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In vitro elucidation of suppression effects of composts to soil-borne pathogen Phytophthora nicotianae on pepper plants using 16S amplicon sequencing and metaproteomics

Published online by Cambridge University Press:  25 September 2018

Margarita Ros ,
Josefa Blaya ,
Petr Baldrian ,
Felipe Bastida ,
Hans H Richnow ,
Nico Jehmlich  and
Jose Antonio Pascual
Margarita Ros*
Affiliation:
Department of Soil and Water Conservation, CEBAS-CSIC, Campus Universitario de Espinardo, Murcia30100, Spain
Josefa Blaya
Affiliation:
Department of Soil and Water Conservation, CEBAS-CSIC, Campus Universitario de Espinardo, Murcia30100, Spain
Petr Baldrian
Affiliation:
Laboratory of Environmental Microbiology, Institute of Microbiology of the CAs, Vídenská 1083, Praha 4 14220, Czech Republic
Felipe Bastida
Affiliation:
Department of Soil and Water Conservation, CEBAS-CSIC, Campus Universitario de Espinardo, Murcia30100, Spain
Hans H Richnow
Affiliation:
Department of Isotope Biogeochemistry, Helmholtz-Centre for Environmental Research – UFZ, Permoserstr. 15, Leipzig04318, Germany
Nico Jehmlich
Affiliation:
Department of Molecular Systems Biology, Helmholtz-Centre for Environmental Research – UFZ, Permoserstr. 15, Leipzig04318, Germany
Jose Antonio Pascual
Affiliation:
Department of Soil and Water Conservation, CEBAS-CSIC, Campus Universitario de Espinardo, Murcia30100, Spain
*
Author for correspondence: Margarita Ros, E-mail: [email protected]
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Abstract

Compost production is a critical component of organic waste management. One of the most important properties of compost is its ability to suppress soil-borne pathogens such as Phytophthora nicotianae in pepper plants. Both the physico-chemical and biological properties of composts can be responsible for the suppression of pathogens, although biological properties are the main driver. In this study, we analyzed composts with various levels of suppressiveness against P. nicotianae. We analyzed both physico-chemical properties like pH and electrical conductivity and biological properties like microbial activity, amplicon sequencing and metaproteomics. We believed that the link between community structures and proteins could provide deep insights into the mechanism of compost suppressiveness. Our results indicate that there are differences between suppressive and non-suppressive composts at the phylogenetic level (sequencing) and at the functional level (based on analysis of the cluster of orthologous groups, COGs). The proteins identified were assigned to the carbohydrate process, cell wall structure and inorganic ion transport and metabolism. Proteobacteria could also be new indicators of P. nicotianae suppression.

Keywords

CompostmetaproteomicsPhytophthora nicotianaesequencingsuppressive
Type
Research Paper
Information
Renewable Agriculture and Food Systems , Volume 35 , Issue 2 , April 2020 , pp. 206 - 214
Copyright
Copyright © Cambridge University Press 2018

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Footnotes

*

These authors contributed equally to this work.

