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Isolation and identification of lactic acid bacteria in fresh plants and in silage from Opuntia and their effects on the fermentation and aerobic stability of silage

Published online by Cambridge University Press:  25 March 2020

G. A. Pereira ,
E. M. Santos ,
G. G. L. Araújo ,
J. S. Oliveira ,
R. M. A. Pinho Open the ORCID record for R. M. A. Pinho [Opens in a new window] ,
A. de M. Zanine Open the ORCID record for A. de M. Zanine [Opens in a new window] ,
A. F. N. Souza ,
A. J. S. Macedo ,
J. M. C. Neto  and
T. V. C. Nascimento Open the ORCID record for T. V. C. Nascimento [Opens in a new window]
G. A. Pereira
Affiliation:
Department of Animal Science, Federal University of Paraíba, Areia, Paraíba, Brazil
E. M. Santos
Affiliation:
Department of Animal Science, Federal University of Paraíba, Areia, Paraíba, Brazil
G. G. L. Araújo
Affiliation:
Brazilian Agricultural Research Corporation, EMBRAPA Semiarid, Petrolina, Pernambuco, Brazil
J. S. Oliveira
Affiliation:
Department of Animal Science, Federal University of Paraíba, Areia, Paraíba, Brazil
R. M. A. Pinho
Affiliation:
Department of Animal Science, Federal University of Maranhão, Chapadinha, Maranhão, Brazil
A. de M. Zanine*
Affiliation:
Department of Animal Science, Federal University of Maranhão, Chapadinha, Maranhão, Brazil
A. F. N. Souza
Affiliation:
Department of Animal Science, Federal University of Paraíba, Areia, Paraíba, Brazil
A. J. S. Macedo
Affiliation:
Department of Animal Science, Federal University of Paraíba, Areia, Paraíba, Brazil
J. M. C. Neto
Affiliation:
Department of Animal Science, Federal University of Paraíba, Areia, Paraíba, Brazil
T. V. C. Nascimento
Affiliation:
Department of Animal Science, Federal University of Maranhão, Chapadinha, Maranhão, Brazil
*
Author for correspondence: A. de M. Zanine, E-mail: [email protected]
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Abstract

The current study aimed to select the strains of lactic acid bacteria (LAB) isolated from forage cactus plants and silage and assess their effects on silage fermentation and aerobic stability. Forty wild isolates from plant and cactus silage, classified as LAB, were evaluated for metabolite production and identified by 16S ribosomal DNA sequencing. These wild isolates were identified as Lactobacillus plantarum, Weissella cibaria, Weissella confusa and Weissella paramesenteroides and the LAB populations differed among the silage. The use of microbial inoculants did not influence gas or effluent losses in forage cactus silage. The silage inoculated with the microbial strain GP15 showed the highest number of LAB populations. The amounts of water-soluble carbohydrates (WSC) and ammonia nitrogen differed among the silage. The silage inoculated with the GP1 strain presented the highest WSC. Populations of enterobacteria and yeasts and moulds were below the minimum detection limit (<2.0 log cfu/g silage) in all the silage studied. The predominant action of inoculants was to maximize dry matter recovery of the silage, which could be the criterion adopted to select the strains of LAB for use as inoculants in Opuntia silage.

Keywords

Lactobacillus plantarumribosomal DNA sequenceWeissella cibariaWeissella confusaWeissella paramesenteroides
Type
Crops and Soils Research Paper
Information
The Journal of Agricultural Science , Volume 157 , Issue 9-10 , December 2019 , pp. 684 - 692
Copyright
Copyright © Cambridge University Press 2020

