Innovative sustainable bioreactor-in-a-granule formulation of Trichoderma asperelloides.
Trichoderma
Biocontrol agent
Bioprotectant
Granule formulation
Solid-state fermentation
White mold
Journal
Applied microbiology and biotechnology
ISSN: 1432-0614
Titre abrégé: Appl Microbiol Biotechnol
Pays: Germany
ID NLM: 8406612
Informations de publication
Date de publication:
04 Sep 2024
04 Sep 2024
Historique:
received:
24
04
2024
accepted:
17
07
2024
revised:
16
07
2024
medline:
4
9
2024
pubmed:
4
9
2024
entrez:
4
9
2024
Statut:
epublish
Résumé
The advancement of fungal biocontrol agents depends on replacing cereal grains with low-cost agro-industrial byproducts for their economical mass production and development of stable formulations. We propose an innovative approach to develop a rice flour-based formulation of the beneficial biocontrol agent Trichoderma asperelloides CMAA1584 designed to simulate a micro-bioreactor within the concept of full biorefinery process, affording in situ conidiation, extended shelf-life, and effective control of Sclerotinia sclerotiorum, a devastating pathogen of several dicot agricultural crops worldwide. Rice flour is an inexpensive and underexplored byproduct derived from broken rice after milling, capable of sustaining high yields of conidial production through our optimized fermentation-formulation route. Conidial yield was mainly influenced by nitrogen content (0.1% w/w) added to the rice meal coupled with the fermentor type. Hydrolyzed yeast was the best nitrogen source yielding 2.6 × 10
Identifiants
pubmed: 39230670
doi: 10.1007/s00253-024-13261-9
pii: 10.1007/s00253-024-13261-9
doi:
Substances chimiques
Nitrogen
N762921K75
Biological Control Agents
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
458Subventions
Organisme : Empresa Brasileira de Pesquisa Agropecuária
ID : 20.19.02.006.00.00
Informations de copyright
© 2024. The Author(s).
Références
Ahmed I, Qazi IM, Jamal S (2015) Quality evaluation of noodles prepared from blending of broken rice and wheat flour. Starch 67:905–912. https://doi.org/10.1002/star.201500037
doi: 10.1002/star.201500037
Asis A, Shahriar SA, Naher L, Saallah S, Fatihah HNN, Kumar V, Siddiquee S (2021) Identification patterns of Trichoderma strains using morphological characteristics, phylogenetic analyses and lignocellulolytic activities. Mol Biol Rep 48:3285–3301. https://doi.org/10.1007/s11033-021-06321-0
doi: 10.1007/s11033-021-06321-0
pubmed: 33880673
Bacilio M, Vazquez P, Bashan Y (2003) Alleviation of noxious effects ofcattle ranch composts on wheat seed germination by inoculation with Azospirillum spp. Biol Fert Soils 38:261–266. https://doi.org/10.1007/s00374-003-0650-1
doi: 10.1007/s00374-003-0650-1
Bich GA, Castrillo ML, Villalba LL, Zapata PD (2018) Evaluation of rice by-products, incubation time, and photoperiod for solid state mass multiplication of the biocontrol agents Beauveria bassiana and Metarhizium anisopliae. Agronomy Res 16:1921–1930. https://doi.org/10.15159/ar.18.197
doi: 10.15159/ar.18.197
Bird AR, Hayakawa T, Marsono Y, Gooden JM, Record IR, Correll RL, Topping DL (2000) Coarse brown rice increases fecal and large bowel short-chain fatty acids and starch but lowers calcium in the large bowel of pigs. J Nutrit 130:1780–1787. https://doi.org/10.1093/jn/130.7.1780
doi: 10.1093/jn/130.7.1780
pubmed: 10867050
