Predatory protists play predominant roles in suppressing soil-borne fungal pathogens under organic fertilization regimes
Soil-borne fungal pathogens pose a major threat to global agricultural production and food security. Pathogen-suppressive bacteria and plant beneficial protists are important components of soil microbiomes and essential to plant health and performance, but it remains largely unknown regarding how ag...
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Published in | The Science of the total environment Vol. 863; p. 160986 |
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Main Authors | , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
Netherlands
Elsevier B.V
10.03.2023
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Abstract | Soil-borne fungal pathogens pose a major threat to global agricultural production and food security. Pathogen-suppressive bacteria and plant beneficial protists are important components of soil microbiomes and essential to plant health and performance, but it remains largely unknown regarding how agricultural management practices influence the relative importance of protists and bacteria in plant disease suppression. Here, we characterized soil microbiomes (including fungi, protists, and bacteria) in bulk and sorghum rhizosphere soils with various long-term inorganic and organic fertilization regimes, and linked the changes in fungal plant pathogens with the protistan and bacterial communities. We found that the relative abundances of fungal pathogens were significantly decreased by organic fertilization regimes, and there was a significant difference in the community composition of fungal pathogens between inorganic and organic fertilization regimes. Organic fertilization significantly enhanced predatory protists but reduced the proportions of protistan phototrophs. Co-occurrence network analysis revealed more intensive connections between fungal plant pathogens with protists, especially predatory protists, than with bacterial taxa, which was further supported by stronger associations between the community structure of fungal pathogens and predatory protists. We identified more protist consumer taxa than bacterial taxa as predictors of fungal plant pathogens, and structural equation modelling revealed a more important impact of protist consumers than bacteria on fungal pathogens. Altogether, we provide new evidence that the disease inhibitory effects of long-term organic fertilization regimes could be best explained by the potential predation pressure of protists. Our findings advance the mechanistic understanding of the role of predator-prey interactions in controlling fungal diseases, and have implications for novel biocontrol strategies to mitigate the consequences of fungal infections for plant performance.
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•Long-term organic fertilization regimes significantly reduced the relative abundances of fungal pathogens.•Organic fertilization significantly increased the proportions of predatory protists.•Predatory protists were the best predictors of the patterns of fungal plant pathogens.•The disease suppression of organic fertilization was best explained by the predation pressure of protists.•This study advanced our understanding of the crucial roles of trophic regulations in regulating fungal plant pathogens. |
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AbstractList | Soil-borne fungal pathogens pose a major threat to global agricultural production and food security. Pathogen-suppressive bacteria and plant beneficial protists are important components of soil microbiomes and essential to plant health and performance, but it remains largely unknown regarding how agricultural management practices influence the relative importance of protists and bacteria in plant disease suppression. Here, we characterized soil microbiomes (including fungi, protists, and bacteria) in bulk and sorghum rhizosphere soils with various long-term inorganic and organic fertilization regimes, and linked the changes in fungal plant pathogens with the protistan and bacterial communities. We found that the relative abundances of fungal pathogens were significantly decreased by organic fertilization regimes, and there was a significant difference in the community composition of fungal pathogens between inorganic and organic fertilization regimes. Organic fertilization significantly enhanced predatory protists but reduced the proportions of protistan phototrophs. Co-occurrence network analysis revealed more intensive connections between fungal plant pathogens with protists, especially predatory protists, than with bacterial taxa, which was further supported by stronger associations between the community structure of fungal pathogens and predatory protists. We identified more protist consumer taxa than bacterial taxa as predictors of fungal plant pathogens, and structural equation modelling revealed a more important impact of protist consumers than bacteria on fungal pathogens. Altogether, we provide new evidence that the disease inhibitory effects of long-term organic fertilization regimes could be best explained by the potential predation pressure of protists. Our findings advance the mechanistic understanding of the role of predator-prey interactions in controlling fungal diseases, and have implications for novel biocontrol strategies to mitigate the consequences of fungal infections for plant performance. Soil-borne fungal pathogens pose