References

Adetumbi, MA and Lau, BHS (1983) Allium sativum (garlic): a natural antibiotic. Medical Hypotheses 12, 227–237.CrossRefGoogle ScholarPubMed
Aronesty, E (2013) Comparison of sequencing utility programs. Open Bioinformatics Journal 7, 1–8.CrossRefGoogle Scholar
Bastida, F, Hernández, T and Garcia, C (2014) Metaproteomics of soils from semiarid environment: functional and phylogenetic information obtained with different protein extraction methods. Journal of Proteomics 101, 31–42.CrossRefGoogle ScholarPubMed
Bastida, F, Selevsek, N, Torres, IF, Hernandez, T and Garcia, C (2015) Soil restoration with organic amendments: linking cellular functionality and ecosystem processes. Scientific Reports 5, 15550.CrossRefGoogle ScholarPubMed
Bastida, F, Torres, IF, Moreno, JL, Baldrian, P, Ondoño, S, Ruiz-Navarro, A, Hernandez, T, Richnow, HH, Starke, R, García, C and Jehmlich, N (2016) The active microbial diversity drives ecosystem multifunctionality and is physiologically related to carbon availability in Mediterranean semi-arid soils. Molecular Ecology 25, 4660–4673.CrossRefGoogle ScholarPubMed
Blaya, J, Lloret, E, Ros, M and Pascual, J (2015) Identification of predictor parameters to determine agro-industrial compost suppressiveness against Fusarium oxysporum and Phytophthora capsici diseases in muskmelon and pepper seedlings. Journal of the Science of Food and Agriculture 95, 1482–1490.CrossRefGoogle ScholarPubMed
Blaya, J, Marhuenda, F, Pascual, J and Ros, M (2016) Microbiota characterization of compost using omics approaches opens new perspectives for Phytophthora root rot control. PLoS ONE 11, e0158048.CrossRefGoogle ScholarPubMed
Bonanomi, G, Antignani, V, Capodilupo, M and Scala, F (2010) Identifying the characteristics of organic soil amendments that suppress soilborne plant diseases. Soil Biology and Biochemistry 42, 136–144.CrossRefGoogle Scholar
Caporaso, JG, Lauber, CL, Walters, WA, Berg-Lyons, D, Huntley, J, Fierer, N, Owens, SM, Betley, J, Fraser, L, Bauer, M, Gormley, N, Gilbert, JA, Smith, G and Knight, R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME Journal 6, 1621–1624.CrossRefGoogle ScholarPubMed
Carini, P, Marsden, PJ, Leff, JW, Morgan, EE, Strickland, MS and Fierer, N (2016) Relic DNA is abundance in soil and obscures estimates of soil microbial diversity. Nature Microbiology 2, 16242.CrossRefGoogle Scholar
Castaño, R, Borreo, C and Aviles, M (2011) Organic matter fractions by SP-MAS 13C NMR and microbial communities involved in the suppression of Fusarium wilting organic growth media. Biological Control 58, 286–293.CrossRefGoogle Scholar
Chourey, K, Jansson, J, VerBerkmoes, N, Shah, M, Chavarria, KL, Tom, LM, Brodie, EL and Hettich, RL (2010) Direct cellular lysis/protein extraction protocol for soil metaproteomics. Journal of Proteome Research 9, 6615–6622.CrossRefGoogle ScholarPubMed
Cole, JR, Wang, Q, Fish, JA, Chai, B, McGarrell, DM, Sun, Y, Brown, CT, Porras-Alfaro, A, Kuske, CR and Tiedje, JM (2014) Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Research 42, D633–D642.CrossRefGoogle ScholarPubMed
Danon, M, Franke-Whittle, IH, Insam, H, Chen, Y and Hadar, Y (2008) Molecular analysis of bacterial community succession during prolonged compost curing. FEMS Microbiology Ecology 65, 133–144.CrossRefGoogle ScholarPubMed
de Gannes, V, Eudoxie, G and Hickey, WJ (2013) Prokaryotic successions and diversity in composts as revealed by 454-pyrosequencing. Bioresource Technology 133, 573–580.CrossRefGoogle ScholarPubMed
Edgar, RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics (Oxford, England) 26, 2460–2461.CrossRefGoogle ScholarPubMed
Edgar, RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods 10, 996–998.CrossRefGoogle ScholarPubMed
Garcia, C, Hernandez, T, Costa, F, Cecanti, B and Masciandaro, G (1993) Dehydrogenase activity of soil as an ecological marker in processes of perturbed system regeneration. In Gallardp-Lancho, J (ed.), Proceedings of the XI International Symposium of Environmental Biogeochemistry. Salamanca, España: CSIC, pp. 89–100.Google Scholar
García, C, Roldán, A and Hernández, T (1997) Changes in microbial activity alter abandonment of cultivation in a semiarid Mediterranean environment. Journal of Environmental Quality 26, 285–291.CrossRefGoogle Scholar