Boland GJ, Hall R (1994) Index of plant hosts of Sclerotinia sclerotiorum. Can J Plant Pathol 16:93–108. https://doi.org/10.1080/07060669409500766
doi: 10.1080/07060669409500766
Bolton MD, Thomma BPHJ, Nelson BD (2006) Sclerotinia sclerotiorum (Lib.) de Bary: biology and molecular traits of a cosmopolitan pathogen. Mol Plant Pathol 7:1–16. https://doi.org/10.1111/j.1364-3703.2005.00316.x
doi: 10.1111/j.1364-3703.2005.00316.x
pubmed: 20507424
Bueno VHP, Parra JRP, Bettiol W, Lenteren JC (2020) Biological control in Brazil. In: Van Lenteren J, Bueno VHP, Luna MG, Colmenarez YC (eds) Biological control in Latin America and the Caribbean: its rich history and bright future. CABI, Wallingford, pp 78–107. https://doi.org/10.1079/9781789242430.0078
Cavalcante RS, Lima HLS, Pinto GAS, Gava CAT, Rodrigues S (2008) Effect of moisture on Trichoderma conidia production on corn and wheat bran by solid state fermentation. Food Biop Technol 1:100–104. https://doi.org/10.1007/s11947-007-0034-x
doi: 10.1007/s11947-007-0034-x
CEPEA - Centro de Estudos Avançados em Economia Aplicada (2023) Indicador do arroz em casca. Available at: https://www.cepea.esalq.usp.br/br/consultas-ao-banco-de-dados-do-site.aspx . Accessed 15 October 2023
Chan ES, Wong SL, Lee PP, Lee JS, Ti TB, Zhang Z, Poncelet D, Ravindra P, Phan SH, Yim ZH (2011) Effects of starch filler on the physical properties of lyophilized calcium–alginate beads and the viability of encapsulated cells. Carbohydr Polym 83:225–232. https://doi.org/10.1016/j.carbpol.2010.07.044
doi: 10.1016/j.carbpol.2010.07.044
Cliquet S, Zeeshan K (2008) Impact of nutritional conditions on yields, germination rate and shelf-life of Plectosporium alismatis conidia and chlamydospores as potential candidates for the development of a mycoherbicide of weeds in rice crops. Biocontrol Sci Technol 18:685–695. https://doi.org/10.1080/09583150802255827
doi: 10.1080/09583150802255827
Dallastra EDG, Dias ACP, Morais PB, Silva JFM, Casciatori FP, Grajales LM (2023) Development of a novel pilot-scale tray bioreactor for solid-state fermentation aiming at process intensification. Chem Eng Proc - Proc Intensif 193:109526. https://doi.org/10.1016/j.cep.2023.109526
doi: 10.1016/j.cep.2023.109526
Elias AM, Favaro CP, Bettiol W, Ribeiro C, Farinas CS (2022) Economic aspects on the production of biofertilizers as granular composites. ACS Sustain Chem Eng. https://doi.org/10.1021/acssuschemeng.2c04021
doi: 10.1021/acssuschemeng.2c04021
Esa NM, Ling TB, Peng LS (2013) By-products of rice processing: an overview of health benefits and applications. J Rice Res 1:107. https://doi.org/10.4172/jrr.1000107
doi: 10.4172/jrr.1000107
Faria MR, Wraight SP (2007) Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43:237–256. https://doi.org/10.1016/j.biocontrol.2007.08.001
doi: 10.1016/j.biocontrol.2007.08.001
Faria M, Hotchkiss JH, Wraight SP (2012) Application of modified atmosphere packaging (gas flushing and active packaging) for extending the shelf life of Beauveria bassiana conidia at high temperatures. Biol Control 61:78–88. https://doi.org/10.1016/j.biocontrol.2011.12.008
doi: 10.1016/j.biocontrol.2011.12.008
