Predatory Protists: The Key Players in the Quest for Sustainable Agricultural Practices

Yıl 2024, Cilt: 30 Sayı: 3, 436 - 443, 23.07.2024

Seda Ozer Bodur Mayu Fujino Rasit Asiloglu

https://doi.org/10.15832/ankutbd.1447822

Öz

To overcome the global problem of food shortage while supporting sustainable life on Earth, we must appreciate the critical importance of soil microorganisms—the key drivers of essential ecosystem services such as nutrient cycling and plant productivity. Protists are one of the major microbial groups in soil ecosystem including primary producers, decomposers, predators, and symbionts. The diverse morphologies and feeding strategies of predatory protists, including amoebae, ciliates, and flagellates, contribute to their versatility in capturing prey. Particularly, trophic interactions between protists and bacteria play a crucial role in regulating bacterial communities in the soil. Protists selectively prey on bacteria, influencing community composition, and enhancing microbial activity. The impact extends to nutrient cycling, secondary metabolite production, and even antibiotic resistance in soil bacterial communities. Despite recent advances, the field of applied protistology remains underexplored, necessitating further research to bridge the gap between theoretical potential and practical application. We call for increased scientific attention, research efforts, and practical implementations to fully harness the benefits of soil protistology for future agricultural practices. In this article, we introduced the frequently overlooked essential roles of predatory protists in soil ecosystem and their potential usage in sustainable agriculture.

Anahtar Kelimeler

Predatory Protist, Soil Protists, Sustainable Agriculture, Trophic Interactions, Plant Growth, Applied Protistology

Etik Beyan

NA

Destekleyen Kurum

NA

Proje Numarası

Japan Society for the Promotion of Science (JSPS) (Grant No. JP22K14804).

