Abstract
The effects of protists on an indigenous soil bacterial community, putative bacterial genes involved in N-cycling, and the rice plant growth were studied in poultry litter biochar (PL) and rice husk biochar (RH) amended (with two application doses: 2% and 4% w/w) paddy field soil. The bacterial community composition, which was evaluated using 16S rRNA gene amplicon sequencing, was significantly and differentially affected by the protists, the PL and the RH. The effects of protists on the bacterial community composition were decreased by the RH and the PL treatments. The number of protist-affected bioindicator bacterial taxa was decreased from 90 to 46, 29, 43, and 21 in the 2% RH-, 4% RH-, 2% PL-, and 4% PL-treated soils, respectively. The presence of the protist significantly increased the abundance of the putative bacterial genes involved in mineralisation, dissimilatory nitrate reduction to ammonium (DNRA), and NO3- assimilation, and the same occurred with PL treatments. The rice plant growth and N uptake were always higher in the presence of protists and PL amendments. Overall our results suggest a new insight into the effects of biochar on the bacterial community via altering the trophic interactions.
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References
Adl SM (2007) Motility and migration rate of protozoa in soil columns. Soil Biol Biochem 39:700–703. https://doi.org/10.1016/j.soilbio.2006.09.008
Anderson CR, Hamonts K, Clough TJ, Condron LM (2014) Biochar does not affect soil N-transformations or microbial community structure under ruminant urine patches but does alter relative proportions of nitrogen cycling bacteria. Agric Ecosyst Environ 191:63–72. https://doi.org/10.1016/j.agee.2014.02.021
Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253. https://doi.org/10.1111/j.1541-0420.2005.00440.x
Asiloglu R, Samuel SO, Sevilir B, Akca MO, Acar Bozkurt P, Suzuki K, Murase J, Turgay OC, Harada N (2020a) Biochar affects taxonomic and functional community composition of protists. Biol Fertil Soils:1–15. https://doi.org/10.1007/s00374-020-01502-8
Asiloglu R, Shiroishi K, Suzuki K, Turgay OC, Murase J, Harada N (2020b) Protist-enhanced survival of a plant growth promoting rhizobacteria, Azospirillum sp. B510, and the growth of rice (Oryza sativa L.) plants. Appl Soil Ecol 154:103599. https://doi.org/10.1016/j.apsoil.2020.103599
Bell T, Bonsall MB, Buckling A, Whiteley AS, Goodall T, Griffiths RI (2010) Protists have divergent effects on bacterial diversity along a productivity gradient. Biol Lett 6:639–642. https://doi.org/10.1098/rsbl.2010.0027
Bhattacharjya S, Chandra R, Pareek N, Raverkar KP (2016) Biochar and crop residue application to soil: effect on soil biochemical properties, nutrient availability and yield of rice ( Oryza sativa L.) and wheat ( Triticum aestivum L.). Arch Agron Soil Sci 62:1095–1108. https://doi.org/10.1080/03650340.2015.1118760
Bonkowski M (2004) Protozoa and plant growth: the microbial loop in soil revisited. New Phytol 162:617–631. https://doi.org/10.1111/j.1469-8137.2004.01066.x
Bonkowski M, Brandt F (2002) Do soil protozoa enhance plant growth by hormonal effects? Soil Biol Biochem 34:1709–1715. https://doi.org/10.1016/S0038-0717(02)00157-8
Bonkowski M, Griffiths B, Scrimgeour C (2000) Substrate heterogeneity and microfauna in soil organic ‘hotspots’ as determinants of nitrogen capture and growth of ryegrass. Appl Soil Ecol 14:37–53. https://doi.org/10.1016/S0929-1393(99)00047-5
Bouvy M, Bettarel Y, Bouvier C, Domaizon I, Jacquet S, Le Floc’h E, Montanié H, Mostajir B, Sime-Ngando T, Torréton JP, Vidussi F, Bouvier T (2011) Trophic interactions between viruses, bacteria and nanoflagellates under various nutrient conditions and simulated climate change. Environ Microbiol 13:1842–1857. https://doi.org/10.1111/j.1462-2920.2011.02498.x