Faria AF, Schulman P, Meyer MC, Campos HD, Cruz-Magalhães V, Godoy CV, Guimarães RA, Silva LHCP, Goussain MM, Martins MC, Nunes Júnior J, Venancio WS, Fantin L, Brustolin R, Jaccoud Filho DS, Carneiro LC, Juliatti FC, Medeiros FHV (2022a) Seven years of white mold biocontrol product’s performance efficacy on Sclerotinia sclerotiorum carpogenic germination in Brazil: a meta-analysis. Biol Control 176:105080. https://doi.org/10.1016/j.biocontrol.2022.105080
doi: 10.1016/j.biocontrol.2022.105080
Faria M, Palhares LAM, Souza DA, Lopes RB (2022b) What would be representative temperatures for shelf-life studies with biopesticides in tropical countries? Estimates through long-term storage of biocontrol fungi and calculation of mean kinetic temperatures. Biocontrol 67:213–224. https://doi.org/10.1007/s10526-021-10126-2
doi: 10.1007/s10526-021-10126-2
Farinas CS (2015) Developments in solid-state fermentation for the production of biomass-degrading enzymes for the bioenergy sector. Renew Sustain En Rev 52:179–188. https://doi.org/10.1016/j.rser.2015.07.092
doi: 10.1016/j.rser.2015.07.092
Garcia RA, Juliatti FC, Cassemiro TA (2012) Production of sclerotia on Sclerotinia sclerotiorum (Lib.) de bary in culture media. Bioscience J 28:1–7
Giroto AS, Garcia RHS, Colnago LA, Klamczynski A, Glenn GM, Ribeiro C (2020) Role of urea and melamine as synergic co-plasticizers for starch composites for fertilizer application. Int J Biol Macromol 144:143–150. https://doi.org/10.1016/j.ijbiomac.2019.12.094
doi: 10.1016/j.ijbiomac.2019.12.094
pubmed: 31843606
Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17–25. https://doi.org/10.1099/mic.0.052274-0
doi: 10.1099/mic.0.052274-0
pubmed: 21998166
Henis Y, Adams PB, Lewis JA, Papavizas GC (1983) Penetration of sclerotia of Sclerotium rolfsii by Trichoderma spp. Phytopathol 73:1043–1046. https://doi.org/10.1094/Phyto-73-1043
doi: 10.1094/Phyto-73-1043
Hewavitharana N, Kannangara SDP, Senanayake SP (2018) Isolation, identification and mass production of five Trichoderma spp. on solid and liquid carrier media for commercialization. Int J Appl Sci Biotechnol 6:285–293. https://doi.org/10.3126/ijasbt.v6i4.22128
doi: 10.3126/ijasbt.v6i4.22128
Hong TD, Jenkins NE, Ellis RH (1999) Fluctuating temperature and the longevity of conidia of Metarhizium flavoviride in storage. Biocontrol Sci Technol 9:165–176. https://doi.org/10.1080/09583159929758
doi: 10.1080/09583159929758
Hong TD, Gunn J, Ellis HR, Jenkins NE, Moore D (2001) The effect of storage environment on the longevity of conidia of Beauveria bassiana. Mycological Res 105:597–602. https://doi.org/10.1017/S0953756201004026
doi: 10.1017/S0953756201004026
Jackson MA, Whipps JM, Lynch JM, Bazin MJ (1991) Effects of some carbon and nitrogen sources on spore germination, production of biomass and antifungal metabolites by species of Trichoderma and Gliocladium virens antagonistic to Sclerotium cepivorum. Biocontrol Sci Technol 1:43–51. https://doi.org/10.1080/09583159109355184
doi: 10.1080/09583159109355184
Jackson MA (1997) Optimizing nutritional conditions for the liquid culture production of effective fungal biological control agents. J Ind Microbiol Biotechnol 19:180–187. https://doi.org/10.1038/sj.jim.2900426
doi: 10.1038/sj.jim.2900426
Jaronski ST (2014) Mass production of entomopathogenic fungi: state of the art. In: Morales-Ramos JA, Rojas MG, Shapiro-Ilan DI (eds) Mass production of beneficial organisms invertebrates and entomopathogens. Elsevier, Amsterdam, pp 357–413. https://doi.org/10.1016/B978-0-12-391453-8.00011-X
