Vinasse and straw retention decrease fungal diversity and pathogenicity in sugarcane soil / Aplicação de vinhaça e retenção de palha diminuem a diversidade e patogenicidade de fungos em solo canavieiro

Victoria Romancini Toledo, Rita de Cássia Félix Alvarez, Eiko Eurya Kuramae, Mattias de Hollander, Raffaella Rossetto, Elisângela de Souza Loureiro, Paulo Eduardo Teodoro, Gisele Herbst Vazquez, Juliana Heloisa Pinê Américo Pinheiro, Siu Mui Tsai, Acacio Aparecido Navarrete

Abstract


This study focused on the effects of vinasse (V), a by-product of the sugar-ethanol industry, combined with mineral nitrogen fertilizer (N) and straw retention on the fungal community diversity, composition, and structure in a sugarcane-cultivated soil. The experiment consisted of a combination of V, mineral N and sugarcane-straw blanket. Soil samples were collected at 7, 157, and 217 days after planting, corresponding to maximum carbon dioxide emissions from soil after three repeated applications of fertilizers into the soil. Across 57 soil metagenomics datasets, it was revealed that the application the V in combination with N fertilizer and straw retention decreased the diversity, evenness and richness of fungi at the community level in soil. Analysis of the soil fungal community composition based on the 20 genera most abundant revealed decrease for Blastomyces, Melampsora, and Penicillium after the third application of V in combination with N fertilizer and straw blanket. An opposite response was revealed for Amauroascus, Cantharellus, Chrysosporium, Clavaria, Morchella, Puccinia, and Tuber in soil under this treatment. Shifts in fungal community composition were followed by increases in mycorrhizal and decomposers soil-borne fungi and decrease in potentially pathogenic fungi, but not by changes in community structure. Based on these results, it is possible to attest that repeated applications of V in combination with N fertilizer and sugarcane-straw blankets affect ecological aspects of the soil fungal community composition and potential functions played by fungi in sugarcane soil, which are essentials to ecosystem function and sustainable management of agricultural ecosystems.


Keywords


decomposer fungi, fungal community, mycorrhizal fungi, shotgun metagenome, sustainability

References


Aime MC, McTaggart AR, Mondo SJ, Duplessis S (2017) Chapter Seven - Phylogenetics and Phylogenomics of Rust Fungi. Adv Genet 100:267-307.

Alves TS, Campos LL, Neto NE et al (2011) Biomassa e atividade microbiana de solo sob vegetação nativa e diferentes sistemas de manejos. Acta Sci Agron 33:341-347. https://doi.org/10.4025/actasciagron.v33i2.4841

Asea PEA, Kucely J, Stewart WB (1988) Inorganic phosphate solubilization by two Penicillium species in solution culture and soil. Soil Biol Biochem 20(4):454-464.

Assis EPM, Cordeiro MAS, Paulino HB, Carneiro MAC (2003) Efeito da aplicação de nitrogênio na atividade microbiana e na decomposição da palhada de sorgo em solo de cerrado sob plantio direto. PAT 33:107-112.

Azevedo LCB (2008) Comunidades de Fungos Micorrízicos Arbusculares no solo e raízes de cana-de-açúcar. Dissertação, Escola Superior de Agricultura Luiz de Queiroz.

Barbieri R, Carvalho IF (2001) Coevolução de plantas e fungos patogênicos. Rev Bras Agrociência 7:79-83.

Barreto PAB, Gama-Rodrigues EF, Gama-Rodrigues AC, et al (2008) Atividade microbiana, carbono e nitrogênio da biomassa microbiana em plantações de eucalipto, em sequência de idades. Rev Bras Ciênc Solo 32:611-619. https://doi.org/10.1590/S0100-06832008000200016

Bödeker ITM, Lindahl BD, Olson  et a (2016). Mycorrhizal and saprotrophic fungal guilds compete for the same organic substrates but affect decomposition differently. Functional Ecology 30:1967–1978. https://doi.org/10.1111/1365-2435.12677

Brundrett M, Bougher N, Dell B et al (1996) Working with mycorrhizas in forestry and agriculture. Canberra: Australian Centre for Agricultural Research.

