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Cited by 121Ruminant Nutrition and Digestive PhysiologyProbiotics and Fermented FoodsMycotoxins in Agriculture and Food

Trends in designing microbial silage quality by biotechnological methods using lactic acid bacteria inoculants: a minireview.

Open access
Fabiszewska, Agata U., Zielińska, K. J., Wróbel, B.·2019·World Journal of Microbiology and Biotechnology
DOI 10.1007/s11274-019-2649-2PMC PMC6499736
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Abstract

Ensiling is one of the best known method to preserve fodder. The forage before ensiling intended for silages usually contains a low number of lactic acid bacteria (LAB), so it is necessary to apply starter cultures of selected strains. Traditionally, LAB starter cultures were applied to lower the pH by producing lactic acid and to inhibit the growth of undesirable epiphytic microorganisms by competing for nutrients. Nowadays, LAB inoculants have become an effective tool for creating microbial quality of silages by selecting species with extraordinary features. Epiphytic microflora characteristic of plant material used for the production of silages and the sources of undesirable microflora in the ensiling process are discussed. This review focuses on the most frequently studied issues related to the microbial silage quality and the recent trends in increasing the quality by LAB inoculants, with respect to recent directions for selecting types of modern LAB for inoculation. Among them, the main trends described were prevention of the growth of filamentous fungi and detoxification of mycotoxins by LAB inoculants, inhibition of yeast growth by LAB present in preparations and limiting the development of pathogenic bacterial microflora through controlled fermentation with the participation of LAB and the presence of their metabolites.

AI snapshot

Written from the paper’s full text.

TL;DR

This minireview summarizes how lactic acid bacteria (LAB) inoculants are used to improve silage microbial quality, moving beyond pH reduction to antifungal activity, mycotoxin detoxification, pathogen inhibition, and aerobic stability. It highlights recent molecular and omics tools for understanding silage microbiota and identifies production-scale mycotoxin detoxification as an understudied area.

Key findings

  • Epiphytic LAB are a small fraction of plant microflora, not exceeding 1% of total microflora; LAB numbers range from below the detection limit of 10 CFU/g on alfalfa up to 1 × 10⁷ CFU/g on sorghum and maize, while *Lactobacillus* and *Pediococcus* often do not exceed 1 × 10³ CFU/g.
  • Modern LAB inoculants are selected for antifungal activity against moulds such as *Monilia*, *Aspergillus*, *Penicillium*, and *Fusarium*, and for detoxification of mycotoxins including OTA, patulin, aflatoxins, deoxynivalenol, zearalenone, and fumonisins.
  • In one cited production example, a *L. plantarum* S KKP 2021 p inoculant reduced OTA content by more than 80% after fermentation of meadow sward and maize plants relative to the starting material.
  • In alfalfa silage, inoculants containing *L. plantarum* and *L. buchneri* significantly reduced undesirable microorganisms including *Listeria* spp. and *Cl. perfringens*, and completely eliminated *Salmonella* and *E. coli*; another cited study reported a 55% reduction of deoxynivalenol when fungal-contaminated feed was mixed with bacterial cultures isolated from poultry gastrointestinal tract.

Methods

  • Design: narrative minireview of ensiling and LAB inoculants, with no primary experimental trial reported.
  • Data/sample: synthesizes published literature and cited examples on epiphytic microflora, undesirable silage microflora, commercial inoculant composition, antifungal and mycotoxin-detoxification abilities, and molecular/omics methods; no new sample or dataset is presented.
  • Main analysis: thematic synthesis organized around epiphytic microflora, sources of undesirable microflora, LAB inoculants, prevention of fungal growth and mycotoxin detoxification, and other fermentation trends; cited techniques include PCR-DGGE, LH-PCR, RAPD-PCR, SMRT sequencing, and metabolomic profiling.