Brunauer S, Emmett PH, Teller E (1938) Adsorption of gases in multimolecular layers. J Am Chem Soc 60:309–319. https://doi.org/10.1021/ja01269a023
Chen H, Xia Q, Yang T, Bowman D, Shi W (2019) The soil microbial community of turf: linear and nonlinear changes of taxa and N-cycling gene abundances over a century-long turf development. FEMS Microbiol Ecol 95:1–14. https://doi.org/10.1093/femsec/fiy224
Chow C-ET, Kim DY, Sachdeva R, Caron DA, Fuhrman JA (2014) Top-down controls on bacterial community structure: microbial network analysis of bacteria, T4-like viruses and protists. ISME J 8:816–829. https://doi.org/10.1038/ismej.2013.199
Clarholm M (1985) Interactions of bacteria, protozoa and plants leading to mineralization of soil nitrogen. Soil Biol Biochem 17:181–187. https://doi.org/10.1016/0038-0717(85)90113-0
Crotty FV, Adl SM, Blackshaw RP, Murray PJ (2012) Using stable isotopes to differentiate trophic feeding channels within soil food webs. J Eukaryot Microbiol 59:520–526. https://doi.org/10.1111/j.1550-7408.2011.00608.x
D’Hose T, Molendijk L, Van Vooren L, van den Berg W, Hoek H, Runia W, van Evert F, ten Berge H, Spiegel H, Sandèn T, Grignani C, Ruysschaert G (2018) Responses of soil biota to non-inversion tillage and organic amendments: An analysis on European multiyear field experiments. Pedobiologia (Jena) 66:18–28. https://doi.org/10.1016/j.pedobi.2017.12.003
Dai Z, Enders A, Rodrigues JLM, Hanley KL, Brookes PC, Xu J, Lehmann J (2018) Soil fungal taxonomic and functional community composition as affected by biochar properties. Soil Biol Biochem 126:159–167. https://doi.org/10.1016/j.soilbio.2018.09.001
Darbyshire JF, Wheatley RE, Greaves MP, Inkson RHE (1974) A rapid micromethod for estimating bacterial and protozoan populations in soil. Rev Écol Biol Sol 11:465–475
Edwards CA (2003) Encyclopedia of Soil Science. Appl Soil Ecol 23:279. https://doi.org/10.1016/S0929-1393(03)00051-9
Ekelund F, Rønn R (1994) Notes on protozoa in agricultural soil with emphasis on heterotrophic flagellates and naked amoebae and their ecology. FEMS Microbiol Rev 15:321–353. https://doi.org/10.1111/j.1574-6976.1994.tb00144.x
England LS, Lee H, Trevors JT (1993) Bacterial survival in soil: Effect of clays and protozoa. Soil Biol Biochem 25:525–531. https://doi.org/10.1016/0038-0717(93)90189-I
Flues S, Bass D, Bonkowski M (2017) Grazing of leaf-associated Cercomonads (Protists: Rhizaria: Cercozoa) structures bacterial community composition and function. Environ Microbiol 19:3297–3309. https://doi.org/10.1111/1462-2920.13824
Fox JW (2007) The dynamics of top-down and bottom-up effects in food webs of varying prey diversity, composition, and productivity. Oikos 116:189–200. https://doi.org/10.1111/j.0030-1299.2007.15280.x
Geisseler D, Scow KM (2014) Long-term effects of mineral fertilizers on soil microorganisms – A review. Soil Biol Biochem 75:54–63. https://doi.org/10.1016/j.soilbio.2014.03.023
Griffiths BS (1994) Microbial-feeding nematodes and protozoa in soil: Their effectson microbial activity and nitrogen mineralization in decomposition hotspots and the rhizosphere. Plant Soil 164:25–33. https://doi.org/10.1007/BF00010107
Gul S, Whalen JK, Thomas BW, Sachdeva V, Deng H (2015) Physico-chemical properties and microbial responses in biochar-amended soils: Mechanisms and future directions. Agric Ecosyst Environ 206:46–59. https://doi.org/10.1016/j.agee.2015.03.015
Hale L, Luth M, Crowley D (2015) Biochar characteristics relate to its utility as an alternative soil inoculum carrier to peat and vermiculite. Soil Biol Biochem 81:228–235. https://doi.org/10.1016/j.soilbio.2014.11.023
Hansen BW, Andersen CMB, Hansen PJ, Nielsen TG, Vismann B, Tiselius P (2019) In situ and experimental evidence for effects of elevated pH on protistan and metazoan grazers. J Plankton Res 41:257–271. https://doi.org/10.1093/plankt/fbz020
