Hostname: page-component-76fb5796d-zzh7m Total loading time: 0 Render date: 2024-04-26T04:06:50.379Z Has data issue: false hasContentIssue false
  • English
  • Français

Can repeated soil amendment with biogas digestates increase soil suppressiveness toward non-specific soil-borne pathogens in agricultural lands?

Published online by Cambridge University Press:  17 December 2020

L. M. Manici Open the ORCID record for L. M. Manici [Opens in a new window] ,
F. Caputo Open the ORCID record for F. Caputo [Opens in a new window] ,
G. A. Cappelli Open the ORCID record for G. A. Cappelli [Opens in a new window]  and
E. Ceotto Open the ORCID record for E. Ceotto [Opens in a new window]
L. M. Manici*
Affiliation:
Council of Agricultural Research and Economics (CREA), Research Centre of Agriculture and Environment, Via di Corticella 133, 40128Bologna, Italy
F. Caputo
Affiliation:
Council of Agricultural Research and Economics (CREA), Research Centre of Agriculture and Environment, Via di Corticella 133, 40128Bologna, Italy
G. A. Cappelli
Affiliation:
Council of Agricultural Research and Economics (CREA), Research Centre of Agriculture and Environment, Via di Corticella 133, 40128Bologna, Italy
E. Ceotto
Affiliation:
Council of Agricultural Research and Economics (CREA), Research Centre of Agriculture and Environment, Via di Corticella 133, 40128Bologna, Italy
*
Author for correspondence: L. M. Manici, E-mail: luisamaria.manici@crea.gov.it
Get access Rights & Permissions [Opens in a new window]

Abstract

Soil suppressiveness which is the natural ability of soil to support optimal plant growth and health is the resultant of multiple soil microbial components; which implies many difficulties when estimating this soil condition. Microbial benefits for plant health from repeated digestate applications were assessed in three experimental sites surrounding anaerobic biogas plants in an intensively cultivated area of northern Italy. A 2-yr trial was performed in 2017 and 2018 by performing an in-pot plant growth assay, using soil samples taken from two fields for each experimental site, of which one had been repeatedly amended with anaerobic biogas digestate and the other had not. These fields were similar in management and crop sequences (maize was the recurrent crop) for the last 10 yr. Plant growth response in the bioassay was expressed as plant biomass production, root colonization frequency by soil-borne fungi were estimated to evaluate the impact of soil-borne pathogens on plant growth, abundance of Pseudomonas and actinomycetes populations in rhizosphere were estimated as beneficial soil microbial indicators. Repeated soil amendment with digestate increased significantly soil capacity to support plant biomass production as compared to unamended control in both the years. Findings supported evidence that this increase was principally attributable to a higher natural ability of digestate-amended soils to reduce root infection by saprophytic soil-borne pathogens whose inoculum was increased by the recurrent maize cultivation. Pseudomonas and actinomycetes were always more abundant in digestate-amended soils suggesting that both these large bacterial groups were involved in the increase of their natural capacity to control soil-borne pathogens (soil suppressiveness).