Teşekkür

NA

Kaynakça

• Adl S M, Simpson A G, Lane C E, Lukeš J, Bass D, Bowser S S & Spiegel F W (2012). The revised classification of eukaryotes. Journal of eukaryotic microbiology 59(5): 429-514
• Asiloglu R (2022). Biochar–microbe interaction: more protist research is needed. Biochar 4(1): 72
• 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 Nutrition 62(5-6): 440-446
• Asiloglu R & Murase J (2017). Microhabitat segregation of heterotrophic protists in the rice (Oryza sativa L.) rhizosphere. Rhizosphere 4: 82-88
• 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 Nutrition 61(5): 761-768
• Asiloglu R, Kenya K, Samuel S O, Sevilir B, Murase J, Suzuki K & Harada N (2021c). 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 and Biochemistry 156: 108186
• Asiloglu R, Samuel S O, Sevilir B, Akca M O, Acar Bozkurt P, Suzuki K & Harada N (2021a). Biochar affects taxonomic and functional community composition of protists. Biology and Fertility of Soils 57: 15-29
• Asiloglu R, Shiroishi K, Suzuki K, Turgay O C & Harada N (2021b). 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 and Biochemistry 161: 108397
• 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
• Bahroun A, Jousset A, Mrabet M, Mhamdi R & Mhadhbi H (2021). Protists modulate Fusarium root rot suppression by beneficial bacteria. Applied Soil Ecology 168: 104158
• Bodur S O, Samuel S O, Suzuki K, Harada N & Asiloglu R (2024). Nitrogen-based fertilizers differentially affect protist community composition in paddy field soils. Soil Ecology Letters 6(3): 230221
• Bonkowski M (2004). Protozoa and plant growth: the microbial loop in soil revisited. New Phytologist 162(3): 617-631
• Bonkowski M & Brandt F (2002). Do soil protozoa enhance plant growth by hormonal effects? Soil Biology and Biochemistry 34(11): 1709-1715
• Bonkowski M, Griffiths B & Scrimgeour C (2000). Substrate heterogeneity and microfauna in soil organic ‘hotspots’ as determinants of nitrogen capture and growth of ryegrass. Applied Soil Ecology 14(1): 37-53
• Bunting L A, Neilson J B & Bulmer G S (1979). Cryptococcus neoformans: gastronomic delight of a soil ameba. Sabouraudia 17(3): 225-232.
• Caron D A, Worden A Z, Countway P D, Demir E & Heidelberg K B (2009). Protists are microbes too: a perspective. The ISME journal 3(1): 4-12
• Clarholm M (1985). Interactions of bacteria, protozoa and plants leading to mineralization of soil nitrogen. Soil Biology and Biochemistry 17(2): 181-187
• Creevy A L, Fisher J, Puppe D & Wilkinson D M (2016). Protist diversity on a nature reserve in NW England—With particular reference to their role in soil biogenic silicon pools. Pedobiologia 59(1-2): 51-59
• Dumack K, Müller M E & Bonkowski M (2016). Description of Lecythium terrestris sp. nov.(Chlamydophryidae, Cercozoa), a soil dwelling protist feeding on fungi and algae. Protist 167(2): 93-105
• Fujino M, Suzuki K, Harada N & Asiloglu R (2023). Protists modulate active bacterial community composition in paddy field soils. Biology and Fertility of Soils 59(7): 709-721
• Gao F, Warren A, Zhang Q, Gong J, Miao M, Sun P & Song W (2016). The all-data-based evolutionary hypothesis of ciliated protists with a revised classification of the phylum Ciliophora (Eukaryota, Alveolata). Scientific Reports 6(1): 24874
• Gao Z, Karlsson I, Geisen S, Kowalchuk G & Jousset A (2019). Protists: puppet masters of the rhizosphere microbiome. Trends in Plant Science 24(2): 165-176
• Geisen S, Koller R, Huenninghaus M, Dumack K, Urich T & Bonkowski M (2016). The soil food web revisited: diverse and widespread mycophagous soil protists. Soil Biology and Biochemistry 94: 10-18
• Geisen S, Mitchell E A, Adl S, Bonkowski M, Dunthorn M, Ekelund F & Lara E (2018). Soil protists: a fertile frontier in soil biology research. FEMS Microbiology Reviews, 42(3): 293-323
• Geisen S, Mitchell E A, Wilkinson D M, Adl S, Bonkowski M, Brown M W & Lara E (2017). Soil protistology rebooted: 30 fundamental questions to start with. Soil Biology and Biochemistry 111: 94-103
• Geisen S, Rosengarten J, Koller R, Mulder C, Urich T & Bonkowski M (2015). Pack hunting by a common soil amoeba on nematodes. Environmental microbiology 17(11): 4538-4546
