Protist communities are more sensitive to nitrogen fertilization than other microorganisms in diverse agricultural soils
Tóm tắt
Agricultural food production is at the base of food and fodder, with fertilization having fundamentally and continuously increased crop yield over the last decades. The performance of crops is intimately tied to their microbiome as they together form holobionts. The importance of the microbiome for plant performance is, however, notoriously ignored in agricultural systems as fertilization disconnects the dependency of plants for often plant-beneficial microbial processes. Moreover, we lack a holistic understanding of how fertilization regimes affect the soil microbiome. Here, we examined the effect of a 2-year fertilization regime (no nitrogen fertilization control, nitrogen fertilization, and nitrogen fertilization plus straw amendment) on entire soil microbiomes (bacteria, fungi, and protist) in three common agricultural soil types cropped with maize in two seasons. We found that the application of nitrogen fertilizers more strongly affected protist than bacterial and fungal communities. Nitrogen fertilization indirectly reduced protist diversity through changing abiotic properties and bacterial and fungal communities which differed between soil types and sampling seasons. Nitrogen fertilizer plus straw amendment had greater effects on soil physicochemical properties and microbiome diversity than nitrogen addition alone. Moreover, nitrogen fertilization, even more together with straw, increased soil microbiome network complexity, suggesting that the application of nitrogen fertilizers tightened soil microbiomes interactions. Together, our results suggest that protists are the most susceptible microbiome component to the application of nitrogen fertilizers. As protist communities also exhibit the strongest seasonal dynamics, they serve as the most sensitive bioindicators of soil changes. Changes in protist communities might have long-term effects if some of the key protist hubs that govern microbiome complexities as top microbiome predators are altered. This study serves as the stepping stone to promote protists as promising agents in targeted microbiome engineering to help in reducing the dependency on exogenous unsustainably high fertilization and pesticide applications.
Tài liệu tham khảo
Lal R. Soil carbon sequestration impacts on global climate change and food security. Science. 2004;304:1623–7.
Wagg C, Bender SF, Widmer F, van der Heijden MG. Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci U S A. 2014;111:5266–70.
Loreau M. Biodiversity and ecosystem functioning: a mechanistic model. Proc Natl Acad Sci U S A. 1998;95:5632–6.
Hu HW, He JZ. Manipulating the soil microbiome for improved nitrogen management. Microbiology Australia. 2018;39:24–7.
Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH. Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol. 2013;11:789–99.
Bender SF, Wagg C, van der Heijden MGA. An underground revolution: biodiversity and soil ecological engineering for agricultural sustainability. Trends Ecol Evol. 2016;31:440–52.
Berendsen RL, Pieterse CM, Bakker PA. The rhizosphere microbiome and plant health. Trends Plant Sci. 2012;17:478–86.
McLaughlin A, Mineau P. The impact of agricultural practices on biodiversity. Agric Ecosyst Environ. 1995;55:201–12.
Sun R, Zhang XX, Guo X, Wang D, Chu H. Bacterial diversity in soils subjected to long-term chemical fertilization can be more stably maintained with the addition of livestock manure than wheat straw. Soil Biol Biochem. 2015;88:9–18.
Zhang LM, Offre PR, He JZ, Verhamme DT, Nicol GW, Prosser JI. Autotrophic ammonia oxidation by soil thaumarchaea. Proc Natl Acad Sci U S A. 2010;107:17240–5.
Hu H-W, Macdonald CA, Trivedi P, Anderson IC, Zheng Y, Holmes B, et al. Effects of climate warming and elevated CO2 on autotrophic nitrification and nitrifiers in dryland ecosystems. Soil Biol Biochem. 2016;92:1–15.
Payne RJ, Thompson AM, Standen V, Field CD, Caporn SJM. Impact of simulated nitrogen pollution on heathland microfauna, mesofauna and plants. Eur J Soil Biol. 2012;49:73–9.
Wang C, Liu D, Bai E. Decreasing soil microbial diversity is associated with decreasing microbial biomass under nitrogen addition. Soil Biol Biochem. 2018;120:126–33.