a major threat to global agricultural production and food security. Pathogen-suppressive bacteria and plant beneficial protists are important components of soil microbiomes and essential to plant health and performance, but it remains largely unknown regarding how agricultural management practices influence the relative importance of protists and bacteria in plant disease suppression. Here, we characterized soil microbiomes (including fungi, protists, and bacteria) in bulk and sorghum rhizosphere soils with various long-term inorganic and organic fertilization regimes, and linked the changes in fungal plant pathogens with the protistan and bacterial communities. We found that the relative abundances of fungal pathogens were significantly decreased by organic fertilization regimes, and there was a significant difference in the community composition of fungal pathogens between inorganic and organic fertilization regimes. Organic fertilization significantly enhanced predatory protists but reduced the proportions of protistan phototrophs. Co-occurrence network analysis revealed more intensive connections between fungal plant pathogens with protists, especially predatory protists, than with bacterial taxa, which was further supported by stronger associations between the community structure of fungal pathogens and predatory protists. We identified more protist consumer taxa than bacterial taxa as predictors of fungal plant pathogens, and structural equation modelling revealed a more important impact of protist consumers than bacteria on fungal pathogens. Altogether, we provide new evidence that the disease inhibitory effects of long-term organic fertilization regimes could be best explained by the potential predation pressure of protists. Our findings advance the mechanistic understanding of the role of predator-prey interactions in controlling fungal diseases, and have implications for novel biocontrol strategies to mitigate the consequences of fungal infections for plant performance. [Display omitted] •Long-term organic fertilization regimes significantly reduced the relative abundances of fungal pathogens.•Organic fertilization significantly increased the proportions of predatory protists.•Predatory protists were the best predictors of the patterns of fungal plant pathogens.•The disease suppression of organic fertilization was best explained by the predation pressure of protists.•This study advanced our understanding of the crucial roles of trophic regulations in regulating fungal plant pathogens. Soil-borne fungal pathogens pose a major threat to global agricultural production and food security. Pathogen-suppressive bacteria and plant beneficial protists are important components of soil microbiomes and essential to plant health and performance, but it remains largely unknown regarding how agricultural management practices influence the relative importance of protists and bacteria in plant disease suppression. Here, we characterized soil microbiomes (including fungi, protists, and bacteria) in bulk and sorghum rhizosphere soils with various long-term inorganic and organic fertilization regimes, and linked the changes in fungal plant pathogens with the protistan and bacterial communities. We found that the relative abundances of fungal pathogens were significantly decreased by organic fertilization regimes, and there was a significant difference in the community composition of fungal pathogens between inorganic and organic fertilization regimes. Organic fertilization significantly enhanced predatory protists but reduced the proportions of protistan phototrophs. Co-occurrence network analysis revealed more intensive connections between fungal plant pathogens with protists, especially predatory protists, than with bacterial taxa, which was further supported by stronger associations between the community structure of fungal pathogens and predatory protists. We identified more protist consumer taxa than bacterial taxa as predictors of fungal plant pathogens, and structural equation modelling revealed a more important impact of protist consumers than bacteria on fungal pathogens. Altogether, we provide new evidence that the disease inhibitory effects of long-term organic fertilization regimes could be best explained by the potential predation pressure of protists. Our findings advance the mechanistic understanding of the role of predator-prey interactions in controlling fungal diseases, and have implications for novel biocontrol strategies to mitigate the consequences of fungal infections for plant performance.Soil-borne fungal pathogens pose a major threat to global agricultural production and food security. Pathogen-suppressive bacteria and plant beneficial protists are important components of soil microbiomes and essential to plant health and performance, but it remains largely unknown regarding how agricultural management practices influence the relative importance of protists and bacteria in plant disease suppression. Here, we characterized soil microbiomes (including fungi, protists, and bacteria) in bulk and sorghum rhizosphere soils with various long-term inorganic and organic fertilization regimes, and linked the changes in fungal plant pathogens with the protistan and bacterial communities. We found that the relative abundances of fungal pathogens were significantly decreased by organic fertilization regimes, and there was a significant difference in the community composition of fungal pathogens between inorganic and organic