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References

Abidi, S, Ben Salem, H, Vasta, V and Priolo, A (2009) Supplementation with barley or spineless cactus (Opuntia ficus indica f. inermis) cladodes on digestion, growth and intramuscular fatty acid composition in sheep and goats receiving oaten hay. Small Ruminant Research 87, 9–16.CrossRefGoogle Scholar
Aguilar-Yáñez, MI, Hernández-Mendo, O, Guerrero-Legarreta, I, Ramírez–Bribiesca, JE, Aranda-Osorio, G and Crosby-Galvan, MM (2011) Productive response of lambs fed with fresh or dehydrated spineless cactus (Opuntia ficus indica L.). Journal of the Professional Association for Cactus Development 13, 23–35.Google Scholar
Alli, I, Fairbairn, R, Baker, BE and Garcia, G (1983) The effects of ammonia on the fermentation of chopped sugarcane. Animal Feed Science and Technology 9, 291–299.CrossRefGoogle Scholar
Altschul, SF, Gish, W, Miller, W, Myers, EW and Lipman, DJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.CrossRefGoogle ScholarPubMed
Andrade-Montemayor, HM, Cordova-Torres, AV, García-Gasca, T and Kawas, JR (2011) Alternative foods for small ruminants in semiarid zones, the case of Mesquite (Prosopis laevigata spp.) and Nopal (Opuntia Spp.). Small Ruminant Research 98, 83–92.CrossRefGoogle Scholar
Arriola, KG, Queiroz, OCM, Romero, JJ, Casper, D, Muniz, E, Hamie, J and Adesogan, AT (2015) Effect of microbial inoculants on the quality and aerobic stability of bermudagrass round-bale haylage. Journal of Dairy Science 98, 478–485.CrossRefGoogle ScholarPubMed
Asa, TAR, Uehara, A, Shinzato, I, Toride, Y, Usui, N, Hirakawa, K and Takahashi, J (2010) Effects of protease-resistant antimicrobial substances produced by lactic acid bacteria on rumen methanogenesis. Asian-Australasian Journal of Animal Science 23, 700–707.CrossRefGoogle Scholar
Association of Official Analytical Chemists (AOAC) (1990) Official Methods of Analysis, 15th Edn. Arlington, VA, USA: AOAC.Google Scholar
Ávila, CLS, Pinto, JC, Figueiredo, HCP and Schwan, RF (2009) Effects of an indigenous and a commercial Lactobacillus buchneri strain on quality of sugar cane silage. Grass and Forage Science 64, 384–394.CrossRefGoogle Scholar
Carvalho, BF, Ávila, CLS, Pinto, JC, Neri, J and Schwan, RF (2014) Microbiological and chemical profile of sugar cane silage fermentation inoculated with wild strains of lactic acid bacteria. Animal Feed Science and Technology 195, 1–13.CrossRefGoogle Scholar
Costa, RF, Pires, DAA, Moura, MMA, Sales, ECJ, Rodrigues, JAS and Rigueira, JPS (2016) Agronomic characteristics of sorghum genotypes and nutritional values of silage. Acta Scientiarum. Animal Sciences 38, 127–133.CrossRefGoogle Scholar
Crowley, S, Mahony, J and van Sinderen, D (2013) Current perspectives on antifungal lactic acid bacteria as natural bio-preservatives. Trends in Food Science & Technology 33, 93–109.CrossRefGoogle Scholar
Çürek, M and Özen, N (2004) Feed value of cactus and cactus silage. Turkish Journal of Veterinary and Animal Sciences 28, 633–639.Google Scholar
Detmann, E, Souza, MA, Valadares Filho, SC, Queiroz, AC, Berchielli, TT, Saliba, EOS, Cabral, LS, Pina, DS, Ladeira, MM and Azevedo, JAG (2012) Métodos para Análise de Alimentos. Instituto Nacional de Ciência e Tecnologia de Ciência Animal. 1st Edn. Visconde do Rio Branco, Brazil: Suprema.Google Scholar
du Toit, A, de Wit, M and Hugo, A (2018) Cultivar and harvest month influence the nutrient content of Opuntia Spp. cactus pear cladode mucilage extracts. Molecules 23, 1–12.CrossRefGoogle ScholarPubMed
Felkai-Haddache, L, Remini, H, Dulong, V, Mamou-Belhabib, K, Picton, L, Madani, K and Rihouey, C (2016) Conventional and microwave-assisted extraction of mucilage from Opuntia ficus-indica cladodes: physico-chemical and rheological properties. Food and Bioprocess Technology 9, 481–492.CrossRefGoogle Scholar
Filya, I and Sucu, E (2010) The effects of lactic acid bacteria on the fermentation, aerobic stability and nutritive value of maize silage. Grass and Forage Science 65, 446–455.CrossRefGoogle Scholar
Gusha, J, Katsande, S, Zvinorova, PI and Ncube, SL (2013) The nutritional composition and acceptability of cacti (Opuntia ficus indica)-legume mixed silage. Online Journal of Animal and Feed Research 3, 116–120.Google Scholar
