Effect of Lactobacillus plantarum and Lactobacillus buchneri addition on fermentation, bacterial community and aerobic stability in lucerne silage
Huazhe Si A * , Hanlu Liu A , Zhipeng Li A , Weixiao Nan B * , Chunai Jin A , Yutong Sui A and Guangyu Li A CA Jilin Provincial Key Laboratory for Molecular Biology of Special Economic Animals, Institute of Special Animal and Plant Sciences, Chinese Academy of Agricultural Sciences, Changchun, Jilin 130112, China.
B Jilin Agriculture University, Changchun, Jilin, 130118, China.
C Corresponding author. Email: tcslgy@126.com
Animal Production Science 59(8) 1528-1536 https://doi.org/10.1071/AN16008
Submitted: 18 January 2016 Accepted: 28 August 2018 Published: 25 September 2018
Abstract
Changes in the microbial community are closely related to the fermentation of silage. However, how host genetic variation shapes the community structure of the silage microbiota and its metabolic phenotype is poorly understood. The objective of present study was to evaluate the effects of the application of the homo-fermentative Lactobacillus plantarum and hetero-fermentative Lactobacillus buchneri strains to lucerne silage on the fermentation characteristics, aerobic stability, and microbial community and their correlations. The three silages treated with L. plantarum or L. buchneri were well preserved and had significantly lower pH values, butyric acid, propionic acid, and ammonia-N concentrations, and significantly higher residual water-soluble carbohydrate, dry matter and lactic acid contents than the controls. The treated groups had more lactic acid bacteria and lower quantities of other bacteria in their microbial communities. Inoculation of lactic acid bacteria influenced the abundances of other bacteria and controlled the silage fermentation characteristics. L. buchneri inhibited the abundance of Enterobacter_ludwigii to increase the crude protein content, L. plantarum improve the neutral detergent fibre content by affecting the abundance of Arthrobacter_sp._Ens13. In conclusion, the application of L. plantarum and L. buchneri improved the quality of lucerne silage fermentation, and L. buchneri resulted in greater improvements after aerobic exposure.
Additional keywords: aerobic stability, bacteria diversity, silage fermentation.
References
AOAC (1990) ‘Official methods of analysis.’ 15th edn. (Association of Official Analytical Chemists: Arlington, VA)Ávila CLS, Pinto JC, Figueiredo HCP, 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.
| Effects of an indigenous and a commercial Lactobacillus buchneri strain on quality of sugar cane silage.Crossref | GoogleScholarGoogle Scholar |
Axelsson L (2004) Lactic acid bacteria: classification and physiology. In ‘Lactic acid bacteria’. (Eds S Salminen, A Von Wright) pp. 1–63. (Marcel Dekker: New York, NY)
Broderick G A, Kang J H (1980) Automated simultaneous determination of ammonia and total amino acid in ruminal fluid and in vitro media. Journal of Dairy Science 63, 64–75.
| Automated simultaneous determination of ammonia and total amino acid in ruminal fluid and in vitro media.Crossref | GoogleScholarGoogle Scholar |
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Gormley N (2012) Ultra-high-throughput microbial community analysis on the illumine HiSeq and MiSeq platforms. International Society for Microbial Ecology 1–4.
Carvalho BF, Avila JC, Pinto MNP, Schwan RF (2012) Effects of propionic acid and Lactobacillus buchneri (UFLA SIL 72) addition on fermentative and microbiological characteristics of sugar cane silage treated with or without calcium oxide. Grass and Forage Science 67, 462–471.
| Effects of propionic acid and Lactobacillus buchneri (UFLA SIL 72) addition on fermentative and microbiological characteristics of sugar cane silage treated with or without calcium oxide.Crossref | GoogleScholarGoogle Scholar |
Carvalho BF, Ávila CLS, Pinto JC, Neri J, 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.