fertilization regimes. Organic fertilization significantly enhanced predatory protists but reduced the proportions of protistan phototrophs. Co-occurrence network analysis revealed more intensive connections between fungal plant pathogens with protists, especially predatory protists, than with bacterial taxa, which was further supported by stronger associations between the community structure of fungal pathogens and predatory protists. We identified more protist consumer taxa than bacterial taxa as predictors of fungal plant pathogens, and structural equation modelling revealed a more important impact of protist consumers than bacteria on fungal pathogens. Altogether, we provide new evidence that the disease inhibitory effects of long-term organic fertilization regimes could be best explained by the potential predation pressure of protists. Our findings advance the mechanistic understanding of the role of predator-prey interactions in controlling fungal diseases, and have implications for novel biocontrol strategies to mitigate the consequences of fungal infections for plant performance. |
ArticleNumber | 160986 |
Author | He, Ji-Zheng Hu, Hang-Wei Yu, Dan-Ting Jiao, Xiaoyan Ren, Peixin Sun, Anqi Shen, Ju-Pei Wu, Bingxue Li, Fangfang |
Author_xml | – sequence: 1 givenname: Peixin surname: Ren fullname: Ren, Peixin organization: Key Laboratory for Humid Subtropical Eco-geographical Processes of the Ministry of Education, School of Geographical Sciences, Fujian Normal University, Fuzhou, China – sequence: 2 givenname: Anqi surname: Sun fullname: Sun, Anqi organization: Key Laboratory of Urban Environment and Health, Ningbo Urban Environment Observation and Research Station, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, China – sequence: 3 givenname: Xiaoyan surname: Jiao fullname: Jiao, Xiaoyan organization: College of Resource and Environment, Shanxi Agricultural University, Taiyuan, China – sequence: 4 givenname: Ju-Pei surname: Shen fullname: Shen, Ju-Pei organization: Key Laboratory for Humid Subtropical Eco-geographical Processes of the Ministry of Education, School of Geographical Sciences, Fujian Normal University, Fuzhou, China – sequence: 5 givenname: Dan-Ting surname: Yu fullname: Yu, Dan-Ting organization: Key Laboratory for Humid Subtropical Eco-geographical Processes of the Ministry of Education, School of Geographical Sciences, Fujian Normal University, Fuzhou, China – sequence: 6 givenname: Fangfang surname: Li fullname: Li, Fangfang organization: Key Laboratory for Humid Subtropical Eco-geographical Processes of the Ministry of Education, School of Geographical Sciences, Fujian Normal University, Fuzhou, China – sequence: 7 givenname: Bingxue surname: Wu fullname: Wu, Bingxue organization: Key Laboratory for Humid Subtropical Eco-geographical Processes of the Ministry of Education, School of Geographical Sciences, Fujian Normal University, Fuzhou, China – sequence: 8 givenname: Ji-Zheng surname: He fullname: He, Ji-Zheng organization: Key Laboratory for Humid Subtropical Eco-geographical Processes of the Ministry of Education, School of Geographical Sciences, Fujian Normal University, Fuzhou, China – sequence: 9 givenname: Hang-Wei surname: Hu fullname: Hu, Hang-Wei email: hang-wei.hu@unimelb.edu.au organization: Key Laboratory for Humid Subtropical Eco-geographical Processes of the Ministry of Education, School of Geographical Sciences, Fujian Normal University, Fuzhou, China |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/36528948$$D View this record in MEDLINE/PubMed |
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CitedBy_id | crossref_primary_10_1016_j_envint_2024_108511 crossref_primary_10_1016_j_isci_2024_110973 crossref_primary_10_1016_j_agee_2023_108797 crossref_primary_10_3389_fmicb_2023_1339125 crossref_primary_10_1016_j_scitotenv_2023_168049 crossref_primary_10_1007_s42729_023_01568_x crossref_primary_10_1111_mec_17228 crossref_primary_10_3390_microorganisms13030657 crossref_primary_10_1007_s11104_024_06846_w crossref_primary_10_1016_j_micres_2025_128109 crossref_primary_10_1016_j_soilbio_2023_109206 crossref_primary_10_1111_1758_2229_70024 crossref_primary_10_1002_sae2_12068 crossref_primary_10_1007_s00374_024_01845_6 crossref_primary_10_1007_s00253_024_13106_5 crossref_primary_10_1016_j_eti_2025_104161 crossref_primary_10_1016_j_pedsph_2024_07_006 crossref_primary_10_1016_j_scitotenv_2025_178658 crossref_primary_10_1016_j_ecolind_2024_112328 crossref_primary_10_1111_1462_2920_16477 |
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Keywords | Protists Plant microbiome Fungal plant pathogens Soil food web Biological interactions |
Language | English |
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Snippet | Soil-borne fungal pathogens pose a major threat to global agricultural production and food security. Pathogen-suppressive bacteria and plant beneficial... |
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SubjectTerms | agricultural management Animals autotrophs Bacteria biological control Biological interactions community structure disease control environment equations Eukaryota Fertilization food security Fungal plant pathogens fungi plant health Plant microbiome predation Predatory Behavior Protists rhizosphere Soil - chemistry Soil food web Soil Microbiology soil microorganisms |
Title | Predatory protists play predominant roles in suppressing soil-borne fungal pathogens under organic fertilization regimes |
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