Heemsbergen DA, Berg MP, Loreau M, van Hal JR, Faber JH, Verhoef HA. Biodiversity effects on soil processes explained by interspecific functional dissimilarity. Science. 2004;306:1019–20.
Philippot L, Spor A, Henault C, Bru D, Bizouard F, Jones CM, et al. Loss in microbial diversity affects nitrogen cycling in soil. ISME J. 2013;7:1609–19.
Quan Z, Li S, Zhu F, Zhang L, He J, Wei W, et al. Fates of 15N-labeled fertilizer in a black soil-maize system and the response to straw incorporation in Northeast China. J Soils Sediments. 2017;18:1441–52.
Birkhofer K, Bezemer TM, Bloem J, Bonkowski M, Christensen S, Dubois D, et al. Long-term organic farming fosters below and aboveground biota: implications for soil quality, biological control and productivity. Soil Biol Biochem. 2008;40:2297–308.
Zeng J, Liu X, Song L, Lin X, Zhang H, Shen C, et al. Nitrogen fertilization directly affects soil bacterial diversity and indirectly affects bacterial community composition. Soil Biol Biochem. 2016;92:41–9.
Geisen S, Mitchell EAD, Adl S, Bonkowski M, Dunthorn M, Ekelund F, et al. Soil protists: a fertile frontier in soil biology research. FEMS Microbiol Rev. 2018;42:293–323.
Krashevska V, Sandmann D, Maraun M, Scheu S. Moderate changes in nutrient input alter tropical microbial and protist communities and belowground linkages. ISME J. 2014;8:1126–34.
Scharroba A, Dibbern D, Hünninghaus M, Kramer S, Moll J, Butenschoen O, et al. Effects of resource availability and quality on the structure of the micro-food web of an arable soil across depth. Soil Biol Biochem. 2012;50:1–11.
Guo S, Xiong W, Xu H, Hang X, Liu H, Xun W, et al. Continuous application of different fertilizers induces distinct bulk and rhizosphere soil protist communities. Eur J Soil Biol. 2018;88:8–14.
Lentendu G, Wubet T, Chatzinotas A, Wilhelm C, Buscot F, Schlegel M. Effects of long-term differential fertilization on eukaryotic microbial communities in an arable soil: a multiple barcoding approach. Mol Ecol. 2014;23:3341–55.
Mieczan T. Distributions of testate amoebae and ciliates in different types of peatlands and their contributions to the nutrient supply. Zool Stud. 2012;51:18–26.
Bates ST, Clemente JC, Flores GE, Walters WA, Parfrey LW, Knight R, et al. Global biogeography of highly diverse protistan communities in soil. ISME J. 2013;7:652–9.
Geisen S, Cornelia B, Jörg R, Michael B. Soil water availability strongly alters the community composition of soil protists. Pedobiologia. 2014;57:205–13.
Grossmann L, Jensen M, Heider D, Jost S, Glucksman E, Hartikainen H, et al. Protistan community analysis: key findings of a large-scale molecular sampling. ISME J. 2016;10:2269–79.
Zahn G, Wagai R, Yonemura S. The effects of amoebal bacterivory on carbon and nitrogen dynamics depend on temperature and soil structure interactions. Soil Biol Biochem. 2016;94:133–7.
Ju XT, Xing GX, Chen XP, Zhang SL, Zhang LJ, Liu XJ, et al. Reducing environmental risk by improving N management in intensive Chinese agricultural systems. Proc Natl Acad Sci U S A. 2009;106:3041–6.
Schulz-Bohm K, Geisen S, Wubs ER, Song C, de Boer W, Garbeva P. The prey’s scent - volatile organic compound mediated interactions between soil bacteria and their protist predators. ISME J. 2017;11:817–20.
Bonkowski M. Protozoa and plant growth: the microbial loop in soil revisited. New Phytol. 2004;162:617–31.
de Ruiter PC, Neutel AM, Moore JC. Energetics, patterns of interaction strengths, and stability in real ecosystems. Science. 1995;269:1257–60.