Buée M, Boer W, Martin F et al (2009) The rhizosphere zoo: an overview of plant-associated communities of microorganisms, including phages, bacteria, archaea, and fungi, and of some of their structuring factors. Plant Soil 321:189-212.

Cabané M, Pireaux JC, Léger E et al (2004) Condensed lignins are synthesized in polar leaves exposed to ozone. Plant Physiol 134(2):586-594.

Caesar-Tonthat TC (2002) Soil binding properties of mucilage produced by a basidiomycete fungus in a model system. Mycological Research 106:930–937.

Camargo AO, Moniz AC, Jorge JA et al (2009) Methods of chemical analysis, physical and mineralogical soil Agronomic Institute of Campinas. Agronomic Institute, Campinas pp 77.

Camargo OA, Valadares JMAS, Geraldi RN (1983) Características químicas e físicas de solo que recebeu vinhaça por longo tempo. Instituto Agronômico, Campinas.

Camargo R (1954) O desenvolvimento da flora microbiana nos solos tratados com vinhaça. Instituto Zimotécnico, Piracicaba.

Canellas LP,Velloso ACX, Marciano CR et al (2003) Propriedades químicas de um cambissolo cultivado com cana-de-açúcar, com preservação do palhiço e adição de vinhaça por longo tempo. Rev Bras de Ciênc Solo 27:935–944.

Carvalho JLN, Nogueirol RC, Menandro LMS et al (2017) Agronomic and environmental implications of sugarcane straw removal: a major review. GCB Bioenergy 9:1181–1195.

Cassman NA, Leite MFA, Pan Y et al (2016) Plant and soil fungal but not soil bacterial communities are linked in long-term fertilized grassland. Sci Rep 6:23680.

CETESB – Companhia de Tecnologia de Saneamento Ambiental (2015) Norma Técnica p 4.231 – Vinhaça – Critérios e procedimentos para aplicação no solo agrícola. 3ª ed./2ª versão. CETESB, São Paulo, pp15.

Chaer GM, Fernandes MF, Myrold DD et al (2009) Shifts in microbial community composition and physiological profiles across a gradient of induced soil degradation. Soil Sci Soc of Am J 73(4):1327-1334.

Christofoletti CA, Escher JP, Correia JE et al (2013) Sugarcane vinasse: Environmental implications of its use. Waste Manag 33(12):2752-2761.

Cotrufo FC, Galdo ID, Piermatteo D (2010) Litter decomposition: concepts, methods and future perspectives. In: Kutsch WL, Bahn M, Heinemeyer A (ed) Soil carbon dynamics: an integrated methodology. Cambridge University Press, Cambridge, pp 76-90.

Daynes CN, Zhang N, Saleeba JA et al (2012) Soil aggregates formed in vitro by saprotrophic Trichocomaceae have transient water-stability. Soil Biol & Biochem 48:151–161.

de Chaves MG, Silva GGZ, Rossetto R et al (2019) Acidobacteria Subgroups and Their Metabolic Potential for Carbon Degradation in Sugarcane Soil Amended With Vinasse and Nitrogen Fertilizers. Front Microbiol 10:1680.

Dean R, Kan JALV, Pretorius ZA et al (2012) The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13(4):414–430.

Dias MOS, Ensinas AV, Nebra SA et al (2009) Production of bioethanol and other bio-based materials from sugarcane bagasse: Integration to conventional bioethanol production process. Chem Eng Res Des 87(9):1206-1216.

Donovan PD, Gonzales G, Higgins DG et al (2018) Identification of fungi in shotgun metagenomics datasets. PLoS ONE 13(2):e0192898.

Durrer A, Gumiere T, Taketani RG et al (2017) The drivers underlying biogeographical patterns of bacterial communities in soils under sugarcane cultivation. Appl Soil Ecol 110:12-20.

Duplessis S, Cuomo CA, Lin YC et al (2011) Obligate biotrophy features desvendadas pela análise genômica de fungos de ferrugem. Proc Natl Acad Sci USA 108(22):9166-71. doi: 10.1073 / pnas.1019315108

Edwards IP, Zak DR, Kellner H et al (2011) Simulated atmospheric N deposition alters fungal community composition and suppresses ligninolytic gene expression in a northern hardwood forest. PLoS One 6:e20421.