Limitations

  • Stated in the paper: mechanisms of interaction between LAB cells and pathogens are not fully revealed; there are only a few reports evaluating LAB mycotoxin detoxification under production conditions; previous studies on reducing toxicity, such as AF adsorption in the gastrointestinal tract, are ambiguous; and a more complete picture of silage microflora is still needed.
  • Evident from the text: as a minireview, it does not describe a systematic search strategy, inclusion criteria, or quantitative meta-analysis, and its conclusions rely on cited studies, some of which are model, in vitro, or patent-based.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1007/s11274-019-2649-2

Cites

Statistics

Nothing to recompute.

Claims the paper makes

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  • Premisecitation

    Microbial additives containing LAB are expected to cause faster pH decline.

    “The expected changes during the ensiling process with the use of microbial additives containing LAB include the dominance of these microorganisms during the fermentation process, an increase in the ratio of lactic acid to other fermentation products (i.e., acetic acid, ethanol), faster pH decline, reduction of proteolysis and increased dry matter recovery (Pahlow et al. 2003; Muck 2013).”
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    Microbial additives containing LAB are expected to increase the ratio of lactic acid to other fermentation products such as acetic acid and ethanol.

    “The expected changes during the ensiling process with the use of microbial additives containing LAB include the dominance of these microorganisms during the fermentation process, an increase in the ratio of lactic acid to other fermentation products (i.e., acetic acid, ethanol), faster pH decline, reduction of proteolysis and increased dry matter recovery (Pahlow et al. 2003; Muck 2013).”
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    Epiphytic microflora greatly determines fermentation of ensiled material through the amount and type of organic acids produced, affecting the stability of the obtained silage.

    “Epiphytic microflora greatly determines the fermentation of ensiled material through the amount and type of organic acids produced, at the same time affecting the stability of the obtained silage (Pahlow et al. 2003; Muck 2013).”
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    Microbial additives containing LAB are expected to cause dominance of LAB during fermentation.

    “The expected changes during the ensiling process with the use of microbial additives containing LAB include the dominance of these microorganisms during the fermentation process, an increase in the ratio of lactic acid to other fermentation products (i.e., acetic acid, ethanol), faster pH decline, reduction of proteolysis and increased dry matter recovery (Pahlow et al. 2003; Muck 2013).”
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  • Interpretationreasoning

    Obtaining silages of good quality and high digestibility requires stimulation of the ensiling process by addition of various preparations.

    “Obtaining silages of good quality and high digestibility requires stimulation of the ensiling process by addition of various preparations.”
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    Premisecitation

    The increase in number of epiphytic microflora is favoured by long drying of meadow grass before harvest, high dry matter content (>40%), rain or high temperatures during drying, soil contamination, and high doses of natural fertilizers.

    “The increase in the number of epiphytic microflora is favoured by long drying of meadow grass before harvest, high dry matter content ( > 40%), occurrence of rain or high temperatures during drying, contamination of forage with soil and use of high doses of natural fertilizers (Pauly and Rodhe 2002).”
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    Premisecitation

    Forage intended for silage usually contains a low number of lactic acid bacteria, so starter cultures of selected strains are necessary.

    “The forage before ensiling intended for silages usually contains a low number of lactic acid bacteria (LAB), so it is necessary to apply starter cultures of selected strains.”
    • Also stated in: § Introduction · plain
      “Natural populations of LAB on plant materials are often heterofermentative and low in number (Ben-Dov et al. 2006).”
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    Premisecitation

    Natural populations of LAB on plant materials are often heterofermentative and low in number.

    “Natural populations of LAB on plant materials are often heterofermentative and low in number (Ben-Dov et al. 2006).”
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    Premisecitation

    The presence of mycotoxins in livestock is still a problem, especially as there is no monitoring of the level of contamination.

    “The presence of mycotoxins in livestock is still a problem, especially as there is no monitoring of the level of contamination (Coffey et al. 2009; Dalie et al. 2010; Oliveira et al. 2013; Rubert et al. 2014).”
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    Due to the carry-over effect, contaminated milk may be a source of mycotoxins for people consuming toxin-contaminated products.

