun, C.C., Asakawa, S., Kimura, M., 2003. Microbial community responsible for the decomposition of rice straw in a paddy field: Estimation by phospholipid fatty acid analysis. Biology and Fertility of Soils38, 288–295.
CrossRef
Google scholar
|
[36] |
Picot, E., Hale, C.C., Hilton, S., Teakle, G., Schäfer, H., Huang, Y.J., Perryman, S., West, J.S., Bending, G.D., 2021. Contrasting responses of rhizosphere bacterial, fungal, protist, and nematode communities to nitrogen fertilization and crop genotype in field grown oilseed rape (Brassica napus). Frontiers in Sustainable Food Systems5, 613269.
CrossRef
Google scholar
|
[37] |
Roguet, A., Eren, A.M., Newton, R.J., McLellan, S.L., 2018. Fecal source identification using random forest. Microbiome6, 185.
CrossRef
Google scholar
|
[38] |
Schnurer, J., Clarholm, M., Rosswall, T., 1986. Fungi, bacteria and protozoa in soil from four arable cropping systems. Biology and Fertility of Soils2, 119–126.
|
[39] |
Sibbald SJ, Archibald JM. 2017. More protist genomes needed. Nature Ecology & Evolution1, 0145.
|
[40] |
Sun, A., Jiao, X.Y., Chen, Q., Trivedi, P., Li, Z., Li, F., Zheng, Y., Lin, Y., Hu, H.W., He, J.Z., 2021. Fertilization alters protistan consumers and parasites in crop-associated microbiomes. Environmental Microbiology23, 2169–2183.
CrossRef
Google scholar
|
[41] |
Van Buyten, E., Höfte, M., 2013. Pythium species from rice roots differ in virulence, host colonization and nutritional profile. BMC Plant Biology13, 203.
CrossRef
Google scholar
|
[42] |
Wei, L., Ge, T., Zhu, Z., Ye, R., Peñuelas, J., Li, Y., Lynn, T.M., Jones, D.L., Wu, J., Kuzyakov, Y., 2022. Paddy soils have a much higher microbial biomass content than upland soils: A review of the origin, mechanisms, and drivers. Agriculture, Ecosystems & Environment326, 107798.
CrossRef
Google scholar
|
[43] |
Xiong, W., Jousset, A., Guo, S., Karlsson, I., Zhao, Q., Wu, H., Kowalchuk, G.A., Shen, Q., Li, R., Geisen, S., 2018. Soil protist communities form a dynamic hub in the soil microbiome. ISME Journal12, 634–638.
CrossRef
Google scholar
|
[44] |
Zhang, S., Zhang, H., Liu, H., Wang, H., Xiu, W., Li, G., Zhang, G., Zhou, Z., Jiang, N., Zhang, H., Zhao, J., Yang, D., 2022. Fertilization drives distinct biotic and abiotic factors in regulating functional groups of protists in a 5-year fertilization system. Frontiers in Microbiology13, 1036362.
CrossRef
Google scholar
|
[45] |
Zhao, Z.B., He, J.Z., Geisen, S., Han, L.L., Wang, J.T., Shen, J.P., Wei, W.X., Fang, Y.T., Li, P.P., Zhang, L.M., 2019. Protist communities are more sensitive to nitrogen fertilization than other microorganisms in diverse agricultural soils. Microbiome7, 33.
CrossRef
Google scholar
|
[46] |
Zhao, Z.B., He, J.Z., Quan, Z., Wu, C.F., Sheng, R., Zhang, L.M., Geisen, S., 2020. Fertilization changes soil microbiome functioning, especially phagotrophic protists. Soil Biology & Biochemistry148, 107863.
CrossRef
Google scholar
|
/
〈 | 〉 |