Gonzalez-Sanchez, MA, Perez-Jimenez, RM, Pliego, C, Ramos, C, de Vicente, A and Cazorla, FM (2010) Biocontrol bacteria selected by a direct plant protection strategy against avocado white root rot show antagonism as a prevalent trait. Journal of Applied Microbiology 109, 65–78.Google ScholarPubMed
Gopalakrishnan, S, Srinivas, V, Alekhya, G, Prakash, B, Kudapa, H, Rathore, A and Varshney, RK (2015) The extent of grain yield and plant growth enhancement by plant growth-promoting broad-spectrum Streptomyces sp. in chickpea. SpringerPlus 4, 31.CrossRefGoogle ScholarPubMed
Hadar, Y and Papadopoulou, KK (2012) Suppressive composts: microbial ecology links between abiotic environments and healthy plants. Annual Review of Phytopathology 50, 133–153.CrossRefGoogle ScholarPubMed
Haug, RT (1993) The Practical Handbook of Compost Engineering. Boca Raton, FL: Lewis Publishers, 717 pages.Google Scholar
Hoitink, H and Boehm, M (1999) Biocontrol within the context of soil microbial communities: a substrate-dependent phenomenon. Annual Review of Phytopathology 37, 427–446.CrossRefGoogle ScholarPubMed
Hoitink, HAJ and Fahy, PC (1986) Basis for the control of soilborne plant-pathogens with composts. Annual Review of Phytopathology 24, 93–114.CrossRefGoogle Scholar
Hoitink, HAJ and Grebus, ME (1997) Composts and the control of plant disease. In Hayes, MHB and Wilson, WS (eds), Humic Substances in Soil, Peats and Waters: Health and Environmental Aspects. Cambridge, UK: Royal Society of Chemistry, pp. 359–366.CrossRefGoogle Scholar
Ihrmark, K, Bödeker, IT, Cruz-Martinez, K, Friberg, H, Kubartova, A, Schenck, J, Strid, Y, Stenlid, J, Brandström-Durling, M, Clemmensen, KE and Lindahl, BD (2012) New primers to amplify the fungal ITS2 region evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiology Ecology 82, 666–677.CrossRefGoogle ScholarPubMed
Ishii, K and Takii, S (2003) Comparison of microbial communities in four different composting processes as evaluated by denaturing gradient gel electrophoresis analysis. Journal of Applied Microbiology 95, 109–119.CrossRefGoogle ScholarPubMed
Jehmlich, N, Schmidt, F, Von Bergen, M, Richnow, HH and Vogt, C (2008) Protein-based stable isotope probing (Protein-SIP) reveals active species within anoxic mixed cultures. ISME Journal 2, 1122–1133.CrossRefGoogle ScholarPubMed
Kersters, K, De Vos, P, Gillis, M, Swings, J, Vandamme, P and Stackebrandt, E (2006) Introduction to the Proteobacteria. In: Dwarkin, M, Falkow, S, Rosenberg, E, Schleifer, K-H, Stackebrandt, E (eds), The Prokaryotes, 3rd Edn. vol. 5. New York: Springer, pp. 3–37.CrossRefGoogle Scholar
Koljalg, U, Nilsson, RH, Abarenkov, K, Tedersoo, L, Taylor, FS, Bahram, M, Bates, ST, Bruns, TD, Bengtsson-Palme, J, Callaghan, TM, Douglas, B, Drenkhan, T, Eberhardt, U, Dueñas, M, Grebenc, T, Griffith, GW, Hartmann, M, Kirk, PM, Kohout, P, Larsson, E, Lindahl, BD, Lücking, R, Martín, MP, Matheny, PB, Nguyen, NH, Niskanen, T, Oja, J, Peay, KG, Peintner, U, Peterson, M, Põldmaa, K, Saag, L, Saar, I, Schüßler, A, Scott, JA, Senés, C, Smith, ME, Suija, A, Taylor, DL, Telleria, MT and Weiss, M (2013) Towards a unified paradigm for sequence-based identification of fungi. Molecular Ecology 22, 5271–5277.CrossRefGoogle ScholarPubMed
Kurtboke, DI (2012) Biodiscovery from rare actinomycetes: an ecotaxonomical perspective. Applied Microbiology and Biotechnology 93, 1843–1852.CrossRefGoogle ScholarPubMed
Laemmli, BUK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.CrossRefGoogle ScholarPubMed
Lemaire, F, Dartigues, A and Rivière, LM (1985) Properties of substrate made with spent mushroom compost. Acta Horticulturae 172, 13–29.CrossRefGoogle Scholar
Liu, D, Li, M and XI, B (2015) Metaproteomics reveals major microbial players and their biodegradation functions in a large-scale aerobic composting plant. Microbial Biotechnology 8, 950–960.CrossRefGoogle Scholar
Martin, CCG and Brathwaite, RAI (2012) Compost and compost tea: principles and prospects as substrates and soil-borne disease management strategies in soil-less vegetable production. Biological Agriculture and Horticulture 28, 1–33.CrossRefGoogle Scholar