Entwistle EM, Zak DR, Edwards IP (2013) Long-term experimental nitrogen deposition alters the composition of the active fungal community in the forest floor. Soil Sci Soc Am J 77(5):1648–1658.

Ferreira E, Cavalcanti BB, Nogueira DA et al (2014) ExpDes: An R Package for ANOVA and Experimental Designs. Appl Math 5(19):2952-2958.

Fortes C, Trivelin PCO, Vitti AC (2012) Long-term decomposition of sugarcane harvest residues in Sao Paulo state, Brazil. Biomass Bioenergy 42:189–198.

Frac M, Hannula SE, Belka M et al (2018) Fungal Biodiversity and Their Role in Soil Health. Front Microbiol 9:707.

Frey SD, Knorr M, Parrent JL et al (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. For Ecol Manag 196(1):159–171.

Furtado ANM, Daniels PP, Neves MA (2016) New species and new records of Clavariaceae (Agaricales) from Brazil. Phytotaxa 253(1):01–26.

Gasparotto F, Rodrigues FS, Seratto CD et al (2014) Cadeias Produtivas da Cana-de-Açúcar, do Algodão e de Frutas. UniCesumar, Maringá, pp 219.

Glória NA (1992) Uso Agronômico de Resíduos. In: Reunião Brasileira de Fertilidade do Solo e Nutrição de Plantas, 20. Piracicaba, pp 195-212.

Glória NA, Orlando Filho J (1983) Aplicação de vinhaça como fertilizante. Boletim Técnico do Planalsucar 5:5–38.

Gumiere T, Durrer A, Bohannan BJM et al (2016) Biogeographical patterns in fungal communities from soils cultivated with sugarcane. J Biogeogr 43(10):216-226.

Hartmann M, Frey B, Mayer J et al (2015) Distinct soil microbial diversity under long-term organic and conventional farming. ISME Journal 9:1177–1194.

Hidalgo K, Rodríguez B, Valdivié M et al (2009) Utililización de La vizana de destilería como aditivo para pollos em ceba. Rev cuba cienc agrí 43(3):281-284.

Ho A, Lonardo DPD, Bodelier PLE (2017) Revisiting life strategy concepts in environmental microbial ecology. FEMS Microbiol Ecol 93(3):fix006. https://doi.org/ 10.1093/femsec/fix006.

Jarosz AM, Davelos AL (1995) Effects of disease in wild plant populations and the evolution of pathogen agressiveness. New Phytologist 129:371-387.

Jenkins SN, Waite IS, Blackburn A et al (2009) Actinobacterial community dynamics in long term managed grasslands. Antonie van Leeuwenhoek 95(4):319-334.

Jiang ZP, Li Y, Wei GP et al (2012) Effect of long-term vinasse application on physico-chemical properties of sugarcane field soils. Sugar Tech 14(4):412–417.

Kanaly RA, Hur H.-G (2005) Growth of Phanerochaete chrysosporium on diesel fuel hydrocarbons at neutral pH. Chemosphere 63(2):2002-211.

Kaschuk G, Alberton O, Hungria M et al (2011) Quantifying effects of different agricultural land uses on soil microbial biomass and activity in Brazilian biomes: inferences to improve soil quality. Plant Soil 338:467-481.

Kelly R, Thompson JP, Magarey RC et al (2001) Responses of sugarcane, maize, and soybean to phosphorus and vesicular-arbuscular mycorrhizal fungi. Crop Pasture Sci 52(7):731-743.

Laime EMO, Fernandes PD, Oliveira DCS et al (2011) Possibilidades tecnológicas para a destinação da vinhaça: uma revisão. Revista Trópica: Ciências Agrárias e Biológicas, 5(3):16-29.

Lauber CL, Hamady M, Knight R et al (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75(5):5111-5120.

Leal JR, Amaral Sobrinho NMB, Velloso ACX et al (1983) Potencial redox e pH: variação em um solo tratado com vinhaça. Rev Bras Ciênc Solo 7(1):257–261.

López-Bucio J, Pelagio-Flores R, Herrera-Estrella A (2015) Trichoderma as biostimulant: exploiting the multilevel properties of a plant beneficial fungus. Sci Hortic 196:109–123.

