REVIEW PAPER
 
KEYWORDS
TOPICS
ABSTRACT
Fermentation and enzymolysis are commonly used biological treatment methods to treat forage, especially unconventional one. Both these treatments can improve the nutritional value of the forage, reduce the content of anti-nutritional factors and ameliorate the digestibility of feed. Microbial-enzymatic synergism treatment constitutes an organic combination of fermentation and enzymolysis, which can strengthen the processing of forage and achieve a superior feeding effect. In this review, the objectives of microbial-enzymatic synergism treatment are summarized, including decomposing macromolecular nutrients, decreasing anti-nutritional factors and increasing specific target products. The substrates, microbes and enzymes used in microbe-enzyme synergy are also summarized. Furthermore, the similarities and differences between one-step and two-step technological processes of synergy are presented and the current evaluation system of microbial-enzymatic synergism treatment is reviewed. Existing problems and future development directions of microbial-enzymatic synergism treatment are also discussed.
FUNDING
This study was supported by the Special project of the Ministry of Science and Technology of China (2017YFE0129900), National Natural Science Foundation of China (32072771).
CONFLICT OF INTEREST
The authors declare that there is no conflict of interest.
 
REFERENCES (57)
1.
Abada E., Al-Fifi Z., Osman M., 2019. Bioethanol production with carboxymethyl cellulase of Pseudomonas poae using castor bean (Ricinuscommunis L.) cake. Saudi J. Biol. Sci. 26, 866–871, https://doi.org/10.1016/j.sjbs....
 
2.
Ahmed A., Zulkifli I., Farjam A.S., Abdullah N., Liang J.B., Awad E.A., 2014. Effect of solid state fermentation on nutrient content and ileal amino acids digestibility of canola meal in broiler chickens. Ital. J. Anim. Sci. 13, https://doi.org/10.4081/ijas.2....
 
3.
Alokika, Singh B., 2019. Production, characteristics, and biotechnological applications of microbial xylanases. Appl. Microbiol. Biotechnol. 103, 8763–8784, https://doi.org/10.1007/s00253....
 
4.
Alshelmani M.I., Loh T.C., Foo H.L., Lau W.H., Sazili A.Q., 2014. Biodegradation of palm kernel cake by cellulolytic and hemicellulolytic bacterial cultures through solid state fermentation. Sci. World J. 2014, 729852, https://doi.org/10.1155/2014/7....
 
5.
Atuhaire A.M., Kabi F., Okello S., Mugerwa S., Ebong C., 2016. Optimizing bio-physical conditions and pre-treatment options for breaking lignin barrier of maize stover feed using white rot fungi. Anim. Nutr. 2, 361–369, https://doi.org/10.1016/j.anin....
 
6.
Bartkiene E., Bartkevics V., Krungleviciute V., Juodeikiene G., Zadeike D., Baliukoniene V., Bakutis B., Zelvyte R., Santini A., Cizeikiene D., 2018. Application of hydrolases and probiotic Pediococcus acidilactici BaltBio 01 strain for cereal by-products conversion to bio-product for food/feed. Int. J. Food Sci. Nutr. 69, 165–175, https://doi.org/10.1080/096374....
 
7.
Bernardo B.d.S., Ramos R.F., Callegaro K., Daroit D.J., 2019. Co-production of proteases and bioactive protein hydrolysates from bioprocessing of feather meal. Braz. Arch. Biol. Technol. 62, e19180621, https://doi.org/10.1590/1678-4....
 
8.
Chen L., Li J., Dong Z., Shao T., 2019. Effects of lactic acid bacteria inoculants and fibrolytic enzymes on the fermentation quality, in vitro degradability, ruminal variables and microbial communities of high-moisture alfalfa silage. Grassland Sci. 65, 216–225, https://doi.org/10.1111/grs.12....
 
9.
Cheng Y.-H., Hsiao F.S.-H., Wen C.-M., Wu C.-Y., Dybus A., Yu Y.-H., 2019. Mixed fermentation of soybean meal by protease and probiotics and its effects on the growth performance and immune response in broilers. J. Appl. Anim. Res. 47, 339–348, https://doi.org/10.1080/097121....
 
10.
Chiang G., Lu W.Q., Piao X.S., Hu J.K., Gong L.M., Thacker P.A., 2010. Effects of feeding solid-state fermented rapeseed meal on performance, nutrient digestibility, intestinal ecology and intestinal morphology of broiler chickens. Asian-Australas. J. Anim. Sci. 23, 263–271, https://doi.org/10.5713/ajas.2....
 