Keywords

Actinomycetescrop legacyin-pot bioassaymaizePseudomonassoil-borne pathogenswaste recycling
Type
Research Paper
Information
Renewable Agriculture and Food Systems , Volume 36 , Issue 4 , August 2021 , pp. 353 - 364
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bailey, VL, Smith, JL and Bolton, H (2002) Fungal-to-bacterial ratios in soils investigated for enhanced C sequestration. Soil Biology and Biochemistry 34, 997–1007.CrossRefGoogle Scholar
Barbero, S, Zaccagnino, SM, Mariani S, , Lastoria B, Braca G, Bussettini M, Casaioli M, Marsico L, Rotundo R, Pavan V, Ricciardi G, Zenoni E, Cicogna A, Micheletti S, Cazzuli O, Di Priolo S, Ranci M, Rondanini C, Bianco G, Egiatti G, Montanini P, Saccardo I, Campione E, Pupillo S, Locca F, Lazzeri M, Tedeschini M, Marzano V, Schena P, Licciardello A, Manzella F, Brunier F and Ratto S (2017) Linee guida per il controllo di validità dei dati idro-meteorologici. (Guidelines for the quality check of hydrometeorological data). Available at Website https://www.certifico.com/component/attachments/download/5512.Google Scholar
Barzee, TJ, Edalati, A, El-Mashad, H, Wang, D, Scow, K and Zhang, R (2019) Digestate biofertilizers support similar or higher tomato yields and quality than mineral fertilizer in a subsurface drip fertigation system. Frontiers in Sustainable Food Systems 3, 58.CrossRefGoogle Scholar
Bhatti, AA, Haq, S and Bhat, RA (2017) Actinomycetes benefaction role in soil and plant health. Microbial Pathogenesis 111, 458–467.CrossRefGoogle ScholarPubMed
Bongiorno, G, Postma, J, Bünemann, EK, Brussaard, L, de Goede, RGM, Mäder, P, Tamm, L and Thuerig, B (2019) Soil suppressiveness to Pythium ultimum in ten European long-term field experiments and its relation with soil parameters. Soil Biology and Biochemistry 133, 174–187.CrossRefGoogle Scholar
Borrelli, L, Castelli, F, Ceotto, E, Cabassi, G and Tomasoni, C (2014) Maize grain and silage yield and yield stability in a long-term cropping system experiment in northern Italy. European Journal of Agronomy 55, 12–19.CrossRefGoogle Scholar
Broadbent, P and Baker, KF (1974) Behaviour of Phytophthora cinnamomi in soils suppressive and conducive to root rot. Australian Journal of Agricultural Research 25, 121–137.CrossRefGoogle Scholar
Bustin, SA, Benes, V, Garson, JA, Hellemans, J, Huggett, J, Kubista, M, Mueller, R, Nolan, T, Pfaffl, MW, Shipley, GL, Vandesompele, J and Wittwer, CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 55, 611–622.CrossRefGoogle ScholarPubMed
Capponi, S and Barbanti, L (2010) Utilizzo agronomico del digestato. Normative regionali a confronto.Terra e Vita 25, Supplemento Fertilizzare Oggi.Google Scholar
Carrosio, G (2011) La produzione di energia da biogas nelle campagne italiane: un'analisi neo-istituzionale. Agriregionieuropa 7, 54.Google Scholar
Chambers, KR (1987) Epidemiology of maize root rot in South Africa. Journal of Phytopathology 118, 84–93.CrossRefGoogle Scholar
Chen, J, Wu, L, Xiao, Z, Wu, Y, Wu, H, Qin, X, Wang, J, Wei, X, Khan, MU, Lin, S and Lin, W (2017) Assessment of the diversity of Pseudomonas spp. and Fusarium spp. in Radix pseudostellariae rhizosphere under monoculture by combining DGGE and quantitative PCR. Frontiers in Microbiology 8, 1748.CrossRefGoogle ScholarPubMed
Chiew, YL, Spångberg, J, Baky, A, Hansson, PA and Jönsson, H (2015) Environmental impact of recycling digested food waste as a fertilizer in agriculture—a case study. Resources, Conservation and Recycling 95, 1–14.CrossRefGoogle Scholar
Ciampitti, I (2016) New corn growth and development poster from K-State. Agronomy eUpdate - Kansas State University. Manhattan, KS, USA. Available at Website https://webapp.agron.ksu.edu/agr_social/m_eu_article.throck?article_id=1010.Google Scholar
Consorzio Italiano Biogas (2017) Lo sviluppo del biometano: un'opzione sostenibile per l'economia e per l'ambinete. [Internet]. Available at Website https://www.consorziobiogas.it/wp-content/uploads/2017/03/LA-BIOGAS-REFINERY-NELLA-TRANSIZIONE-ENERGETICA-ITALIANA_SINTESI-marzo-2017.pdf.Google Scholar