Mehta, CM, Yu, D, Srivastava, R, Sinkkonen, A, Kurola, JM, Gupta, V, Jääskeläinen, H, Palni, U, Sharma, AK and Romantschuk, M (2016) Microbial diversity and bioactive substances in disease suppressive composts from India. Compost Science and Utilization 24, 105–116.CrossRefGoogle Scholar
Mengesha, WK, Gill, WM, Powell, SM, Evans, KJ and Bary, KM (2017) A study of selected factors affecting efficacy of compost tea against several fungal pathogens of potato. Journal of Applied Microbiology 123, 732–747.CrossRefGoogle ScholarPubMed
Morales, AB, Ros, M, Ayuso, LM, Bustamante, MA, Moral, R and Pascual, JA (2017) Agroindustrial composts to reduce the use of peat and fungicides in the cultivation of muskmelon seedlings. Journal of the Science of Food and Agriculture 97, 875–881.CrossRefGoogle ScholarPubMed
Neher, DA, Weicht, TR, Bates, ST, Leff, JW and Fierer, N (2013) Changes in bacterial and fungal communities across compost recipes, preparation and composting times. PLoS One 8, e79512.CrossRefGoogle ScholarPubMed
Nilsson, RH, Veldre, V, Hartmann, M and Kristiansson, E (2010) An open source software package for automated extraction of ITS1 and ITS2 from fungal ITS sequences for use in high-throughput community assays and molecular ecology. Fungal Ecology 3, 284–287.CrossRefGoogle Scholar
Ntougias, S, Papadopoulou, KK and Zervakis, GI (2008) Suppression of soil-borne pathogens of tomato by composts derived from agro-industrial wastes abundant in Mediterranean regions. Biology and Fertility of Soils 44, 1081–1090.CrossRefGoogle Scholar
Partanen, P, Hultman, J, Paulin, L, Auvinen, P and Romantschuk, M (2010) Bacterial diversity at different stages of the composting process. BMC Microbiology 10, 94.CrossRefGoogle ScholarPubMed
Postma, J, Sheper, RWA and Schilder, MT (2010) Effect of successive cauliflower plantings and Rhizoctonia solani AG 2-1 inoculations on disease suppressiveness of a suppressive and conducive soil. Soil Biology and Biochemistry 42, 804–812.CrossRefGoogle Scholar
Rynk, R (1992) On-farm Composting Handbook (NRAES-54). Ithaca, NY: Northeast Regional Agricultural Engineering Service.Google Scholar
Schneider, T, Keblinger, KM, Schmid, E, Sterflinger-Gleixner, K, Ellersdorfer, G, Roschitzki, B, Richter, A, Eberl, L, Zechmeister-Boltenstern, S and Riedel, K (2012) Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions. ISME Journal 6, 1749–1762.CrossRefGoogle ScholarPubMed
Stackebrandt, E and Ebers, J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiology Today 33, 152–155.Google Scholar
Sullivan, DM and Miller, RO (2000) Compost, quality attributes measurements and variability. In Stoffella, PJ and Kahn, BA (eds), Compost Utilization in Horticultural Cropping Systems. Boca Raton, FL: CRC Press, pp. 95–120.Google Scholar
Thinggaard, K and Andersen, H (1995) Influence of watering frequency and electrical conductivity of the nutrient solution on Phytophthora root rot in pot plants of Gerbera. Plant Disease 79, 259–263.CrossRefGoogle Scholar
Tian, B, Yang, J and Zhang, KQ (2007) Bacteria used in the biological control of plant-parasitic nematodes: populations, mechanisms of action, and future prospects. FEMS Microbiology Ecology 61, 197–213.CrossRefGoogle ScholarPubMed
Větrovský, T and Baldrian, P (2013) Analysis of soil fungal communities by amplicon pyrosequencing: current approaches to data analysis and the introduction of the pipeline SEED. Biology and Fertility of Soils 49, 1027–1037.CrossRefGoogle Scholar
Wilmes, P and Bond, PL (2006) Metaproteomics: studying functional gene expression in microbial ecosystems. Trends in Microbiology 14, 92–97.CrossRefGoogle ScholarPubMed
Yu, D, Sinkkonen, A, Hui, N, Kurola, JM, Kukkonen, S, Parikka, P, Vestberg, M and Romantschuk, M (2015) Molecular profile of microbiota of Finnish commercial compost suppressive against Pythium disease on cucumber plants. Applied Soil Ecology 92, 47–53.CrossRefGoogle Scholar
Žifčáková, L, Větrovský, T, Howe, A and Baldrian, P (2016) Microbial activity in forest soil reflects the changes in ecosystem properties between summer and winter. Environmental Microbiology 18, 288–301.CrossRefGoogle ScholarPubMed
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