Lourenço KS, Suleiman AKA, Pijl A et al (2020) Dynamics and resilience of soil mycobiome under multiple organic and inorganic pulse disturbances. Sci Total Environ 773:139173.

Madejón E, Burgos P, López R et al (2001) Soil enzymatic response to addition of heavy metals with organic residues. Biol Fertil Soils 34(3):144-150.

Magoc T, Salzberg SL (2011) FLASH: Fast Length adjustment of Short Reads to Improve Genome Assemblies. Bioinformatics 27:2957-63.

Mcbride JA, Gauthier GM, Klein BS (2019) Turning on virulence: Mechanisms that underpin the morphologic transition and pathogenicity of Blastomyces. Virulence 10(1):801–809. doi: 10.1080/21505594.2018.1449506

Moraes BS, Junqueira TL, Pavanello LG et al (2014) Anaerobic digestion of vinasse from sugarcane biorefineries in Brazil from energy, environmental, and economic perspectives: Profit or expense?. Appl Energy 113:825-835.

Muñoz JF, McEwen JG, Clay OK et al (2018) Genome analysis reveals evolutionary mechanisms of adaptation in systemic dimorphic fungi. Sci Rep 8:4473, 2018. doi:10.1038/s41598-018-22816-6

Muyzer G, Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59(3):695-700.

Nahas E (1996) Factors determining rock phosphate solubilization by microorganisms isolated from soil. World J Microbiol Biotechnol 12:567-572.

Navarrete AA, Kuramae EE, Hollander M et al (2013) Acidobacterial community responses to agricultural management of soybean in Amazon Forest soils. FEMS Microbiol Ecol 83(3)607-621.

Navarrete AA, Diniz TR, Braga LPP et al (2015) Multi-Analytical Approach Reveals Potential Microbial Indicators in Soil for Sugarcane Model Systems. PLoS ONE 10:1-19.

Neves MCP, Lima IT, Dobereiner J (1983) Efeito da vinhaça sobre a microflora do solo. Rev Bras de Ciênc Solo 7(2):131–136.

Nguyen NH, Song Z, Bates ST et al (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecology 20:241–248.

Nilsson LO, Bååth E, Falkengren-Grerup U et al (2007) Growth of ectomycorrhizal mycelia and composition of soil microbial communities in oak Forest soils along a nitrogen deposition gradient. Oecologia 153(2):375-384.

Oliveira IS, Moura RM, Luz EDMN et al (2006) Patogenicidade de Penicillium sclerotigenum a diferentes frutas e hortaliças em pós-colheita. Fitopatol bras 31(4):408-410.

Oliveira MW, Trivelin PCO, Penatti CP et al (1999) Decomposição e liberação de nutrientes da palhada de cana-de-açúcar em campo. Pesq agropec bras 34(12):2359–2362.

Pace NR (2009) Mapping the tree of life: progress and prospects. Microbiol Mol Biol Rev 73(4):565–576.

Paungfoo-Lonhienne C, Yeoh Y, Kasinadhuni N et al (2015) Nitrogen fertilizer dose alters fungal communities in sugarcane soil and rizosphere. Sci Rep 5:8678.

Penatti CP, Cambria S, Boni PS et al (1988) Efeitos da aplicação de vinhaça e nitrogênio na soqueira da cana-de-açúcar. Boletim Técnico Copersucar 44:32-38.

Pöggeler S (2011) Evolution of multicopper oxidase genes in coprophilous and noncoprophilous members of the order sordariales. Curr Genomics 12(2):95–103.

Pradhan N, Sukla LB (2005) Solubilization of inorganic phosphates by fungi isolated from agriculture soil. Afr J Biotechnol 5(10):850-854.

Prata F, Lavorenti A, Regitano JB et al (2001) Degradação e sorção de ametrina em dois solos com aplicação de vinhaça. Pesq agropec bras 36:975– 981.

Raes J, Rohde A, Christensen JH et al (2003) Genome-wide characterization of the lignification tollbox in Arabidopsis. Plant Physiol 133:1051-1071.