Cook, RJ and Baker, KF (1983) The nature and practice of biological control of plant pathogens. American Phytopathological Society (APS), St. Paul, MN, USA. pp. 539.Google Scholar
Crawford, DL, Lynch, JM, Whipps, JM and Ousley, MA (1993) Isolation and characterization of actinomycete antagonists of a fungal root pathogen. Applied and Environmental Microbiology 59, 3899–3905.CrossRefGoogle ScholarPubMed
De Corato, U (2020) Disease-suppressive compost enhances natural soil suppressiveness against soil-borne plant pathogens: a critical review. Rhizosphere 13, 100192.CrossRefGoogle Scholar
Dignam, BEA, O'Callaghan, M, Condron, LM, Raaijmakers, JM, Kowalchuk, GA and Wakelin, SA (2019) Impacts of long-term plant residue management on soil organic matter quality, Pseudomonas community structure and disease suppressiveness. Soil Biology and Biochemistry 135, 396–406.CrossRefGoogle Scholar
El-Tarabily, KA and Sivasithamparam, K (2006) Non-streptomycete actinomycetes as biocontrol agents of soil-borne fungal plant pathogens and as plant growth promoters. Soil Biology and Biochemistry 38, 1505–1520.CrossRefGoogle Scholar
Emilia Romagna, R (2013) Le zone vulnerabili ai nitrati (ZVN) in Emilia-Romagna—agricoltura, caccia e pesca. Available at Website https://agricoltura.regione.emilia-romagna.it/produzioni-agroalimentari/temi/bio-agro-climambiente/effluenti-e-nitrati-1/le-zone-vulnerabili-ai-nitrati-zvn-in-emilia-romagna.Google Scholar
ERSAF (2013) Le Zone Vulnerabili ai Nitrati. Carta delle Zone Vulnerabili ai Nitrati. Avaialble at Website https://www.ersaf.lombardia.it/it/servizi-al-territorio/nitrati/normativa/regione-lombardia.Google Scholar
European Parliament and the Council of the European Union (2015) Directive (EU) 2015/1513 of the European Parliament and of the Council of 9 September 2015 amending Directive 98/70/EC relating to the quality of petrol and diesel fuels and amending Directive 2009/28/EC on the promotion of the use of energy from renewable sources. Official Journal of The European Union L239, September 2015, 1-29.Google Scholar
Fierer, N and Jackson, RB (2006) The diversity and biogeography of soil bacterial communities. Proceedings of the National Academy of Sciences of the United States of America 103, 626–631.CrossRefGoogle ScholarPubMed
Franke-Whittle, IH, Juárez, MFD, Insam, H, Schweizer, S, Naef, A, Topp, AR, Kelderer, M, Rühmer, T, Baab, G, Henfrey, J and Manici, LM (2020) Performance evaluation of locally available composts to reduce replant disease in apple orchards of central Europe. Renewable Agriculture and Food Systems 34, 543–557.CrossRefGoogle Scholar
Ganeshan, G and Kumar, AM (2005) Pseudomonas fluorescens, a potential bacterial antagonist to control plant diseases. Journal of Plant Interaction 1, 123–134.CrossRefGoogle Scholar
Ghini, R, Patrício, FRA, Bettiol, W, de Almeida, IMG, de H, A and Maia, N (2007) Effect of sewage sludge on suppressiveness to soil-borne plant pathogens. Soil Biology and Biochemistry 39, 2797–2805.CrossRefGoogle Scholar
Ghorbani-Nasrabadi, R, Greiner, R, Alikhani, AH, Hamedi, J and Yakhchali, B (2013) Distribution of actinomycetes in different soil ecosystems and effect of media composition on extracellular phosphatase activity. Journal of Soil Science and Plant Nutrition 13, 223–236.Google Scholar
Hammer, Ø, Harper, DAT and Ryan, PD (2001) Past: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4, 9.Google Scholar
Heuer, H, Krsek, M, Baker, P, Smalla, K and Wellington, EM (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Applied Environmental Microbiology 63, 3233–3241.CrossRefGoogle ScholarPubMed
Karst, J, Gaster, J, Wiley, E and Landhäusser, SM (2017) Stress differentially causes roots of tree seedlings to exude carbon. Tree Physiology 37, 154–164.Google ScholarPubMed
