Pinpointing the distinctive impacts of ten cover crop species on the resident and active fractions of the soil microbiome

Applied Soil Ecology - Tập 190 - Trang 105012 - 2023
Sara G. Cazzaniga1,2, Lize Braat1,3, Sven van den Elsen1, Carin Lombaers2, Johnny Visser4, Lia Obinu1,5, Jose G. Maciá-Vicente6, Joeke Postma2, Liesje Mommer7, Johannes Helder1
1Laboratory of Nematology, Wageningen University & Research, P.O. Box 8123, 6700 ES Wageningen, the Netherlands
2Biointeractions and Plant Health, Wageningen University & Research, P.O. Box 16, 6700, AA Wageningen, the Netherlands
3Plant Breeding, Wageningen University & Research, P.O. Box 384, 6700 AJ, Wageningen, The Netherlands
4Field Crops, Wageningen University & Research, Edelhertweg 1, 8219, PH, Lelystad, The Netherlands
5Department of Agricultural Sciences, University of Sassari, Viale Italia 39A, 07100 Sassari, Sardinia, Italy
6Plant Ecology and Nature Conservation Group, Wageningen University & Research, P.O. Box 47, 6700 AA Wageningen, the Netherlands
7Forest Ecology and Forest Management Group, Wageningen University & Research, P.O. Box 47, 6700 AA Wageningen, the Netherlands

Tài liệu tham khảo

Bacq-Labreuil, 2019, Cover crop species have contrasting influence upon soil structural genesis and microbial community phenotype, Sci. Rep., 9, 1, 10.1038/s41598-019-43937-6 Badri, 2009, Regulation and function of root exudates, Plant Cell Environ., 32, 666, 10.1111/j.1365-3040.2009.01926.x Bais, 2006, The role of root exudates in rhizosphere interactions with plants and other organisms, Annu. Rev. Plant Biol., 57, 233, 10.1146/annurev.arplant.57.032905.105159 Bakker, 2016, The potential for cereal rye cover crops to host corn seedling pathogens, Phytopathology, 106, 591, 10.1094/PHYTO-09-15-0214-R Banerjee, 2019, Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots, ISME J., 13, 1722, 10.1038/s41396-019-0383-2 Bay, 2021, Agricultural management affects the active rhizosphere bacterial community composition and nitrification, mSystems, 6, 10.1128/mSystems.00651-21 Bensch, 2012, The genus Cladosporium, Stud. Mycol., 72, 1, 10.3114/sim0003 Berendsen, 2012, The rhizosphere microbiome and plant health, Trends Plant Sci., 17, 478, 10.1016/j.tplants.2012.04.001 Berg, 2009, Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere, FEMS Microbiol. Ecol., 68, 1, 10.1111/j.1574-6941.2009.00654.x Blagodatskaya, 2013, Active microorganisms in soil: critical review of estimation criteria and approaches, Soil Biol. Biochem., 67, 192, 10.1016/j.soilbio.2013.08.024 Blanco-Canqui, 2015, Cover crops and ecosystem services: insights from studies in temperate soils, Agron. J., 107, 2449, 10.2134/agronj15.0086 Blazewicz, 2013, Evaluating rRNA as an indicator of microbial activity in environmental communities: limitations and uses, ISME J., 7, 2061, 10.1038/ismej.2013.102 Bolyen, 2019, Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2, Nat. Biotechnol., 37, 852, 10.1038/s41587-019-0209-9 Bonkowski, 2004, Protozoa and plant growth: the microbial loop in soil revisited, New Phytol., 162, 617, 10.1111/j.1469-8137.2004.01066.x Bressan, 2009, Exogenous glucosinolate produced by Arabidopsis thaliana has an impact on microbes in the rhizosphere and plant roots, ISME J., 3, 1243, 10.1038/ismej.2009.68 Callahan, 2016, DADA2: high-resolution sample inference from Illumina amplicon data, Nat. Methods, 13, 581, 10.1038/nmeth.3869 Callahan, 2017, Exact sequence variants should replace operational taxonomic units in marker-gene data analysis, ISME J., 11, 2639, 