    “Due to the carry-over effect, contaminated milk may be a source of mycotoxins for people consuming toxin-contaminated products.”
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    Premisecitation

    Ensiling is accompanied by fermentation of sugars leading to a decrease in pH and growth of undesirable microorganisms such as yeasts and moulds.

    “The ensiling process in feed is accompanied by the fermentation of sugars that lead to a decrease in pH and the growth of undesirable microorganisms, such as yeasts and moulds (O’Brien et al. 2007).”
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    Premisecitation

    Brusetti et al. reported the presence of B. megaterium, Weissella kimchii, and Enterococcus flavescens in the ensiling of maize.

    “Brusetti et al. (2006) reported the presence of B. megaterium in the ensiling of maize, as well as Weissella kimchii and Enterococcus flavescens.”
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    New PCR-based techniques are uncovering new species of epiphytic microflora on plants.

    “New polymerase chain reaction (PCR)-based techniques are uncovering some new species of epiphytic microflora on plants (Muck 2013).”
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    Premisecitation

    Pang et al. reported the presence of Leuconostoc lactis, E. mundtii, and W. cibaria.

    “Pang et al. (2011a, b) reported the presence of Leuconostoc lactis, E. mundtii and W. cibaria.”
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    Premisecitation

    LAB produce numerous compounds with antibacterial activity and inhibit the growth of fungi of the genera Monilia, Aspergillus, Penicillium, and Fusarium.

    “LAB produce numerous compounds with antibacterial activity and inhibit the growth of fungi of the genera Monilia, Aspergillus, Penicillium and Fusarium.”
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    • cites Dalie et al. 2010 source

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    • Rests on an assumption: LAB strains that show antifungal or antibacterial activity in laboratory conditions retain these properties in silage.

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    Premisecitation

    W. cibaria and W. confusa were the dominant species observed in maize silage.

    “The same group isolated LAB strains from maize, rice, sorghum and alfalfa silages and found that W. cibaria and W. confusa were the dominant species observed in maize silage.”
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    New species isolated from silage include Lactobacillus taiwanensis and P. lolii.

    “New species that have been isolated from silage include Lactobacillus taiwanensis (Wang et al. 2009) and P. lolii (Doi et al. 2009).”
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    Premisecitation

    The most frequently mentioned species in the market are L. plantarum, L. buchneri, E. faecium, and P. acidilactici, and less often L. rhamnosus and Lactococcus lactis.

    “The most frequently mentioned species are L. plantarum, L. buchneri, E. faecium and P.acidilactici, and less often L. rhamnosus and Lactococcus lactis.”
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    Premisecitation

    Cool weather lowers numbers of LAB, and high amounts of LAB often occur at second and third harvests when temperature is highest.

    “Cool weather lowers the numbers of LAB, and high amounts of LAB therefore occurs often at second and third harvests, when the temperature is at its highest in climates like northern Europe for grasses and alfalfa and for early cultivars of maize (Pahlow et al. 2003; Broberg et al. 2007; Comino et al. 2014).”
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    Premisecitation

    The survival time of Salmonella spp. in soil depends on conditions and can last about 33 weeks or longer.

    “The survival time of Salmonella spp. in the soil depends on the conditions and can last about 33 weeks or longer.”
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    Premisecitation

    Many mould species produce mycotoxins toxic to humans and animals, and their presence in feed threatens food safety.

    “Many mould species are also capable of producing secondary metabolites that toxic to human and animals, called mycotoxins, the presence of which in feed evoke a threat to food safety (Van Egmond 2004).”
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    Premisecitation

    Pediococcus species presence has been observed at a number not exceeding 1 × 103 CFU/g.

    “The presence of bacteria of the genus Pediococcus (P. pentosaceus, P. acidilactici, P. damnosus, P. confusa) has been observed at a number that does not exceed 1 × 103 CFU/g (Müller et al. 2001).”
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    On the basis of the fermentative pathway, LAB are divided into homofermentative, relatively heterofermentative, and heterofermentative groups.