Herdler S, Kreuzer K, Scheu S, Bonkowski M (2008) Interactions between arbuscular mycorrhizal fungi (Glomus intraradices, Glomeromycota) and amoebae (Acanthamoeba castellanii, Protozoa) in the rhizosphere of rice (Oryza sativa). Soil Biol Biochem 40:660–668. https://doi.org/10.1016/j.soilbio.2007.09.026
Hervey RJ, Greaves JE (1941) Nitrogen fixation by Azotobacter chroococcum in the presence of soil protozoa. Soil Sci 51:85–100
Homma Y, Cook RJ (1985) Influence of matric and osmotic water potentials and soil pH on the activity of giant vampyrellid amoebae. Phytopathology 75:243. https://doi.org/10.1094/Phyto-75-243
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363. https://doi.org/10.1002/bimj.200810425
Hünninghaus M, Koller R, Kramer S, Marhan S, Kandeler E, Bonkowski M (2017) Changes in bacterial community composition and soil respiration indicate rapid successions of protist grazers during mineralization of maize crop residues. Pedobiologia (Jena) 62:1–8. https://doi.org/10.1016/j.pedobi.2017.03.002
Jousset A, Scheu S, Bonkowski M (2008) Secondary metabolite production facilitates establishment of rhizobacteria by reducing both protozoan predation and the competitive effects of indigenous bacteria. Funct Ecol 22:714–719. https://doi.org/10.1111/j.1365-2435.2008.01411.x
Kamau S, Karanja NK, Ayuke FO, Lehmann J (2019) Short-term influence of biochar and fertilizer-biochar blends on soil nutrients, fauna and maize growth. Biol Fertil Soils 55:661–673. https://doi.org/10.1007/s00374-019-01381-8
Kolton M, Graber ER, Tsehansky L, Elad Y, Cytryn E (2017) Biochar-stimulated plant performance is strongly linked to microbial diversity and metabolic potential in the rhizosphere. New Phytol 213:1393–1404. https://doi.org/10.1111/nph.14253
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 Biol Biochem 38:1665–1672. https://doi.org/10.1016/j.soilbio.2005.11.027
Kurm V, van der Putten WH, Weidner S, Geisen S, Snoek BL, Bakx T, Hol WHG (2019) Competition and predation as possible causes of bacterial rarity. Environ Microbiol 21:1356–1368. https://doi.org/10.1111/1462-2920.14569
Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821. https://doi.org/10.1038/nbt.2676
Lehmann J, Rillig MC, Thies J, Masiello CA, Hockaday WC, Crowley D (2011) Biochar effects on soil biota – A review. Soil Biol Biochem 43:1812–1836. https://doi.org/10.1016/j.soilbio.2011.04.022
Liu T, Yang L, Hu Z, Xue J, Lu Y, Chen X, Griffiths BS, Whalen JK, Liu M (2020) Biochar exerts negative effects on soil fauna across multiple trophic levels in a cultivated acidic soil. Biol Fertil Soils 56:597–606. https://doi.org/10.1007/s00374-020-01436-1
Matz C, Kjelleberg S (2005) Off the hook – how bacteria survive protozoan grazing. Trends Microbiol 13:302–307. https://doi.org/10.1016/j.tim.2005.05.009
Murase J, Frenzel P (2008) Selective grazing of methanotrophs by protozoa in a rice field soil. FEMS Microbiol Ecol 65:408–414. https://doi.org/10.1111/j.1574-6941.2008.00511.x
Murase J, Noll M, Frenzel P (2006) Impact of protists on the activity and structure of the bacterial community in a rice field soil. Appl Environ Microbiol 72:5436–5444. https://doi.org/10.1128/AEM.00207-06
Pansu M, Gautheyrou J (2006) Exchangeable Cations. In: Handbook of soil analysis. Springer, Berlin, pp 667–676
Quilliam RS, Glanville HC, Wade SC, Jones DL (2013) Life in the ‘charosphere’ – Does biochar in agricultural soil provide a significant habitat for microorganisms? Soil Biol Biochem 65:287–293. https://doi.org/10.1016/j.soilbio.2013.06.004
Rajkovich S, Enders A, Hanley K, Hyland C, Zimmerman AR, Lehmann J (2012) Corn growth and nitrogen nutrition after additions of biochars with varying properties to a temperate soil. Biol Fertil Soils 48:271–284. https://doi.org/10.1007/s00374-011-0624-7
Rondon MA, Lehmann J, Ramírez J, Hurtado M (2007) Biological nitrogen fixation by common beans (Phaseolus vulgaris L.) increases with bio-char additions. Biol Fertil Soils 43:699–708. https://doi.org/10.1007/s00374-006-0152-z