10.1038/ismej.2017.119 Cheng, 2016, Phylogenetic relationships in the Festuca-Lolium complex (Loliinae; Poaceae): new insights from chloroplast sequences, Front. Ecol. Evol., 4, 89, 10.3389/fevo.2016.00089 Choesin, 1991, Allyl isothiocyanate release and the allelopathic potential of Brassica napus (Brassicaceae), Am. J. Bot., 78, 1083, 10.1002/j.1537-2197.1991.tb14516.x Clarholm, 1985, Interactions of bacteria, protozoa and plants leading to mineralization of soil nitrogen, Soil Biol. Biochem., 17, 181, 10.1016/0038-0717(85)90113-0 Cloutier, 2023, Tillage intensity and plant rhizosphere selection shape bacterial-archaeal assemblage diversity and nitrogen cycling genes, Soil Tillage Res., 225, 10.1016/j.still.2022.105525 Cordero, 2020, Bacterial microbiome associated with the rhizosphere and root interior of crops in Saskatchewan, Canada, Can. J. Microbiol., 66, 71, 10.1139/cjm-2019-0330 Cosme, 2018, Non-mycorrhizal plants: the exceptions that prove the rule, Trends Plant Sci., 23, 577, 10.1016/j.tplants.2018.04.004 Csardi, 2006, The igraph software package for complex network research, Int. J. Complex Syst., 1695, 1 Doornbos, 2012, Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. A review, Agron. Sustain. Dev., 32, 227, 10.1007/s13593-011-0028-y Elhakeem, 2021, Do cover crop mixtures give higher and more stable yields than pure stands?, Field Crop Res., 270, 10.1016/j.fcr.2021.108217 Eyhorn, 2019, Sustainability in global agriculture driven by organic farming, Nat. Sustain., 2, 253, 10.1038/s41893-019-0266-6 Fierer, 2017, Embracing the unknown: disentangling the complexities of the soil microbiome, Nat. Rev. Microbiol., 15, 579, 10.1038/nrmicro.2017.87 Filion, 2009, Permeabilization and hybridization protocols for rapid detection of Bacillus spores using fluorescence in situ hybridization, J. Microbiol. Methods, 77, 29, 10.1016/j.mimet.2008.12.009 Finney, 2017, Living cover crops have immediate impacts on soil microbial community structure and function, J. Soil Water Conserv., 72, 361, 10.2489/jswc.72.4.361 Fiore-Donno, 2022, Soil compartments (bulk soil, litter, root and rhizosphere) as main drivers of soil protistan communities distribution in forests with different nitrogen deposition, Soil Biol. Biochem., 168, 10.1016/j.soilbio.2022.108628 Fitzpatrick, 2018, Assembly and ecological function of the root microbiome across angiosperm plant species, Proc. Natl. Acad. Sci. U. S. A., 115, E1157, 10.1073/pnas.1717617115 Friedman, 2012, Inferring correlation networks from genomic survey data, PLoS Comput. Biol., 8, 10.1371/journal.pcbi.1002687 Gao, 2019, Protists: puppet masters of the rhizosphere microbiome, Trends Plant Sci., 24, 165, 10.1016/j.tplants.2018.10.011 Geisen, 2018, Soil protists: a fertile frontier in soil biology research, FEMS Microbiol. Rev., 42, 293, 10.1093/femsre/fuy006 Gkarmiri, 2017, Identifying the active microbiome associated with roots and rhizosphere soil of oilseed rape, Appl. Environ. Microbiol., 83, 10.1128/AEM.01938-17 Glöckner, 2017, 25 years of serving the community with ribosomal RNA gene reference databases and tools, J. Biotechnol., 261, 169, 10.1016/j.jbiotec.2017.06.1198 Griffiths, 2022, Optimisation of root traits to provide enhanced ecosystem services in agricultural systems: a focus on cover crops, Plant Cell Environ., 45, 751, 10.1111/pce.14247 Guillou, 2012, The Protist ribosomal reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy, Nucleic Acids Res., 41, D597, 10.1093/nar/gks1160 Gupta, 2020, Robust demarcation of the family Caryophanaceae (Planococcaceae) and its different genera including three novel genera based on phylogenomics and highly specific molecular signatures, Front. Microbiol., 10, 2821, 10.3389/fmicb.2019.02821 Gustavsen, 2019, RCy3: network biology using Cytoscape from within R, F1000Research, 8, 10.12688/f1000research.20887.2 Harkes, 2019, Conventional and organic soil management as divergent drivers of resident and active fractions of major soil food web constituents, Sci. Rep., 9, 1, 10.1038/s41598-019-49854-y Harkes, 2021, Characterization of the habitat-and season-independent increase in fungal biomass induced by the invasive giant goldenrod and its impact on the fungivorous nematode community, Microorganisms, 9, 1, 10.3390/microorganisms9020437 Hirano, 2019, Difficulty in inferring microbial community structure based on co-occurrence network approaches, BMC Bioinformatics, 20, 1, 10.1186/s12859-019-2915-1 Hooks, 2010, Using marigold (Tagetes spp.) as a cover crop to protect crops from plant-parasitic nematodes, Appl. Soil Ecol., 46, 307, 10.1016/j.apsoil.2010.09.005 Hudek, 2022, Functional root trait-based classification of cover crops to improve soil physical properties, Eur. J. Soil Sci., 73, 10.1111/ejss.13147 Isobe, 2001, Flavonoids in the extract and exudate of the roots of leguminous crops, Plant Prod. Sci., 4, 278, 10.1626/pps.4.278 Jousset, 2008, Secondary metabolite production facilitates establishment of rhizobacteria by reducing both protozoan predation and the competitive effects of indigenous bacteria, Funct. Ecol., 22, 714, 10.1111/j.1365-2435.2008.01411.x Kaye, 2017, Using cover crops to mitigate and adapt to climate change. A review, Agron. Sustain. Dev., 37, 1, 10.1007/s13593-016-0410-x Kim, 2020, Do cover crops benefit soil microbiome? A meta-analysis of current research, Soil Biol. Biochem., 142, 10.1016/j.soilbio.2019.107701 Korthals, 2014, Long-term effects of eight soil health treatments to control plant-parasitic nematodes and Verticillium dahliae in agro-ecosystems, Appl. Soil Ecol., 76, 112, 10.1016/j.apsoil.2013.12.016 Kurtz, 2021 Lackner, 2011, Parascedosporium and its relatives: phylogeny and ecological trends, IMA Fungus, 2, 39, 10.5598/imafungus.2011.02.01.07 Lahti, 2012, Microbiome R package, Bioconductor. Lennon, 2011, Microbial seed banks: the ecological and evolutionary implications of dormancy, Nat. Rev. Microbiol., 9, 119, 10.1038/nrmicro2504 Lentendu, 2014, Effects of long-term differential fertilization on eukaryotic microbial communities in an arable soil: a multiple barcoding approach, Mol. Ecol., 23, 3341, 10.1111/mec.12819 Li, 2020, Effects of continuous cropping of sugar beet (Beta vulgaris L.) on its endophytic and soil bacterial community by high-throughput sequencing, Ann. Microbiol., 70, 1, 10.1186/s13213-020-01583-8 Lin, 2020, Analysis of compositions of microbiomes with bias correction, Nat. Commun., 11, 1, 10.1038/s41467-020-17041-7 Longley, 2020, Crop management impacts the soybean (Glycine max) microbiome, Front. Microbiol., 11, 1116, 10.3389/fmicb.2020.01116 Lugtenberg, 2009, Plant-growth-promoting rhizobacteria, Annu. Rev. Microbiol., 63, 541, 10.1146/annurev.micro.62.081307.162918 Lupatini, 2014, Network topology reveals high connectance levels and few key microbial genera within soils, Front. Environ. Sci., 2, 10, 10.3389/fenvs.2014.00010 Marzano, 2015, Organic transition effects on soilborne diseases of soybean and populations of Pseudomonadaceae, Agron. J., 107, 1087, 10.2134/agronj14.0318 McMurdie, 2013, Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data, PLoS