Ramos SMS, Cruz R, Barbosa R et al (2018) Penicillium and Talaromyces Communities of Sugarcane Soils (Saccharum officinarum L.): Ecological and Phylogenetic Aspects. J Agric Sci 10(4):335-350, 2018.

Rachid CTCC, Piccolo MC, Leite DCA et al (2012) Physical-chemical and microbiological changes in Cerrado Soil under differing sugarcane harvest management systems. BMC Microbiology 12:170.

Rachid CTCC, Pires CA, Leite DCA et al (2016) Sugarcane trash levels in soil affects the fungi but not bacteria in a short-term field experiment. Braz J Microbiol 47:322-326.

Reyes I, Bernier L, Antoun H (2002) Rock phosphate solubilization and colonization of maize rhizosphere by wild and genetically modifield strains of Penicillium rugulosum. Microb Ecol 44:39-48.

Romão AS (2010) Análise da comunidade fúngica associada à cana-de-açúcar e estudo da interação Trichoderma virens - planta hospedeira. Dissertação, Universidade de São Paulo.

Rouphael Y, Franken P, Schneider C et al (2015) Arbuscular mycorrhizal fungi act as biostimulants in horticultural crops. Scientia Horticulturae 196:91–108.

Santos TMC, Santos MAL, Santos CG et al (2009) Efeito da fertirrigação com vinhaça nos microrganismos do solo. Revista Caatinga 22:155–160.

Schoch CL, Seifert KA, Huhndorf S et al (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci USA 109:6241-6246.

Silva A, Rossetto R, Thorburn P et al (2013) Occurrence and simulation of nitrification in sugarcane vinasse applied to soil. In: Proceedings of the 28th ISSCT Congress, São Paulo, Brazil.

Silva GGZ, Cuevas DA, Dutilh BE et al (2014) FOCUS: an alignment-free model to identify organisms in metagenomes using non-negative least squares. Peer J 2:e425.

Silva JE, Resck DVS (1997) Matéria orgânica do solo. In: Vargas MAT, Hungria M (ed) Biologia dos solos do cerrado, Embrapa-CPAC, Planaltina, pp 465-516.

Soković M, Glamoclija J, Ćirić A et al (2018) Mushrooms as Sources of Therapeutic Foods. Therapeutic Foods 5:141-178. https://doi.org/10.1016/B978-0-12-811517-6.00005-2.

Souza RA, Telles TS, Machado W, et al (2012) Effects of sugarcane harvesting with burning on the chemical and microbiological properties of the soil. Agriculture, Ecosystems &Environment 155:1-6.

Taiz L, Zeiger E (2004) Fisiologia vegetal. ARTMED, Porto Alegre.

Tang H, Li C, Xiao X et al (2020) Functional diversity of rhizosphere soil microbial communities in response to different tillage and crop residue retention in a double-cropping rice field. PLoS ONE 15:e0233642.

Tejada M, Gonzalez JL (2006) Effects of two beet vinasse forms on soil physical properties and soil loss. Catena 68:41-50.

ter Braak CJF, Šmilauer P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination (version 4.5). Microcomputer Power, New York.

Thorn, G (1997) The fungi in soil. In: Van Elsas, J. D.; Trevors, J. T.; Wellington, E. M. H. Marcel Dekker (ed) Modern soil microbiology, New York, pp 63-127.

Val-Moraes SP, Macedo HS, Kishi LT et al (2016) Liming in the sugarcane burnt system and the green harvest practice affect soil bacterial community in northeastern São Paulo, Brazil. Antonie van Leeuwenhoek 109:1643–1654.

Van der heijden MGA, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296-310.

Varanda LL, Cherubin MR, Cerri CEP (2019) Decomposition dynamics altered by straw removal management in the sugarcane-expansion regions in Brazil. Soil Research 57:41–52.

Wagg C, Bender SF, Widmer F et al (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci USA 111:5266-5270.

Wallenstein MD, McNulty S, Fernandez IJ et al (2006) Nitrogen fertilization decreases forest soil fungal andbacterial biomass in three long-term experiments. For Ecol Manage 222:459-468.

Whitelaw MA (2000) Growth promotion of plants inoculated with phosphate solubilizing fungi. Advancesin Agronomy, New York




DOI: https://doi.org/10.34117/bjdv8n6-149