Rønn R, McCaig AE, Griffiths BS, Prosser JI (2002) Impact of protozoan grazing on bacterial community structure in soil microcosms. Appl Environ Microbiol 68:6094–6105. https://doi.org/10.1128/AEM.68.12.6094-6105.2002
Rutherford PM, Juma NG (1992) Influence of texture on habitable pore space and bacterial-protozoan populations in soil. Biol Fertil Soils 12:221–227. https://doi.org/10.1007/BF00336036
Salcher M, Pernthaler J, Psenner R, Posch T (2005) Succession of bacterial grazing defense mechanisms against protistan predators in an experimental microbial community. Aquat Microb Ecol 38:215–229. https://doi.org/10.3354/ame038215
Saleem M, Fetzer I, Dormann CF, Harms H, Chatzinotas A (2012) Predator richness increases the effect of prey diversity on prey yield. Nat Commun 3:1305. https://doi.org/10.1038/ncomms2287
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60. https://doi.org/10.1186/gb-2011-12-6-r60
Singh BN (1941) Selectivity in bacterial food by soil amoebae in pure mixed culture and in sterilized soil. Ann Appl Biol 28:52–64. https://doi.org/10.1111/j.1744-7348.1941.tb07536.x
Singh BN (1942) Selection of bacterial food by soil flagellates and amoebae. Ann Appl Biol 29:18–22. https://doi.org/10.1111/j.1744-7348.1942.tb06917.x
Trap J, Bonkowski M, Plassard C, Villenave C, Blanchart E (2016) Ecological importance of soil bacterivores for ecosystem functions. Plant Soil 398:1–24. https://doi.org/10.1007/s11104-015-2671-6
Truog E (1930) The determination of the readily available phosphorus of soils. Agron J 22:874–882. https://doi.org/10.2134/agronj1930.00021962002200100008x
Wang W, Shor LM, LeBoeuf EJ, Wikswo JP, Kosson DS (2005) Mobility of protozoa through narrow channels. Appl Environ Microbiol 71:4628–4637. https://doi.org/10.1128/AEM.71.8.4628-4637.2005
Woolf D, Amonette JE, Street-Perrott FA, Lehmann J, Joseph S (2010) Sustainable biochar to mitigate global climate change. Nat Commun 1:1–9. https://doi.org/10.1038/ncomms1053
Wright DA, Killham K, Glover LA, Prosser JI (1995) Role of pore size location in determining bacterial activity during predation by protozoa in soil. Appl Environ Microbiol 61:3537–3543. https://doi.org/10.1128/AEM.61.10.3537-3543.1995
Wu H, Zeng G, Liang J, Chen J, Xu J, Dai J, Li X, Chen M, Xu P, Zhou Y, Li F, Hu L, Wan J (2016) Responses of bacterial community and functional marker genes of nitrogen cycling to biochar, compost and combined amendments in soil. Appl Microbiol Biotechnol 100:8583–8591. https://doi.org/10.1007/s00253-016-7614-5
Zahn G, Wagai R, Yonemura S (2016) The effects of amoebal bacterivory on carbon and nitrogen dynamics depend on temperature and soil structure interactions. Soil Biol Biochem 94:133–137. https://doi.org/10.1016/j.soilbio.2015.11.021
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This research was supported by The Yanmar Environmental Sustainability Support Association (K30059) and by a Kakenhi grant (19H00305H) from the Japan Society for the Promotion of Science to R.A.
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RA conceived and designed the study, analysed the sequence data, performed bioinformatic and statistical analyses and prepared the manuscript. RA and JM interpreted the data. RA, BS, SOS, MA, MOA and OCT performed the laboratory works. MA, KS, OCT, JM and NH provided feedback and comments. All authors read and approved the final manuscript.
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Asiloglu, R., Sevilir, B., Samuel, S.O. et al. Effect of protists on rhizobacterial community composition and rice plant growth in a biochar amended soil. Biol Fertil Soils 57, 293–304 (2021). https://doi.org/10.1007/s00374-020-01525-1
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DOI: https://doi.org/10.1007/s00374-020-01525-1