Payne RJ. Seven reasons why protists make useful bioindicators. Acta Protozool. 2013;52:105–13.
Zhou J, Jiang X, Zhou B, Zhao B, Ma M, Guan D, et al. Thirty four years of nitrogen fertilization decreases fungal diversity and alters fungal community composition in black soil in northeast China. Soil Biol Biochem. 2016;95:135–43.
Zhou Z, Wang C, Zheng M, Jiang L, Luo Y. Patterns and mechanisms of responses by soil microbial communities to nitrogen addition. Soil Biol Biochem. 2017;115:433–41.
Fierer N. Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol. 2017;15:579–90.
Eisenhauer N, Bessler H, Engels C, Gleixner G, Habekost M, Milcu A, et al. Plant diversity effects on soil microorganisms support the singular hypothesis. Ecology. 2010;91:485–96.
Delgado-Baquerizo M, Oliverio AM, Brewer TE, Benavent-Gonzalez A, Eldridge DJ, Bardgett RD, et al. A global atlas of the dominant bacteria found in soil. Science. 2018;359:320.
Wu W, Lu HP, Sastri A, Yeh YC, Gong GC, Chou WC, et al. Contrasting the relative importance of species sorting and dispersal limitation in shaping marine bacterial versus protist communities. ISME J. 2018;12:485–94.
Murase J, Hida A, Ogawa K, Nonoyama T, Yoshikawa N, Imai K. Impact of long-term fertilizer treatment on the microeukaryotic community structure of a rice field soil. Soil Biol Biochem. 2015;80:237–43.
Lu C, Chen H, Teng Z, Yuan L, Ma J, He H, et al. Effects of N fertilization and maize straw on the dynamics of soil organic N and amino acid N derived from fertilizer N as indicated by 15N labeling. Geoderma. 2018;321:118–26.
Lu C, Wang H, Chen H, Yuan L, Ma J, Shi Y, et al. Effects of N fertilization and maize straw on the transformation and fate of labeled ((NH4)-15N)(2) SO4 among three continuous crop cultivations. Agr Water Manage. 2018;208:275–83.
Eisenhauer N, Cesarz S, Koller R, Worm K, Reich PB. Global change belowground: impacts of elevated CO2, nitrogen, and summer drought on soil food webs and biodiversity. Glob Chang Biol. 2012;18:435–47.
Friman VP, Dupont A, Bass D, Murrell DJ, Bell T. Relative importance of evolutionary dynamics depends on the composition of microbial predator-prey community. ISME J. 2016;10:1352–62.
Saleem M, Fetzer I, Dormann CF, Harms H, Chatzinotas A. Predator richness increases the effect of prey diversity on prey yield. Nat Commun. 2012;3:1305.
Geisen S, Koller R, Hünninghaus M, Dumack K, Urich T, Bonkowski M. The soil food web revisited: diverse and widespread mycophagous soil protists. Soil Biol Biochem. 2016;94:10–8.
Banerjee S, Schlaeppi K, van der Heijden MGA. Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microbiol. 2018;16:567–76.
Wang S, Wang X, Han X, Deng Y. Higher precipitation strengthens the microbial interactions in semi-arid grassland soils. Glob Ecol Biogeogr. 2018;27:570–80.
Shi S, Nuccio EE, Shi ZJ, He Z, Zhou J, Firestone MK. The interconnected rhizosphere: high network complexity dominates rhizosphere assemblages. Ecol Lett. 2016;19:926–36.
Yu J, Deem LM, Crow SE, Deenik JL, Penton CR. Biochar application influences microbial assemblage complexity and composition due to soil and bioenergy crop type interactions. Soil Biol Biochem. 2018;117:97–107.
Morrien E, Hannula SE, Snoek LB, Helmsing NR, Zweers H, de Hollander M, et al. Soil networks become more connected and take up more carbon as nature restoration progresses. Nat Commun. 2017;8:14349.
Li J, Ma YB, Hu HW, Wang JT, Liu YR, He JZ. Field-based evidence for consistent responses of bacterial communities to copper contamination in two contrasting agricultural soils. Front Microbiol. 2015;6:31.