Koenning, SR, Frye, JW, Pataky, JK, Gibbs, M and Cotton, D (2007) First report of Phoma terrestris causing red root rot on sweet corn (Zea mays) in north Carolina. Plant Disease 91, 1054–1054.CrossRefGoogle Scholar
Latz, E, Eisenhauer, N, Rall, BC, Scheu, S and Jousset, A (2016) Unravelling linkages between plant community composition and the pathogen-suppressive potential of soils. Scientific Reports 6, 1–10.CrossRefGoogle ScholarPubMed
Launay, M and Guérif, M (2003) Ability for a model to predict crop production variability at the regional scale: an evaluation for sugar beet. Agronomie 23, 135–146.CrossRefGoogle Scholar
Lević, J, Petrović, T, Stanković, S, Krnjaja, V and Stanković, G (2011) Frequency and incidence of Pyrenochaeta terrestris in root internodes of different maize hybrids. Journal of Phytopathology 159, 424–428.Google Scholar
Manici, LM and Bonora, P (2007) Molecular genetic variability of Italian binucleate Rhizoctonia spp. Isolates from strawberry. European Journal of Plant Pathology 118, 31–42.CrossRefGoogle Scholar
Manici, LM and Caputo, F (2010) Soil fungal communities as indicators for replanting new peach orchards in intensively cultivated areas. European Journal of Agronomy 33, 188–196.CrossRefGoogle Scholar
Manici, LM and Caputo, F (2020) Growth promotion of apple plants is the net effect of binucleate Rhizoctonia sp. as rhizosphere-colonizing fungus. Rhizosphere 13, 100185.CrossRefGoogle Scholar
Manici, LM, Saccà, ML, Caputo, F, Zanzotto, A, Gardiman, M and Fila, G (2017) Long-term grapevine cultivation and agro-environment affect rhizosphere microbiome rather than plant age. Applied Soil Ecology 119, 214–225.CrossRefGoogle Scholar
Manici, LM, Caputo, F, Nicoletti, F, Leteo, F and Campanelli, G (2018) The impact of legume and cereal cover crops on rhizosphere microbial communities of subsequent vegetable crops for contrasting crop decline. Biological Control 120, 17–25.CrossRefGoogle Scholar
Mazurier, S, Corberand, T, Lemanceau, P and Raaijmakers, JM (2009) Phenazine antibiotics produced by fluorescent pseudomonads contribute to natural soil suppressiveness to Fusarium wilt. ISME Journal 3, 977–991.CrossRefGoogle ScholarPubMed
Mazzola, M (2002) Mechanisms of natural soil suppressiveness to soilborne diseases. Antonie van Leeuwenhoek 81, 557–564.CrossRefGoogle ScholarPubMed
Mendes, R, Kruijt, M, De Bruijn, I, Dekkers, E, Van Der Voort, M, Schneider, JHM, Piceno, YM, DeSantis, TZ, Andersen, GL, Bakker, PAHM and Raaijmakers, JM (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science (New York, N.Y.) 332, 1097–1100.CrossRefGoogle ScholarPubMed
MIPAAF (2016) Criteri e norme tecniche generali per la disciplina regionale dell'utilizzazione agronomica degli effluenti di allevamento e delle acque reflue, nonche’ per la produzione e l'utilizzazione agronomica del digestato. Gazzetta Ufficiale. (GU Serie Generale no. 90 del 18-04-2016 - Suppl. Ordinario no. 9) [Internet]. Available at website https://www.gazzettaufficiale.it/eli/id/2016/04/18/16A02762/sg.Google Scholar
Molinari, F and Donati, F (2015) Valutazione del potenziale energetico ed economico dei residui colturali in Italia. Agriregionieuropa 11, 41.Google Scholar
Monteny, GJ (2001) The EU nitrates directive: a European approach to combat water pollution from agriculture. The Scientific World Journal 1, 927–935.CrossRefGoogle ScholarPubMed
Munkvold, GP and White, DG (2015) Infectious diseases. In: Munkvold GP and White DG (ed.), Compendium of Corn Diseases Fourth Edi. St. Paul, MN, USA: American Phytopathology Society. p. 7–130.Google Scholar
Musacchio, A, Re, V, Mas-Pla, J and Sacchi, E (2020) EU Nitrates directive, from theory to practice: environmental effectiveness and influence of regional governance on its performance. Ambio 49, 504–516.CrossRefGoogle ScholarPubMed
Muyzer, G, De Waal, E and Uitterlinden, AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction amplified genes coding for 16S rRNA. Applied Environmental Microbiology 59, 695–700.CrossRefGoogle ScholarPubMed