Jin X, Custis D (2011) Microencapsulating aerial conidia of Trichoderma harzianum through spray drying at elevated temperatures. Biol Control 56:202–208. https://doi.org/10.1016/j.biocontrol.2010.11.008
doi: 10.1016/j.biocontrol.2010.11.008
Klaic R, Giroto AS, Guimarães GGF, Plotegher F, Ribeiro C, Zangirolami TC, Farinas CS (2018) Nanocomposite of starch-phosphate rock bioactivated for environmentally-friendly fertilization. Miner Eng 128:230–237. https://doi.org/10.1016/j.mineng.2018.09.002
doi: 10.1016/j.mineng.2018.09.002
Lavie S, Stotzky G (1986a) Adhesion of the clay minerals montmorillonite, kaolinite and attapulgite reduces respiration of Histoplasma capsulatum. Appl Environ Microbiol 51:65–73. https://doi.org/10.1128/aem.51.1.65-73.19
doi: 10.1128/aem.51.1.65-73.19
pubmed: 3954340
pmcid: 238816
Lavie S, Stotzky G (1986b) Interactions between clay minerals and siderophores affect the respiration of Histoplasma capsulatum. Appl Environ Microbiol 51:74–79. https://doi.org/10.1128/aem.51.1.74-79.1986
doi: 10.1128/aem.51.1.74-79.1986
pubmed: 2937365
pmcid: 238817
Lehner MS, Pethybridge SJ, Meyer MC, Del Ponte EM (2017) Meta-analytic modelling of the incidence-yield and incidence-sclerotial production relationships in soybean white mould epidemics. Plant Pathol 66:460–468. https://doi.org/10.1111/ppa.12590
doi: 10.1111/ppa.12590
Lewis J, Papavizas G (1985) Characteristics of alginate pellets formulated with Trichoderma and Gliocladium and their effect on the proliferation of the fungi in soil. Plant Pathol 34:571–577. https://doi.org/10.1111/j.1365-3059.1985.tb01409.x
doi: 10.1111/j.1365-3059.1985.tb01409.x
Li Z, Alves SB, Roberts DW, Fan M, Delalibera I, Tang J, Lopes RB, Faria M, Rangel DEN (2010) Biological control of insects in Brazil and China: history, current programs and reasons for their successes using entomopathogenic fungi. Biocontrol Sci Technol 20:117–136. https://doi.org/10.1080/09583150903431665
doi: 10.1080/09583150903431665
Liu H, Wan H, Xu S, Fang Z, Lin Y, Che L, Li J, Li Y, Su X, Wu D (2016) Influence of extrusion of corn and broken rice on energy content and growth performance of weaning pigs. Anim Sci J 87:1386–1395. https://doi.org/10.1111/asj.12578
doi: 10.1111/asj.12578
pubmed: 26935985
Lorito M, Woo SL, Harman GE, Monte E (2010) Translational research on Trichoderma : from ’omics to the field. Ann Rev Phytopathol 48:395–417. https://doi.org/10.1146/annurev-phyto-073009-114314
doi: 10.1146/annurev-phyto-073009-114314
Mascarin GM, Jackson MA, Behle RW, Kobori NN, Júnior ÍD (2016) Improved shelf life of dried Beauveria bassiana blastospores using convective drying and active packaging processes. Appl Microbiol Biotechnol 100:8359–8370. https://doi.org/10.1007/s00253-016-7597-2
doi: 10.1007/s00253-016-7597-2
pubmed: 27198727
Mascarin GM, Kobori NN, Jackson MA, Dunlap CA, Delalibera Í Jr (2018) Nitrogen sources affect productivity, desiccation tolerance and storage stability of Beauveria bassiana blastospores. J Appl Microbiol 124:810–820. https://doi.org/10.1111/jam.13694
doi: 10.1111/jam.13694
pubmed: 29327477
Mascarin GM, Lopes RB, Delalibera Í, Fernandes ÉKK, Luz C, Faria M (2019) Current status and perspectives of fungal entomopathogens used for microbial control of arthropod pests in Brazil. J Inverteb Pathol 165:46–53. https://doi.org/10.1016/j.jip.2018.01.001