One, 8, 10.1371/journal.pone.0061217 Micallef, 2009, Plant age and genotype impact the progression of bacterial community succession in the Arabidopsis rhizosphere, Plant Signal. Behav., 4, 777, 10.4161/psb.4.8.9229 Mielke, 2022, Nematode grazing increases the allocation of plant-derived carbon to soil bacteria and saprophytic fungi, and activates bacterial species of the rhizosphere, Pedobiologia, 90, 10.1016/j.pedobi.2021.150787 Mikryukov, 2018, metagMisc: an R package for metagenomic analysis, Zenodo Moora, 2014, Anthropogenic land use shapes the composition and phylogenetic structure of soil arbuscular mycorrhizal fungal communities, FEMS Microbiol. Ecol., 90, 609, 10.1111/1574-6941.12420 Normile, 1999, Crop scientists seek a new revolution, Science, 283, 310, 10.1126/science.283.5400.310 Ofek, 2014, Host signature effect on plant root-associated microbiomes revealed through analyses of resident vs. active communities, Environ. Microbiol., 16, 2157, 10.1111/1462-2920.12228 Oksanen, 2013 Pascale, 2019, Modulation of the root microbiome by plant molecules: the basis for targeted disease suppression and plant growth promotion, Front. Plant Sci., 10, 1741, 10.3389/fpls.2019.01741 Pathan, 2020, 17 Paulson, 2013, Differential abundance analysis for microbial marker-gene surveys, Nat. Methods, 10, 1200, 10.1038/nmeth.2658 Pausch, 2018, Carbon budgets of top- and subsoil food webs in an arable system, Pedobiologia, 69, 29, 10.1016/j.pedobi.2018.06.002 Pedregosa, 2011, Scikit-learn: machine learning in Python, J. Mach. Learn. Res., 12, 2825 Rossmann, 2020, Multitrophic interactions in the rhizosphere microbiome of wheat: from bacteria and fungi to protists, FEMS Microbiol. Ecol., 96, fiaa032, 10.1093/femsec/fiaa032 Saleem, 2018, Impact of root system architecture on rhizosphere and root microbiome, Rhizosphere, 6, 47, 10.1016/j.rhisph.2018.02.003 Sanaullah, 2012, Carbon allocation in grassland communities under drought stress followed by 14C pulse labeling, Soil Biol. Biochem., 55, 132, 10.1016/j.soilbio.2012.06.004 Sandoval-Denis, 2016, New species of Cladosporium associated with human and animal infections, Persoonia, 36, 281, 10.3767/003158516X691951 Sandoval-Denis, 2016, Phylogeny and taxonomic revision of Microascaceae with emphasis on synnematous fungi, Stud. Mycol., 83, 193, 10.1016/j.simyco.2016.07.002 Santos, 2020, Land use as a driver for protist community structure in soils under agricultural use across Europe, Sci. Total Environ., 717, 10.1016/j.scitotenv.2020.137228 Schlaeppi, 2014, Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives, Proc. Natl. Acad. Sci., 111, 585, 10.1073/pnas.1321597111 Schrama, 2018, Crop yield gap and stability in organic and conventional farming systems, Agric. Ecosyst. Environ., 256, 123, 10.1016/j.agee.2017.12.023 Schratzberger, 2019, A worm’s world: ecological flexibility pays off for free-living nematodes in sediments and soils, BioScience, 69, 867, 10.1093/biosci/biz086 Schreiner, 1993, Mustards, mustard oils and mycorrhizas, New Phytol., 123, 107, 10.1111/j.1469-8137.1993.tb04536.x Shannon, 2003, Cytoscape: a software environment for integrated models of biomolecular interaction networks, Genome Res., 13, 2498, 10.1101/gr.1239303 Shi, 2016, The interconnected rhizosphere: high network complexity dominates rhizosphere assemblages, Ecol. Lett., 19, 926, 10.1111/ele.12630 Tao, 2018, Integrated network analysis reveals the importance of microbial interactions for maize growth, Appl. Microbiol. Biotechnol., 102, 3805, 