    “On the basis of the fermentative pathway, LAB are divided into three groups: homofermentative, relatively heterofermentative and heterofermentative.”
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    Premisecitation

    Reduction of faecal bacteria in soil varies due to temperature, pH, type and humidity of soil, season, and presence of antagonistic microflora.

    “The reduction of faecal bacteria in the soil varies due to the temperature, pH, type and humidity of the soil, as well as the season and presence of an antagonistic microflora in relation to pathogens (You et al. 2006; Holley et al. 2006; Edrington et al. 2009).”
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    Premisecitation

    Production of fungistatic ingredients depends on growth phase, being highest in the logarithmic growth phase, and on temperature, substrate, nutrients, and pH.

    “The production of fungistatic ingredients depends on the growth phase, which is the highest in the logarithmic growth phase, as well as on temperature, substrate, nutrients and pH (Dalie et al. 2010).”
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    LAB have GRAS (generally recognized as safe) status.

    “Moreover, these microorganisms have the GRAS (generally recognized as safe) status.”
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    Premisecitation

    PCR-DGGE enables obtaining information on the genotypes of microorganisms based on the analysis of differences in selected parts of the genome.

    “PCR and its modification, polymerase chain reaction-denaturing gradient gel electrophoresis (PCR-DGGE), enables obtaining information on the genotypes of microorganisms based on the analysis of differences in selected parts of the genome.”
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    Premisecitation

    The beneficial effect of bacteria is explained by increasing the amount of enzymes in food, which facilitates digestion and chelating of mycotoxins.

    “The beneficial effect of bacteria is explained by increasing the amount of enzymes in food, which facilitates digestion and chelating of mycotoxins (El-Nezami et al. 2006).”
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    Premisecitation

    Inoculants containing selected strains of L. buchneri and L. diolivorans can shift silage biochemistry towards limiting lactic acid synthesis and increasing acetic and propionic acid synthesis, thereby ensuring overall stability, aerobic stability and increased biogas yield.

    “Under the influence of inoculants containing selected bacterial strains from L. buchneri and L. diolivorans species, biochemical changes may be aimed at limiting the synthesis of lactic acid, while increasing the synthesis of acetic and propionic acids, and thus, ensuring overall stability, aerobic stability and increased biogas yield from these silages (Herrmann et al. 2015; Nussbaum 2012).”
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    • cites Nussbaum 2012

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    Premisecitation

    Zhou et al. (2016) considered fingerprint techniques such as DGGE to be interesting approaches for investigating microbial population dynamics during ensiling, for example the influence of low temperatures on the evolution of the LAB population responsible for whole plant corn silage fermentation.

    “Zhou et al. (2016) considered fingerprint techniques such as DGGE as interesting approaches to investigate the microbial population dynamics during the ensiling process, e.g., the influence of low temperatures that contribute to creating the various evolution of the LAB population responsible for whole plant corn silage fermentation.”
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    Premisecitation

    Trials to limit absorption of mycotoxins using probiotic LAB are in the research phase, although there are reports of reductions in AFB1 in the gastrointestinal tract of chickens.

    “So far, these trials are in the research phase, although there are reports of reductions in AFB1 in the gastrointestinal tract of chickens (El-Nezami et al. 2000).”
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    Premisecitation

    Length heterogeneity PCR (LH-PCR) uses variation in the length of a particular gene between different microbial species to determine how many species may be active in the environment.

    “Moreover, length heterogeneity PCR (LH-PCR) uses variation in the length of a particular gene between different microbial species to determine how many species may be active in the environment (Muck 2013; Garofalo et al. 2017).”
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    Premisecitation

    Zielińska et al. (2015) acknowledged the usefulness of the RAPD-PCR technique for evaluating the genetic diversity of LAB strains used in silage inoculants.

    “Zielińska et al. (2015) acknowledged the usefulness of RAPD-PCR technique (random amplification of polymorphic DNA) to evaluate the genetic diversity of LAB strains used in silage inoculants.”
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    Premisecitation

    Strains of the genus Lactobacillus, especially L. plantarum and L. rhamnosus, produce metabolites with a strong antifungal effect and demonstrate specific AFB1 removal from fermented roughages.