Gusha, J, Halimani, TE, Ngongoni, NT and Ncube, S (2015) Effect of feeding cactus-legume silages on nitrogen retention, digestibility and microbial protein synthesis in goats. Animal Feed Science and Technology 206, 1–7.CrossRefGoogle 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 gelelectrophoretic separation in denaturing gradients. Applied and Environmental Microbiology 63, 3233–3241.CrossRefGoogle Scholar
Holt, JG, Krieg, NR and Sneath, PHA (1994) Bergey's Manual of Determinative Bacteriology, 9th Edn, Baltimore, MD, USA: Williams and Wilkins.Google Scholar
Isaac, AA (2016) Overview of cactus (Opuntia ficus-indica (L): a myriad of alternatives. Studies on Ethno-Medicine 10, 195–205.CrossRefGoogle Scholar
Kalegowda, P, Chauhan, AS and Urs, SMN (2017) Opuntia dillenii (Ker-Gawl) Haw cladode mucilage: physico-chemical, rheological and functional behavior. Carbohydrate Polymers 157, 1057–1064.CrossRefGoogle ScholarPubMed
Ke, W, Ding, W, Xu, D, Shah, MN, Zhang, P and Guo, X (2018) Influences of addition of malic acid or citric acid, Lactobacillus plantarum and their mixtures on fermentation quality, proteolysis and fatty acid composition of ensiled alfalfa. Archives of Animal Nutrition 72, 492–502.CrossRefGoogle ScholarPubMed
Kleinschmit, DH and Kung, L Jr (2006) The effects of Lactobacillus buchneri 40788 and Pediococcus pentosaceus R1094 on the fermentation of corn silage. Journal of Dairy Science 89, 3999–4004.CrossRefGoogle ScholarPubMed
Kung, L Jr and Ranjit, NK (2001) The effect of Lactobacillus buchneri and other additives on the fermentation and aerobic stability of barley silage. Journal of Dairy Science 84, 1149–1155.CrossRefGoogle ScholarPubMed
Kung, L Jr, Shaver, RD, Grant, RJ and Schmidt, RJ (2018) Silage review: interpretation of chemical, microbial, and organoleptic components of silages. Journal of Dairy Science 101, 4020–4033.CrossRefGoogle ScholarPubMed
Li, D, Ni, K, Pang, H, Wang, Y, Cai, Y and Jin, Q (2015) Identification and antimicrobial activity detection of lactic acid bacteria isolated from corn stover silage. Asian-Australasian Journal of Animal Science 28, 620–631.CrossRefGoogle ScholarPubMed
Li, X, Tian, J, Zhang, Q, Jiang, Y, Hou, J, Wu, Z and Yu, Z (2018) Effects of applying Lactobacillus plantarum and Chinese gallnut tannin on the dynamics of protein degradation and proteases activity in alfalfa silage. Grass and Forage Science 73, 648–659.CrossRefGoogle Scholar
Macêdo, AJS, Santos, EM, Araújo, GGL, Edvan, RL, Oliveira, JS, Perazzo, AF, Sá, WCCS and Pereira, DM (2018) Silages in the form of diet based on spineless cactus and buffelgrass. African Journal of Range & Forage Science 35, 121–129.CrossRefGoogle Scholar
Mertens, DR (2002) Gravimetric determination of amylase-treated neutral detergent fiber in feeds with refluxing in beakers or crucibles: collaborative study. Journal of AOAC International 85, 1217–1240.Google ScholarPubMed
Monrroy, M, García, E, Ríos, K and García, JR (2017) Extraction and physicochemical characterization of mucilage from Opuntia cochenillifera (L.) Miller. Journal of Chemistry 2017, 1–9.CrossRefGoogle Scholar
Moon, NJ, Ely, L and Sudweeks, EM (1981) Fermentation of wheat, corn and alfalfa silages inoculated with Lactobacillus acidophilus and Candida sp. at ensiling. Journal of Dairy Science 64, 807–813.CrossRefGoogle Scholar
Muck, RE (2008) Improving alfalfa silage quality with inoculants and silo management. In Proceedings of the 70th Annual Cornell Nutrition Conference for Feed Manufacturers. Syracuse, NY, USA: Cornell University Syracuse, pp. 137–146.Google Scholar
Muck, RE (2010) Silage microbiology and its control through additives. Revista Brasileira de Zootecnia 39, 183–191.CrossRefGoogle Scholar
Ndagano, D, Lamoureux, T, Dortu, C, Vandermoten, S and Thonart, P (2011) Antifungal activity of 2 lactic acid bacteria of the Weissella Genus isolated from food. Journal of Food Science 76, M305–M311.CrossRefGoogle ScholarPubMed
Nelson, N (1944) A photometric adaptation of the Somogyi method for the determination of glucose. Journal of Biological Chemistry 153, 375–380.Google Scholar