| Microbiological and chemical profile of sugar cane silage fermentation inoculated with wild strains of lactic acid bacteria.Crossref | GoogleScholarGoogle Scholar |
Contreras-Govea FE, Albrecht KA, Muck RE (2006) Spring yield and silage characteristics of kura clover, winter wheat, and in mixtures. Agronomy Journal 98, 781–787.
| Spring yield and silage characteristics of kura clover, winter wheat, and in mixtures.Crossref | GoogleScholarGoogle Scholar |
Denek N, Can A, Avci M, Aksu T, Durmaz H (2011) The effect of molasses-based pre-fermented juice on the fermentation quality of first-cut Lucerne silage. Grass and Forage Science 66, 243–250.
| The effect of molasses-based pre-fermented juice on the fermentation quality of first-cut Lucerne silage.Crossref | GoogleScholarGoogle Scholar |
Dewettinck T, Hulsbosch W, Hege K, Top E, Verstraete W (2001) Molecular fingerprinting of bacterial populations in groundwater and bottled mineral water. Applied Microbiology & Biotechnology 57, 412–418.
Driehuis F, Oude Elferink SJWH, Van Wikselaar PG (2001) Fermentation characteristics and aerobic stability of grass silage inoculated with Lactobacillus buchneri, with or without homo fermentative lactic acid bacteria. Grass and Forage Science 56, 330–343.
| Fermentation characteristics and aerobic stability of grass silage inoculated with Lactobacillus buchneri, with or without homo fermentative lactic acid bacteria.Crossref | GoogleScholarGoogle Scholar |
Enishi O, Shijimaya K (1998) Changes of chemical composition of plant parts and nutritive value of silage in male sterile rice plant (Oryza sativa L.). Grass and Forage Science 44, 260–265.
Ennahar S, Cai Y, Yasuhito F (2003) Phylogenetic diversity of lactic acid bacteria associated with paddy rice silage as determined by 16S ribosomal DNA analysis. Applied and Environmental Microbiology 69, 444–451.
| Phylogenetic diversity of lactic acid bacteria associated with paddy rice silage as determined by 16S ribosomal DNA analysis.Crossref | GoogleScholarGoogle Scholar |
Filya I (2003) The effect of Lactobacillus buchneri, with or without homofermentative lactic acid bacteria, on the fermentation, aerobic stability and ruminal degradability of wheat, sorghum and maize silages. Journal of Applied Microbiology 95, 1080–1086.
| The effect of Lactobacillus buchneri, with or without homofermentative lactic acid bacteria, on the fermentation, aerobic stability and ruminal degradability of wheat, sorghum and maize silages.Crossref | GoogleScholarGoogle Scholar |
Gatesoupe FJ (1999) The use of probiotics in aquaculture. Aquaculture 180, 147–165.
| The use of probiotics in aquaculture.Crossref | GoogleScholarGoogle Scholar |
Hall MB (2000) Calculation of non-structural carbohydrate content of feeds that contain non-protein nitrogen. University of Florida Bulletin 339, A-25. University of Florida, Gainesville.
Heinl S, Wibberg D, Eikmeyer F, Szczepanowski R, Blom J, Linke B, Goesmann A, Grabherr R, Schwab H, Puhler A, Schluter A (2012) Insights into the completely annotated genome of Lactobacillus buchneri CD034, a strain isolated from stable grass silage. Journal of Biotechnology 161, 153–166.
| Insights into the completely annotated genome of Lactobacillus buchneri CD034, a strain isolated from stable grass silage.Crossref | GoogleScholarGoogle Scholar |
Jones BA, Hatfield RD, Muck RE (1995) Characterization of proteolysis in alfalfa and red clover. Crop Science 35, 537–541.
| Characterization of proteolysis in alfalfa and red clover.Crossref | GoogleScholarGoogle Scholar |
Ke WC, Yang FY, Undersander DJ, Guo XS (2015) Fermentation characteristics, aerobic stability, proteolysis and lipid composition of alfalfa silage ensiled with apple or grape pomace. Animal Feed Science and Technology 202, 12–19.