Bates ST, Berg-Lyons D, Caporaso JG, Walters WA, Knight R, Fierer N. Examining the global distribution of dominant archaeal populations in soil. ISME J. 2011;5:908–17.
Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, et al. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J. 2010;4:1340–51.
Stoeck T, Bass D, Nebel M, Christen R, Jones MD, Breiner HW, et al. Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol Ecol. 2010;19(Suppl 1):21–31.
Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, et al. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci U S A. 2012;109:6241–6.
Price MN, Dehal PS, Arkin AP. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol. 2009;26:1641–50.
Washburne AD, Morton JT, Sanders J, McDonald D, Zhu Q, Oliverio AM, et al. Methods for phylogenetic analysis of microbiome data. Nat Microbiol. 2018;3:652–61.
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6.
Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10:996–8.
Guillou L, Bachar D, Audic S, Bass D, Berney C, Bittner L, et al. The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Res. 2013;41:D597–604.
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–6.
Kenkel NC, Orloci L. Applying metric and nonmetric multidimensional scaling to ecological studies: some new results. Ecology. 1986;67:919–28.
Soffer N, Zaneveld J, Vega TR. Phage-bacteria network analysis and its implication for the understanding of coral disease. Environ Microbiol. 2015;17:1203–18.
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13:2498–504.
Hu HW, Wang JT, Li J, Li JJ, Ma YB, Chen D, et al. Field-based evidence for copper contamination induced changes of antibiotic resistance in agricultural soils. Environ Microbiol. 2016;18:3896–909.
Faust K, Sathirapongsasuti JF, Izard J, Segata N, Gevers D, Raes J, et al. Microbial co-occurrence relationships in the human microbiome. PLoS Comput Biol. 2012;8:e1002606.
Faust K, Raes J. Microbial interactions: from networks to models. Nat Rev Microbiol. 2012;10:538–50.
Hu HW, Wang JT, Li J, Shi XZ, Ma YB, Chen D, et al. Long-term nickel contamination increases the occurrence of antibiotic resistance genes in agricultural soils. Environ Sci Technol. 2017;51:790–800.
Jacomy M, Bastian M, Heymann S. Gephi: an open source software for exploring and manipulating networks. Int AAAI Conf Weblogs Soc Media. 2009.
Assenov Y, Ramirez F, Schelhorn SE, Lengauer T, Albrecht M. Computing topological parameters of biological networks. Bioinformatics. 2008;24:282–4.
Barberan A, Bates ST, Casamayor EO, Fierer N. Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J. 2012;6:343–51.
Sporns O, Honey CJ, Kotter R. Identification and classification of hubs in brain networks. PLoS One. 2007;2:e1049.
Martin Gonzalez AM, Dalsgaard B, Olesen JM. Centrality measures and the importance of generalist species in pollination networks. Ecol Complex. 2010;7:36–43.
Deng Y, Jiang YH, Yang Y, He Z, Luo F, Zhou J. Molecular ecological network analyses. BMC Bioinformatics. 2012;13:113.
Jun-Tao Wang, Yuan-Ming Zheng, Hang-Wei Hu, Jing Li, Li-Mei Zhang, Bao-Dong Chen, Wei-Ping Chen, Ji-Zheng He. Coupling of soil prokaryotic diversity and plant diversity across latitudinal forest ecosystems. Scientific Reports 2016;6:1.
Grace JB, Keeley JE. A structural equation model analysis of postfire plant diversity in California shrublands. Ecol Appl. 2006;16:503–14.
Wagner MR, Lundberg DS, Del Rio TG, Tringe SG, Dangl JL, Mitchell-Olds T. Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Nat Commun. 2016;7:12151.
Bell TH, Hassan SE, Lauron-Moreau A, Al-Otaibi F, Hijri M, Yergeau E, et al. Linkage between bacterial and fungal rhizosphere communities in hydrocarbon-contaminated soils is related to plant phylogeny. ISME J. 2014;8:331–43.
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:R60.