Neiendam Nielsen, A and Winding, M (2002) Microorganisms as indicators of soil health. NERI Technical Report No. 388.Google Scholar
Neiendam Nielsen, M, Winding, A, Svend, B, Hansen, BM, Hendriksen, NB and Kroer, N (2002) Microorganisms as indicators of soil health. NERI Technical Report No. 388. National Environmental Research Institute, Denmark.Google Scholar
Newby, DL, Carroll, RB and Whittington, DP (1997) Incidence of Phoma terrestris, causal agent of red root rot, in corn roots and soil in Delaware and on the eastern shore of Maryland. Plant Disease 81, 232.CrossRefGoogle Scholar
Nkoa, R (2014) Agricultural benefits and environmental risks of soil fertilization with anaerobic digestates: a review. Agronomy for Sustainable Development 34, 473–492.CrossRefGoogle Scholar
Novik, G, Savich, V and Kiselev, E (2015) An insight into beneficial Pseudomonas bacteria. In Microbiology in Agriculture and Human Health InTech. London, UK: IntechOpen, pp. 132.Google Scholar
Nübel, U, Engelen, B, Felske, A, Snaidr, J, Wieshuber, A, Amann, RI, Ludwig, W and Backhaus, H (1996) Sequence heterogeneities of genes encoding 16SrRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis. Journal of Bacteriology 178, 5636–5643.CrossRefGoogle Scholar
Oldfield, EE, Bradford, MA and Wood, SA (2019) Global meta-analysis of the relationship between soil organic matter and crop yields. Soil 5, 15–32.CrossRefGoogle Scholar
Patten, CL and Glick, BR (2002) Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Applied and Environmental Microbiology 68, 3795–3801.CrossRefGoogle ScholarPubMed
Peel, MC, Finlayson, BL and McMahon, TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Sciences 11, 1633–1644.CrossRefGoogle Scholar
Podmirseg, SM, Waldhuber, S, Knapp, BA, Insam, H and Goberna, M (2019) Robustness of the autochthonous microbial soil community after amendment of cattle manure or its digestate. Biology and Fertility of Soils 55, 565–576.CrossRefGoogle Scholar
Saccà, ML, Manici, LM, Caputo, F and Frisullo, S (2019) Changes in rhizosphere bacterial communities associated with tree decline: Grapevine esca syndrome case study. Canadian Journal of Microbiology 65, 930–943.CrossRefGoogle ScholarPubMed
Saxton, KE, Rawls, WJ, Romberger, JS and Papendick, RI (1986) Estimating generalized soil-water characteristics from texture. Soil Science Society of America Journal 50, 1031–1036.CrossRefGoogle Scholar
Schlatter, D, Kinkel, L, Thomashow, L, Weller, D and Paulitz, T (2017) Disease suppressive soils: new insights from the soil microbiome. Phytopathology 107, 1284–1297.CrossRefGoogle ScholarPubMed
Shipton, PJ (1977) Monoculture and soilborne plant pathogens. Annual Review of Phytopathology 15, 387–407.CrossRefGoogle Scholar
Song, F, Han, X, Zhu, X and Herbert, SJ (2012) Response to water stress of soil enzymes and root exudates from drought and non-drought tolerant corn hybrids at different growth stages. Canadian Journal of Soil Science 92, 501–507.CrossRefGoogle Scholar
Tambone, F, Scaglia, B, D'Imporzano, G, Schievano, A, Orzi, V, Salati, S and Adani, F (2010) Assessing amendment and fertilizing properties of digestates from anaerobic digestion through a comparative study with digested sludge and compost. Chemosphere 81, 577–583.CrossRefGoogle ScholarPubMed
Vitti, C, Stellacci, AM, Leogrande, R, Mastrangelo, M, Cazzato, E and Ventrella, D (2016) Assessment of organic carbon in soils: a comparison between the Springer–Klee wet digestion and the dry combustion methods in Mediterranean soils (Southern Italy). CATENA 137, 113–119.CrossRefGoogle Scholar
Yang, Y, Zuzak, K, Harding, M, Neilson, E, Feindel, D and Feng, J (2017) First report of pink root rot caused by Setophoma (Pyrenochaeta) terrestris on canola. Canadian Journal of Plant Pathology 39, 354–360.CrossRefGoogle Scholar
Supplementary material: Image

Manici et al. supplementary material

Manici et al. supplementary material

Download Manici et al. supplementary material(Image)
Image 70.8 KB