• Gómez W, Buela L, Castro L T, Chaparro V, Ball M M & Yarzábal L A (2010). Evidence for gluconic acid production by Enterobacter intermedium as an efficient strategy to avoid protozoan grazing. Soil Biology and Biochemistry 42(5): 822-830
• Gonzalez J M, Sherr E B & Sherr B F (1990). Size-selective grazing on bacteria by natural assemblages of estuarine flagellates and ciliates. Applied and Environmental Microbiology 56(3): 583-589
• Guo S, Tao C, Jousset A, Xiong W, Wang Z, Shen Z & Geisen S (2022). Trophic interactions between predatory protists and pathogen-suppressive bacteria impact plant health. The ISME Journal 16(8): 1932-1943
• Guo S, Xiong W, Hang X, Gao Z, Jiao Z, Liu H & Geisen S (2021). Protists as main indicators and determinants of plant performance. Microbiome 9: 1-11 Hairston N G, Smith F E & Slobodkin L B (1960). Community structure, population control, and competition. The american naturalist 94(879): 421-425
• Heal O W (1963). Soil fungi as food for amoebae. Soil organisms pp. 289-297 Hervey R J & Greaves J E (1941). Nitrogen Fixation by Azotobacter Chroococcum in the Presence Of Soil Protozoa. Soil Science 51(2): 85-100
• Ratsak C H, Maarsen K A & Kooijman S A L M (1996). Effects of protozoa on carbon mineralization in activated sludge. Water Research 30(1): 1-12
• Hu X, Gu H, Liu J, Wei D, Zhu P, Zhou B & Wang G (2024). Different long-term fertilization regimes affect soil protists and their top-down control on bacterial and fungal communities in Mollisols. Science of The Total Environment 908: 168049
• Huang X, Wang J, Dumack K, Liu W, Zhang Q, He Y & Li, Y (2021). Protists modulate fungal community assembly in paddy soils across climatic zones at the continental scale. Soil Biology and Biochemistry 160: 108358
• Jan P (2008). The twilight of Sarcodina: a molecular perspective on the polyphyletic origin of amoeboid protists. Protistology 5(4): 281-302
• Jansson J K, McClure R & Egbert R G (2023). Soil microbiome engineering for sustainability in a changing environment. Nature Biotechnology 41(12): 1716-1728
• Jassey V E, Hamard S, Lepère C, Céréghino R, Corbara B, Küttim M & Carrias J F (2022). Photosynthetic microorganisms effectively contribute to bryophyte CO2 fixation in boreal and tropical regions. ISME Communications 2(1): 64
• Jousset A (2017). Application of protists to improve plant growth in sustainable agriculture. Rhizotrophs: Plant growth promotion to bioremediation pp. 263-273
• Jousset A & Bonkowski M (2010). The model predator Acanthamoeba castellanii induces the production of 2, 4, DAPG by the biocontrol strain Pseudomonas fluorescens Q2-87. Soil Biology and Biochemistry 42(9): 1647-1649
• Jousset A, Rochat L, Lanoue A, Bonkowski M, Keel C & Scheu S (2011). Plants respond to pathogen infection by enhancing the antifungal gene expression of root-associated bacteria. Molecular Plant-Microbe Interactions 24(3): 352-358
• Jürgens K & Massana R (2008). Protistan grazing on marine bacterioplankton. Microbial ecology of the oceans 383-441
• Kreuzer K, Adamczyk J, Iijima M, Wagner M, Scheu S & Bonkowski M (2006). Grazing of a common species of soil protozoa (Acanthamoeba castellanii) affects rhizosphere bacterial community composition and root architecture of rice (Oryza sativa L.). Soil Biology and Biochemistry 38(7): 1665-1672
• Krome K, Rosenberg K, Dickler C, Kreuzer K, Ludwig-Müller J, Ullrich-Eberius C & Bonkowski M (2010). Soil bacteria and protozoa affect root branching via effects on the auxin and cytokinin balance in plants. Plant and Soil 328: 191-201
• Kuikman P J, Lekkerkerk L J A & Van Veen J A (1991). Carbon Dynamics of a Soil Planted with Wheat under an Elevated Atmospheric CO2. Advances in soil organic matter research: The impact on agriculture and the Environment 267 pp
• Levrat P, Pussard M & Alabouvette C (1992). Enhanced bacterial metabolism of a Pseudomonas strain in response to the addition of culture filtrate of a bacteriophagous amoeba. European journal of protistology 28(1): 79-84
• Matz C & Kjelleberg S (2005). Off the hook–how bacteria survive protozoan grazing. Trends in microbiology 13(7): 302-307
• Matz C, Boenigk J, Arndt H & Jürgens K (2002). Role of bacterial phenotypic traits in selective feeding of the heterotrophic nanoflagellate Spumella sp. Aquatic microbial ecology 27(2): 137-148