    “Several other studies have found that strains of the genus Lactobacillus, especially L. plantarum and L. rhamnosus, produce metabolites with a strong antifungal effect and demonstrate specific AFB1 removal, such as from fermented roughages.”
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    • cites Ogunbanwo et al. 2005

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    Premisecitation

    Bacterial community profiles varied during ensiling and were influenced by aerobic exposure, but Lactobacillus spp. dominated during the ensiling process.

    “The bacterial community profiles varied during ensiling and were influenced by aerobic exposure; nevertheless, Lactobacillus spp. dominated during the ensiling process.”
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    • cites Zhou et al. 2016 source

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    • cites Hu et al. 2018

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    • cites Ogunade et al. 2018 source

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    Premisecitation

    Latest in vitro studies on the ability to bind AFB1 by lactobacilli probiotic strains showed that mycotoxin binding was fast and stable.

    “The latest in vitro studies on the ability to bind AFB1 by lactobacilli probiotic strains (including commercially available L. rhamnosus GG and L. casei Shirota, P. freudenreichii ssp., shermanii JS and E. coli) showed that mycotoxin binding was fast (removal from the supernatant was already observed by time zero of contact) and stable (almost no differences in removal were observed after 72 h of”
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    • cites Vinderola and Ritieni 2015 source

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    Premisecitation

    Cyclic peptides composed mainly of proline and phenylalanine, glycine and l-leucine, as well as mevalonolactone, inhibit mould growth at concentrations of mg/cm3, but their antifungal properties are weaker than those of fatty acids.

    “Cyclic peptides composed mainly of proline and phenylalanine, glycine and l-leucine, as well as mevalonolactone, inhibit mould growth at concentrations of mg/cm3, but their antifungal properties are weaker than those of fatty acids (Ström et al. 2002; Magnusson and Schnurer 2005).”
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    Interpretationcitation

    Strains with the highest OTA biodegradation were claimed to be usable in the silage industry as inoculants or feed additives to reduce OTA intake in animal production, considering animals are the most susceptible livestock to OTA toxicity.

    “The strains that evidenced the highest OTA biodegradation were claimed to be used in the silage industry as inoculants or as feed additives to reduce the problem of the intake of OTA in animal production, considering these animals are the most susceptible livestock to the toxic effects of OTA.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Luz et al. 2018 source

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    • Rests on an assumption: In vitro and model-test results on LAB mycotoxin binding or degradation predict efficacy in silage or livestock.

  • Classified as probably not a substantial claim. May combine two claims.

    Premisenone given

    LAB use sugars for the synthesis of lactic acid, thereby reducing the pH and protecting against the development of undesirable microflora.

    “LAB have been used for centuries in the production of fermented food and feed due to its ability to use sugars for the synthesis of lactic acid, thereby reducing the pH and protecting against the development of undesirable microflora.”
    Quote in the paperSubstantial claim

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    Premisecitation

    A preparation based on a strain of L. plantarum S KKP 2021 p has the ability to eliminate ochratoxin A (OTA) and was used for ensiling roughages contaminated with the mycotoxin.

    “One of the latest examples is a preparation based on a strain of L. plantarum S KKP 2021 p with the ability to eliminate OTA, which was used for ensiling of roughages contaminated with the mycotoxin.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Zielińska et al. 2014

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    Interpretationnone given

    The mechanisms of interaction between LAB cells and pathogens are not fully revealed.

    “Still, some limitations refers to the not fully revealed mechanisms of interactions between LAB cells and pathogens.”
    Quote in the paperNot a substantial claim
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  • The paper relies on this without support.

    In vitro and model-test results on LAB mycotoxin binding or degradation predict efficacy in silage or livestock.