Kim YS, Kim J, Park SJ (2015) High-throughput 16S rRNA gene sequencing reveals alterations of mouse intestinal microbiota after radiotherapy. Anaerobe 33, 1–7.
| High-throughput 16S rRNA gene sequencing reveals alterations of mouse intestinal microbiota after radiotherapy.Crossref | GoogleScholarGoogle Scholar |
Kleinschmit DH, Kung L (2006a) The effects of Lactobacillus buchneri 40788 and Pediococcus pentosaceus r1094 on the fermentation of corn silage. Journal of Dairy Science 89, 3999–4004.
| The effects of Lactobacillus buchneri 40788 and Pediococcus pentosaceus r1094 on the fermentation of corn silage.Crossref | GoogleScholarGoogle Scholar |
Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeqillumina sequencing platform. Applied and Environmental Microbiology 79, 5112–5120.
| Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeqillumina sequencing platform.Crossref | GoogleScholarGoogle Scholar |
Kung L (2001) Silage fermentation and additives. Science and Tehcnology in the Feed Industry 17, 145–159.
Lane DJ (1991) 16S/23S rRNA sequencing. In ‘Nucleic acid techniques in bacteria systematics’. (Ed. EGM Stackebrandt) pp. 75–115. (Wiley: New York)
Li Y, Nishino N (2011) Effects of inoculation of Lactobacillus rhamnosus and Lactobacillus buchneri on fermentation, aerobic stability and microbial communities in whole crop corn silage. Japan. Grassland Science 57, 184–191.
| Effects of inoculation of Lactobacillus rhamnosus and Lactobacillus buchneri on fermentation, aerobic stability and microbial communities in whole crop corn silage. Japan.Crossref | GoogleScholarGoogle Scholar |
Lundberg DS, Yourstone S, Mieczkowski P, Jones CD, Dangl JL (2013) Practical innovations for high-throughput amplicon sequencing. Nature Methods 10, 999–1002.
| Practical innovations for high-throughput amplicon sequencing.Crossref | GoogleScholarGoogle Scholar |
McAllister TA, Feniuk R, Mir Z, Mir P, Selinger LB, Cheng KJ (1998) Inoculants for alfalfa silage: effects on aerobic stability, digestibility and the growth performance of feed lot steers. Livestock Production Science 53, 171–181.
| Inoculants for alfalfa silage: effects on aerobic stability, digestibility and the growth performance of feed lot steers.Crossref | GoogleScholarGoogle Scholar |
McDonald P (1991) ‘The biochemistry of silage.’ (Chalcombe Publications: Marlow, Buckinghamshire)
Mceniry J, O’Kiely P, Clipson NJW, Forristal PD, Doyle EM (2009) Assessing the impact of various ensilage factors on the fermentation of grass silage using conventional culture and bacterial community analysis techniques. Journal of Applied Microbiology 108, 1584–1593.
McGarvey JA, Franco RB, Palumbo JD, Hnasko R, Stanker L, Mitloehner FM (2013) Bacterial population dynamics during the ensiling of Medicago sativa (alfalfa) and subsequent exposure to air. Journal of Applied Microbiology 114, 1661–1670.
| Bacterial population dynamics during the ensiling of Medicago sativa (alfalfa) and subsequent exposure to air.Crossref | GoogleScholarGoogle Scholar |
Muck RE (1987) Dry matter level effects on alfalfa silage quality. I. Nitrogen transformations. Transactions of the ASAE 30, 7–14.
| Dry matter level effects on alfalfa silage quality. I. Nitrogen transformations.Crossref | GoogleScholarGoogle Scholar |
Muck RE, Dickerson JT (1988) Storage temperature effects on proteolysis in alfalfa silage. Transactions of the ASAE 31, 1005–1009.