doi: 10.1016/j.jip.2018.01.001
Meher J, Rajput RS, Bajpai R, Teli B, Sarma BK (2020) Trichoderma: a globally dominant commercial biofungicide. In: Manoharachary C, Singh HB, Varma A (eds) Trichoderma: agricultural applications and beyond. Springer, pp 195–208
doi: 10.1007/978-3-030-54758-5_9
Morán-Diez ME, Tranque E, Bettiol W, Monte E, Hermosa R (2020) Differential response of tomato plants to the application of three Trichoderma species when evaluating the control of Pseudomonas syringae populations. Plants 9:626. https://doi.org/10.3390/plants9050626
doi: 10.3390/plants9050626
pubmed: 32422955
pmcid: 7285377
Muniz PHPC, Peixoto GHS, Teixeira MPM, Mello SCM, Carvalho DDC (2018) Produção de conídios em substrato sólido e colonização superficial por Trichoderma harzianum. Rev Agr Neotropical 5:40–44. https://doi.org/10.32404/rean.v5i4.2608
doi: 10.32404/rean.v5i4.2608
Myburgh MW, Cripwell RA, Favaro L, van Zyl WH (2019) Application of industrial amylolytic yeast strains for the production of bioethanol from broken rice. Bioresour Technol 294:122222. https://doi.org/10.1016/j.biortech.2019.122222
doi: 10.1016/j.biortech.2019.122222
pubmed: 31683453
Nakano S, Ugwu CU, Tokiwa Y (2012) Efficient production of D-(−)-lactic acid from broken rice by Lactobacillus delbrueckii using Ca(OH)
doi: 10.1016/j.biortech.2011.10.017
pubmed: 22093977
Napoleão R, Nasser L, Lopes C, Café Filho A (2006) Neon-S, novo meio para detecção de Sclerotinia sclerotiorum em sementes. Summa Phytopathol 32:180–182. https://doi.org/10.1590/S0100-54052006000200014
doi: 10.1590/S0100-54052006000200014
Nardi S, Pizzeghello D, Muscolo A, Vianello A (2002) Physiological effects of humic substances on higher plants. Soil Biol Biochem 34:1527–1536. https://doi.org/10.1016/S0038-0717(02)00174-8
doi: 10.1016/S0038-0717(02)00174-8
Pereira EI, Minussi FB, Cruz CCT, Bernardi ACC, Ribeiro C (2012) Urea–montmorillonite-extruded nanocomposites: a novel slow-release material. J Agricul Food Chem 60:5267–5272. https://doi.org/10.1021/jf3001229
doi: 10.1021/jf3001229
Przyklenk M, Vemmer M, Hanitzsch M, Patel A (2017) A bioencapsulation and drying method increases shelf life and efficacy of Metarhizium brunneum conidia. J Microencapsul 34:498–512. https://doi.org/10.1080/02652048.2017.1354941
doi: 10.1080/02652048.2017.1354941
pubmed: 28699822
Rezende LC, Carvalho ALA, Costa LB, Halfeld-Vieira BA, Silva LG, Pinto ZV, Morandi MAB, Medeiros FHV, Mascarin GM, Bettiol W (2020) Optimizing mass production of Trichoderma asperelloides by submerged liquid fermentation and its antagonism against Sclerotinia sclerotiorum. World J Microbiol Biotechnol 36:1–14. https://doi.org/10.1007/s11274-020-02882-7
doi: 10.1007/s11274-020-02882-7
Ribeiro C, Carmo M (2019) Why nonconventional materials are answers for sustainable agriculture. MRS Energy Sustain 7:E9. https://doi.org/10.1557/mre.2019.7
doi: 10.1557/mre.2019.7
Rubio MB, Hermosa R, Vicente R, Gómez-Acosta FA, Morcuende R, Monte E, Bettiol W (2017) The combination of Trichoderma harzianum and chemical fertilization leads to the deregulation of phytohormone networking, preventing the adaptive responses of tomato plants to salt stress. Front Plant Sci 8:294. https://doi.org/10.3389/fpls.2017.00294
doi: 10.3389/fpls.2017.00294
pubmed: 28303151
pmcid: 5332374