• Mazzola M, De Bruijn I, Cohen M F & Raaijmakers J M (2009). Protozoan-induced regulation of cyclic lipopeptide biosynthesis is an effective predation defense mechanism for Pseudomonas fluorescens. Applied and Environmental Microbiology 75(21): 6804-6811
• Mitchell D R (2007). The evolution of eukaryotic cilia and flagella as motile and sensory organelles. Eukaryotic membranes and cytoskeleton: Origins and evolution pp. 130-140
• Murase J & Asiloglu R (2023). Protists: the hidden ecosystem players in a wetland rice field soil. Biology and Fertility of Soils pp. 1-15
• Murase J & Frenzel P (2008). Selective grazing of methanotrophs by protozoa in a rice field soil. FEMS microbiology ecology 65(3): 408-414
• Murase J, Noll M & Frenzel P (2006). Impact of protists on the activity and structure of the bacterial community in a rice field soil. Applied and environmental microbiology 72(8): 5436-5444
• Nguyen T B A, Bonkowski M, Dumack K, Chen Q L, He J Z & Hu H W (2023). Protistan predation selects for antibiotic resistance in soil bacterial communities. The ISME Journal 17(12): 2182-2189
• Nielsen L T & Kiørboe T (2021). Foraging trade-offs, flagellar arrangements, and flow architecture of planktonic protists. Proceedings of the National Academy of Sciences 118(3): e2009930118
• Nikolaev S I, Berney C, Fahrni J F, Bolivar I, Polet S, Mylnikov A P & Pawlowski J (2004). The twilight of Heliozoa and rise of Rhizaria, an emerging supergroup of amoeboid eukaryotes. Proceedings of the National Academy of Sciences 101(21): 8066-8071
• Old K M & Darbyshire J F (1978). Soil fungi as food for giant amoebae. Soil Biology and Biochemistry 10(2): 93-100
• Pernthaler J (2005). Predation on prokaryotes in the water column and its ecological implications. Nature Reviews Microbiology 3(7): 537-546
• Ratsak C H, Maarsen K A & Kooijman S A L M (1996). Effects of protozoa on carbon mineralization in activated sludge. Water Research 30(1): 1-12
• Rodrı́guez H & Fraga R (1999). Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnology advances 17(4-5): 319-339
• Rønn R M, Griffiths B S & Young I M (2001). Protozoa, nematodes and N-mineralization across a prescribed soil textural gradient. Pedobiologia 45(6): 481-495
• Rosenberg K, Bertaux J, Krome K, Hartmann A, Scheu S & Bonkowski M (2009). Soil amoebae rapidly change bacterial community composition in the rhizosphere of Arabidopsis thaliana. The ISME Journal 3(6): 675-684
• Schulz-Bohm K, Geisen S, Wubs E J, Song C, de Boer W & Garbeva P (2017). The prey’s scent–volatile organic compound mediated interactions between soil bacteria and their protist predators. The ISME journal 11(3): 817-820
• Seppey C V, Singer D, Dumack K, Fournier B, Belbahri L, Mitchell E A & Lara E (2017). Distribution patterns of soil microbial eukaryotes suggests widespread algivory by phagotrophic protists as an alternative pathway for nutrient cycling. Soil Biology and Biochemistry 112: 68-76
• Sherr B F, Sherr E B & Berman T (1983). Grazing, growth, and ammonium excretion rates of a heterotrophic microflagellate fed with four species of bacteria. Applied and Environmental Microbiology 45(4): 1196-1201
• Šimek K, Vrba J & Hartman P (1994). Size-selective feeding by Cyclidium sp. on bacterioplankton and various sizes of cultured bacteria. FEMS microbiology ecology 14(2): 157-167
• Trivedi P, Leach J E, Tringe S G, Sa T & Singh B K (2020). Plant–microbiome interactions: from community assembly to plant health. Nature reviews microbiology 18(11): 607-621
• Verity P G (1991). Feeding in planktonic protozoans: evidence for non‐random acquisition of prey. The Journal of protozoology 38(1): 69-76.
• Wang B, Chen C, Xiao Y M, Chen K Y, Wang J, Zhao S & Zhou G Y (2024). Trophic relationships between protists and bacteria and fungi drive the biogeography of rhizosphere soil microbial community and impact plant physiological and ecological functions. Microbiological Research 280: 127603
• Xiong W, Song Y, Yang K, Gu Y, Wei Z, Kowalchuk G A & Geisen S (2020). Rhizosphere protists are key determinants of plant health. Microbiome 8: 1-9
• Xue P, Minasny B, McBratney A, Jiang Y & Luo Y (2023). Land use effects on soil protists and their top-down regulation on bacteria and fungi in soil profiles. Applied soil ecology 185: 104799