    “The effects of the synergistic action of the discussed group of microorganisms was confirmed by few model tests (Vinderola and Ritieni 2015).”
    “The strains that evidenced the highest OTA biodegradation were claimed to be used in the silage industry as inoculants or as feed additives to reduce the problem of the intake of OTA in animal production, considering these animals are the most susceptible livestock to the toxic effects of OTA.”

  • The paper relies on this without support.

    LAB strains that show antifungal or antibacterial activity in laboratory conditions retain these properties in silage.

    “The modern approach of inhibiting the development of mould microflora in fodder involves the use of natural abilities of microorganisms for antagonistic interaction among themselves, and in particular, scientific attention is paid to the diverse species of LAB.”
    “LAB produce numerous compounds with antibacterial activity and inhibit the growth of fungi of the genera Monilia, Aspergillus, Penicillium and Fusarium.”

  • The paper relies on this without support.

    Only a few reports attempt to evaluate the capability of LAB to detoxify mycotoxins under production conditions.

    “Unfortunately, there are only a few reports attempting to evaluate LAB capability of mycotoxin detoxification under production conditions.”

  • The paper relies on this without support.

    Previous studies on the possibility of reducing toxicity, for example aflatoxin adsorption in the gastrointestinal tract, are ambiguous.

    “Previous studies on the possibility of reducing toxicity, e.g., AF adsorption in the gastrointestinal tract, are ambiguous”
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References 52 · Cited by 121

Research works printed but not linked: 4

  1. Dellaglio F, Felis GE (2005) Probiotics scientific aspects. Tannock Caister Academic Press, Norfolk
  2. Nussbaum H (2012) Effects of silage additives based of homo- or heterofermentative lactic acid bacteria on methane yields in the biogas processing In: Proceedings of the XVI international silage conference, 2–4 July 2012, Hameenlinna, Finland. pp 452–453
  3. Ogunbanwo ST, Enitan AM, Emeya P, Okanlawon BM (2005) Influence of lactic acid bacteria on fungal growth and aflatoxin production in ogi, an indigenous fermented food. Adv Food Sci 27:189–194
  4. Pauly TM, Rodhe I (2002) Slurry application on ley-effect of method on the hygienic quality of grass silage In: Proceedings of the XIII International Silage Conference, Auchincruive, Scotland, pp. 410–411.

Authors
Fabiszewska, A. U., Zielińska, K. J., & Wróbel, B.
Affiliations
  • Warsaw University of Life Sciences (PL)
  • Institute of Agricultural and Food Biotechnology (PL)
  • Institute of Technology and Life Sciences (PL)
Corresponding author
Fabiszewska, Agata U.
ORCID
Venue
World Journal of Microbiology and Biotechnology
Publisher
Springer Science and Business Media LLC
Published
2019-05
Volume
35
Issue
5
Pages
76-76
ISSN
  • 0959-3993 (ISSN-L)
  • 1573-0972
DOI
10.1007/s11274-019-2649-2
PMC
PMC6499736
OpenAlex
W2942929015
Semantic Scholar
8595d6c785b12a93791f1c3b0139f9dcf614b285
Cited by
121
References
52
Citations by year
2026: 9 · 2025: 16 · 2024: 18 · 2023: 28 · 2022: 24 · 2021: 12 · 2020: 11 · 2019: 2
FWCI
1.55
Type
journal article
Language
en
Open access
Licence
Locations
  • World Journal of Microbiology and Biotechnology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Agronomy and Crop Science › Ruminant Nutrition and Digestive Physiology
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Mycotoxins in Agriculture and Food
Keywords
silage quality, lactic acid bacteria, starter cultures, microbial inoculants, silage fermentation, forage preservation, epiphytic microflora, filamentous fungi, mycotoxin detoxification, yeast inhibition, pathogenic bacteria, controlled fermentation
MeSH terms
Biotechnology, Fermentation, Food Microbiology, Food Preservation, Fungi, Hydrogen-Ion Concentration, Lactobacillus, Mycotoxins, Plants, Silage, Yeasts, Lactic Acid, Lactobacillales, Food Quality

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