10.1007/s00253-018-8837-4 Thavarajah, 2012, Detection of common vetch (Vicia sativa L.) in lentil (Lens culinaris L.) using unique chemical fingerprint markers, Food Chem., 135, 2203, 10.1016/j.foodchem.2012.06.124 Tkacz, 2015, Stability and succession of the rhizosphere microbiota depends upon plant type and soil composition, ISME J., 9, 2349, 10.1038/ismej.2015.41 Tribouillois, 2015, A functional characterisation of a wide range of cover crop species: growth and nitrogen acquisition rates, leaf traits and ecological strategies, PLoS One, 10, 10.1371/journal.pone.0122156 Tsiafouli, 2015, Intensive agriculture reduces soil biodiversity across Europe, Glob. Chang. Biol., 21, 973, 10.1111/gcb.12752 Turner, 2013, Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants, ISME J., 7, 2248, 10.1038/ismej.2013.119 Uksa, 2014, Community structure of prokaryotes and their functional potential in subsoils is more affected by spatial heterogeneity than by temporal variations, Soil Biol. Biochem., 75, 197, 10.1016/j.soilbio.2014.04.018 Veerman, 2020 Vukicevich, 2016, Cover crops to increase soil microbial diversity and mitigate decline in perennial agriculture. A review, Agron. Sustain. Dev., 36, 1, 10.1007/s13593-016-0385-7 Wagg, 2019, Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning, Nat. Commun., 10, 1, 10.1038/s41467-019-12798-y Walder, 2017, Community profiling of Fusarium in combination with other plant-associated fungi in different crop species using SMRT sequencing, Front. Plant Sci., 8, 2019, 10.3389/fpls.2017.02019 Wayman, 2015, The influence of cover crop variety, termination timing and termination method on mulch, weed cover and soil nitrate in reduced-tillage organic systems, Renewable Agric. Food Syst., 30, 450, 10.1017/S1742170514000246 Weller, 2002, Microbial populations responsible for specific soil suppressiveness to plant pathogens, Annu. Rev. Phytopathol., 40, 309, 10.1146/annurev.phyto.40.030402.110010 Wick, 2017, 127 Wiesel, 2015, Determination of the optimal soil sample size to accurately characterise nematode communities in soil, Soil Biol. Biochem., 80, 89, 10.1016/j.soilbio.2014.09.026 Wollenweber, 2002, On the occurrence of exudate flavonoids in the borage family (Boraginaceae), Z. Naturforsch. C, 57, 445, 10.1515/znc-2002-5-607 Wydro, 2022, Soil microbiome study based on DNA extraction: a review, Water, 14, 10.3390/w14243999 Xiong, 2020, Rhizosphere protists are key determinants of plant health, Microbiome, 8, 1, 10.1186/s40168-020-00799-9 Yadav, 2018, Microbiome in crops: diversity, distribution, and potential role in crop improvement, 305 Yang, 2017, An integrated insight into the relationship between soil microbial community and tobacco bacterial wilt disease, Front. Microbiol., 8, 2179, 10.3389/fmicb.2017.02179 Yeoh, 2017, Evolutionary conservation of a core root microbiome across plant phyla along a tropical soil chronosequence, Nat. Commun., 8, 1, 10.1038/s41467-017-00262-8 Zhang, 2022, Leveraging functional traits of cover crops to coordinate crop productivity and soil health, J. Appl. Ecol., 59, 2627, 10.1111/1365-2664.14264 Zhao, 2021, Variation of rhizosphere microbial community in continuous mono-maize seed production, Sci. Rep., 11, 1 Zhou, 2017, Variation in soil microbial community structure associated with different legume species is greater than that associated with different grass species, Front. Microbiol., 8, 1007, 10.3389/fmicb.2017.01007 Zukalová, 2002, The role and effects of glucosinolates of Brassica species-a review, Rostlinna Vyroba, 48, 175