| Storage temperature effects on proteolysis in alfalfa silage.Crossref | GoogleScholarGoogle Scholar |
Nkosi BD, Meeske R, Palic D, Langa T, Leeuw KJ, Groenewald IB (2009) Effects of ensiling whole crop maize with bacterial inoculants on the fermentation, aerobic stability, and growth performance of lambs. Animal Feed Science and Technology 154, 193–203.
| Effects of ensiling whole crop maize with bacterial inoculants on the fermentation, aerobic stability, and growth performance of lambs.Crossref | GoogleScholarGoogle Scholar |
Pahlow G, Muck RE, Driehuis F, Oude Elferink SJWH, Spoelstra SF (2003) Microbiology of ensiling. Agronomy (Basel) 42, 31–94.
Park SJ, Kim J, Lee J S, Rhee SK, Kim H (2014) Characterization of the fecal microbiome in different swine groups by high-throughput sequencing. Anaerobe 157–162.
Pedroso AF, Nussio LG, Loures DRS, Paziani SDF, Ribeiro JL, Mari LJ, Horii J (2008) Fermentation, losses, and aerobic stability of sugar cane treated with chemical or bacterial additives. Scientia Agrícola 65, 589–594.
| Fermentation, losses, and aerobic stability of sugar cane treated with chemical or bacterial additives.Crossref | GoogleScholarGoogle Scholar |
Schmidt P, Mari LJ, Nussio LG, Pedroso ADF, Paziani SDF, Wechsler FS (2007) Chemical and biological additives in the ensiling of sugar cane. 1. Chemical composition, dry matter intake, digestibility and ingestive behavior. Revista Brasileira De Zootecnia (Brazilian Journal of Animal Science) 36, 1666–1675.
| Chemical and biological additives in the ensiling of sugar cane. 1. Chemical composition, dry matter intake, digestibility and ingestive behavior.Crossref | GoogleScholarGoogle Scholar |
Seale DR (1986) Bacterial inoculants as silage additives. The Journal of Applied Bacteriology 61, 9s–26s.
Sonja NH, Martens SD, Avila P, Hoedtke S (2012) The effect of inoculant and sucrose addition on the silage quality of tropical forage legumes with varying ensilability. Animal Feed Science and Technology 174, 201–210.
Tao L, Zhou H, Zhang N, Si B, Tu Y, Ma T, Diao Q (2017) Effects of different source additives and wilt conditions on the pH value, aerobic stability, and carbohydrate and protein fractions of alfalfa silage. Animal Science Journal 88, 99–106.
| Effects of different source additives and wilt conditions on the pH value, aerobic stability, and carbohydrate and protein fractions of alfalfa silage.Crossref | GoogleScholarGoogle Scholar |
Van Soest PJ, Robertson JB, Lewis BA (1991) Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74, 3583–3597.
| Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition.Crossref | GoogleScholarGoogle Scholar |
Van Vuuren AM, Huhtanen P, Dulphy JP (1995) Improving the feeding and health value of ensiled forages. In ‘Recent developments in the nutrition of herbivores. Proceedings of the 4th international symposium on the nutrition of herbivores’. (Eds M Journet, E Grenet, MH Farce, M Therie) pp. 279–307. (INRA Editions: Paris, France)
Wang X, Haruta S, Wang P, Ishii M, Igarashi Y, Cui Z (2006) Diversity of a stable enrichment culture which is useful for silage inoculant and its succession in alfalfa silage. FEMS Microbiology Ecology 57, 106–115.
| Diversity of a stable enrichment culture which is useful for silage inoculant and its succession in alfalfa silage.Crossref | GoogleScholarGoogle Scholar |
Weinberg ZG, Muck RE (1996) New trends and opportunities in the development and use of inoculants for silage. FEMS Microbiology Reviews 19, 53–68.
| New trends and opportunities in the development and use of inoculants for silage.Crossref | GoogleScholarGoogle Scholar |
Yitbarek MB, Tamir B (2014) Silage additives: review. Open Journal of Applied Sciences 4, 258–274.