Schellart JA, Visser FMW, Zandstra T, Middelhoven WJ (1976) Starch degradation by the mould Trichoderma viride I. The mechanism of starch degradation. Antonie Leeuwenhoek 42:229–238. https://doi.org/10.1007/BF00394119
doi: 10.1007/BF00394119
pubmed: 10832
Schoebitz M, Simonin H, Poncelet D (2012) Starch filler and osmoprotectants improve the survival of rhizobacteria in dried alginate beads. J Microencapsul 29:532–538. https://doi.org/10.3109/02652048.2012.665090
doi: 10.3109/02652048.2012.665090
pubmed: 22372947
Smolińska U, Kowalska B (2018) Biological control of the soil-borne fungal pathogen Sclerotinia sclerotiorum - a review. J Plant Pathol 100:1–12. https://doi.org/10.1007/s42161-018-0023-0
doi: 10.1007/s42161-018-0023-0
Soccol CR, Costa ESF, Letti LAJ, Karp SG, Woiciechowski AL, Vandenberghe LPS (2017) Recent developments and innovations in solid state fermentation. Biotechnol Res Inn 1:52–71. https://doi.org/10.1016/j.biori.2017.01.002
doi: 10.1016/j.biori.2017.01.002
Stanbury PF, Whitaker A, Hall SJ (2017) Media for industrial fermentations. In: Stanbury PF, Whitaker A, Hall SJ (eds) Principles of fermentation technology, Elsevier, Cambridge, pp 213–272. https://doi.org/10.1016/B978-0-08-099953-1.00004-1
Stotzky G, Burns RG (1982) The soil environment, clay-humus-microbe interactions. In: Burns RG, Slater JH (eds) Experimental microbial ecology. Blackwell, Oxford, pp 105–133
Swaminathan J, Van Koten C, Henderson HV, Jackson TA, Wilson MJ (2016) Formulations for delivering Trichoderma atroviridae spores as seed coatings, effects of temperature and relative humidity on storage stability. J Appl Microbiol 120:425–431. https://doi.org/10.1111/jam.13006
doi: 10.1111/jam.13006
pubmed: 26600429
van Lenteren JC, Bolckmans K, Köhl J, Ravensberg WJ, Urbaneja A (2018) Biological control using invertebrates and microorganisms: plenty of new opportunities. Biocontrol 63:39–59. https://doi.org/10.1007/s10526-017-9801-4
doi: 10.1007/s10526-017-9801-4
Vassilev N, Vassileva M, Martos V, Garcia del Moral LF, Kowalska J, Tylkowski B, Malusá E (2020) Formulation of microbial inoculants by encapsulation in natural polysaccharides: focus on beneficial properties of carrier additives and derivatives. Front Plant Sci 11:270. https://doi.org/10.3389/fpls.2020.00270
doi: 10.3389/fpls.2020.00270
pubmed: 32211014
pmcid: 7077505
Verma M, Brar SK, Tyagi RD, Surampalli RY, Valéro JR (2007) Starch industry wastewater as a substrate for antagonist, Trichoderma viride production. Bioresour Technol 98:2154–2162. https://doi.org/10.1016/j.biortech.2006.08.032
doi: 10.1016/j.biortech.2006.08.032
pubmed: 17084079
Woo SL, Ruocco M, Vinale F, Nigro M, Marra R, Lombardi N, Pascale A, Lanzuise S, Manganiello G, Lorito M (2014) Trichoderma-based products and their widespread use in agriculture. Open Mycol J 8:71–126. https://doi.org/10.2174/1874437001408010071
doi: 10.2174/1874437001408010071
Woo SL, Hermosa R, Lorito M, Monte E (2023) Trichoderma: a multipurpose, plant-beneficial microorganism for eco-sustainable agriculture. Nat Rev Microbiol 21:312–326. https://doi.org/10.1038/s41579-022-00819-5
doi: 10.1038/s41579-022-00819-5
pubmed: 36414835
Young CC, Rekha PD, Lai WA, Arun AB (2006) Encapsulation of plant growth-promoting bacteria in alginate beads enriched with humic acid. Biotechnol Bioeng 95:76–83. https://doi.org/10.1002/bit.20957
doi: 10.1002/bit.20957
pubmed: 16619210