Pedroso, AF, Nussio, LG, Paziani, SF, Loures, DRS, Igarasi, MS, Coelho, RM, Packer, IH, Hori, IJ and Gomes, LH (2005) Fermentation and epiphytic microflora dynamics in sugar cane silage. Scientia Agricola 62, 427–432.CrossRefGoogle Scholar
Petera, B, Delattre, C, Pierre, G, Wadouachi, A, Elboutachfaiti, R, Engel, E, Poughon, L, Michaud, P and Fenoradosoa, TA (2015) Characterization of arabinogalactan-rich mucilage from Cereus triangularis cladodes. Carbohydrate Polymers 127, 372–380.CrossRefGoogle ScholarPubMed
Pholsen, S, Khota, W, Pang, H, Higgs, D and Cai, Y (2016) Characterization and application of lactic acid bacteria for tropical silage preparation. Animal Science Journal 87, 1202–1211.CrossRefGoogle ScholarPubMed
Playne, MJ and McDonald, P (1966) The buffering constituents of herbage and of silage. Journal of the Science of Food and Agriculture 17, 264–268.CrossRefGoogle Scholar
Rodrigues, AM, Pitacas, FI, Reis, CMG and Blasco, M (2016) Nutritional value of opuntia ficus-indica cladodes from Portuguese ecotypes. Bulgarian Journal of Agricultural Science 22, 40–45.Google Scholar
Santos, AO, Ávila, CLS, Pinto, JC, Carvalho, BF, Dias, DR and Schwan, RF (2016) Fermentative profile and bacterial diversity of corn silages inoculated with new tropical lactic acid bacteria. Journal of Applied Microbiology 120, 266–279.CrossRefGoogle ScholarPubMed
Saraiva, CAS, Gonzaga Neto, S, Henriques, LT, Queiroz, MFS, Saraiva, EP, Albuquerque, RPF, Fonseca, VFC and Nascimento, GV (2015) Forage cactus associated with different fiber sources for lactating Sindhi cows: production and composition of milk and ingestive behavior. Revista Brasileira de Zootecnia 44, 60–66.CrossRefGoogle Scholar
Schmidt, RJ, Hu, W, Mills, JA and Kung Junior, L (2009) The development of lactic acid bacteria and Lactobacillus buchneri and their effects on the fermentation of alfalfa silage. Journal of Dairy Science 92, 5005–5010.CrossRefGoogle ScholarPubMed
Shah, AA, Xianjun, Y, Zhihao, D, Junfeng, L and Sao, T (2018) Microbiological and chemical profiles of elephant grass inoculated with and without Lactobacillus plantarum and Pediococcus acidilactici. Archives of Microbiology 200, 311–328.CrossRefGoogle ScholarPubMed
Siegfried, VR, Ruckemann, H and Stumpf, G (1984) Method for the determination of organic acids in silage by high performance liquid chromatography. Landwirtschaftliche Forschung 37, 298–304.Google Scholar
Sifeeldein, A, Yuan, Z, Dong, Z, Li, J, Youns, H and Shao, T (2018) Characterization and identification of lactic acid bacteria by 16S rRNA gene sequence and their effect on the fermentation quality of Elephant Grass (Pennisetum purpureum) Silage. Kafkas Üniversitesi Veteriner Fakültesi Dergisi 24, 123–130.Google Scholar
Silva, RC, Ferreira, MA, Oliveira, JCV, Santos, DC, Gama, MAS, Chagas, JCC, Inácio, JG, Silva, ETS and Pereira, LGR (2018) Orelha de Elefante Mexicana (Opuntia stricta [Haw.] Haw.) spineless cactus as an option in crossbred dairy cattle diet. South African Journal of Animal Science 48, 516–525.CrossRefGoogle Scholar
Vilela, MS, Ferreira, MA, Azevedo, M, Modesto, EC, Farias, I, Guimarães, AV and Bispo, SV (2010) Effect of processing and feeding strategy of the spineless cactus (Opuntia fícus-indica Mill.) for lactating cows: ingestive behavior. Applied Animal Behaviour Science 125, 1–8.CrossRefGoogle Scholar
Weirich, DT, Neres, MA, Hunoff, CA, Ströher, SM, Nath, CD, Sunahara, SMM, Sarto, JRW and Oldoni, T (2018) Microbiological profile and aerobic stability of Tifton 85 bermudagrass silage with or without vacuum and microbial inoculants. Bioscience Journal 34, 151–161.CrossRefGoogle Scholar
Xu, Z, He, H, Zhang, S and Kong, J (2017) Effects of inoculants Lactobacillus brevis and Lactobacillus parafarraginis on the fermentation characteristics and microbial communities of corn stover silage. Scientific Reports 7, 1–9.Google ScholarPubMed
Zanine, AM, Santos, EM, Dórea, JRR, Dantas, PAS, Silva, TC and Pereira, OG (2010) Evaluation of elephant grass silage with the addition of cassava scrapings. Revista Brasileira de Zootecnia 39, 2611–2616.CrossRefGoogle Scholar