11.
Chu Y.T., Lo C.T., Chang S.C., Lee T.T., 2017. Effects of Trichoderma fermented wheat bran on growth performance, intestinal morphology and histological findings in broiler chickens. Ital. J. Anim. Sci. 16, 82–92, https://doi.org/10.1080/182805....
 
12.
Chuang W.Y., Lin W.C., Hsieh Y.C., Huang C.M., Chang S.C., Lee T.-T., 2019. Evaluation of the combined use of Saccharomyces cerevisiae and Aspergillus oryzae with Phytase fermentation products on growth, inflammatory, and intestinal morphology in broilers. Animals 9, 1051, https://doi.org/10.3390/ani912....
 
13.
Coban H.B., Demirci A., 2014. Enhanced submerged Aspergillus ficuum phytase production by implementation of fed-batch fermentation. Bioprocess Biosyst. Eng. 37, 2579–2586, https://doi.org/10.1007/s00449....
 
14.
Dai C., Ma H., He R., Huang L., Zhu S., Ding Q., Luo L., 2017. Improvement of nutritional value and bioactivity of soybean meal by solid-state fermentation with Bacillus subtilis. LWT 86, 1–7, https://doi.org/10.1016/j.lwt.....
 
15.
de Brito A.R., Reis N.d.S., Silva T.P., Ferreira B.R.C., Trovatti U.A.P., de Assis S.A., Paranhos da S.E.G., Aguiar-Oliveira E., Oliveira J.R., Franco M., 2017. Comparison between the univariate and multivariate analysis on the partial characterization of the endoglucanase produced in the solid state fermentation by Aspergillus oryzae ATCC 10124. Prep. Biochem. Biotechnol. 47, 977–985, https://doi.org/10.1080/108260....
 
16.
de Oliveira C.C., Santos de Souza A.K., Soaresde Castro R.J., 2019. Bioconversion of chicken feather meal by Aspergillus niger: Simultaneous enzymes production using a cost-effective feedstock under solid state fermentation. Indian J. Microbiol. 59, 209–216, https://doi.org/10.1007/s12088....
 
17.
Ding W.R., Long R.J., Guo X.S., 2013. Effects of plant enzyme inactivation or sterilization on lipolysis and proteolysis in alfalfa silage. J. Dairy Sci. 96, 2536–2543, https://doi.org/10.3168/jds.20....
 
18.
Dossou S., Koshio S., Ishikawa M., Yokoyama S., El Basuini M.F., Zaineldin A.I., Mzengereza K., Moss A., Dawood M.A.O., 2019. Effects of replacing fishmeal with fermented and non-fermented rapeseed meal on the growth, immune and antioxidant responses of red sea bream (Pagrus major). Aquac. Nutr. 25, 508–517, https://doi.org/10.1111/anu.12....
 
19.
Du J., Cheng L., Hong Y., Deng Y., Li Z., Li C., Gu Z., 2018. Enzyme assisted fermentation of potato pulp: An effective way to reduce water holding capacity and improve drying efficiency Food Chem. 258, 118–123, https://doi.org/10.1016/j.food....
 
20.
Feng J., Liu X., Xu Z.R., Lu Y.P., Liu Y.Y., 2007. Effect of fermented soybean meal on intestinal morphology and digestive enzyme activities in weaned piglets. Dig. Dis. Sci. 52, 1845, https://doi.org/10.1007/s10620....
 
21.
Ghosh K., Ray A.K., Ringo E., 2019. Applications of plant ingredients for tropical and sub-tropical freshwater finfish: possibilities and challenges. Rev. Aquac. 11, 793–815, https://doi.org/10.1111/raq.12....
 
22.
Goodarzi Boroojeni F., Kozłowski K., Jankowski J., Senz M., Wiśniewska M., Boros D., Drażbo A., Zentek J., 2018. Fermentation and enzymatic treatment of pea for turkey nutrition. Anim. Feed Sci. Technol. 237, 78–88, https://doi.org/10.1016/j.anif....
 
23.
Goodarzi Boroojeni F.G., Senz M., Kozlowski K., Boros D., Wisniewska M., Rose D., Maenner K., Zentek J., 2017. The effects of fermentation and enzymatic treatment of pea on nutrient digestibility and growth performance of broilers. Animal 11, 1698–1707, https://doi.org/10.1017/S17517....
 
24.
Hmidet N., Jemil N., Nasri M., 2019. Simultaneous production of alkaline amylase and biosurfactant by Bacillus methylotrophicus DCS1: application as detergent additive. Biodegradation 30, 247–258, https://doi.org/10.1007/s10532....
 
25.
Jazi V., Boldaji F., Dastar B., Hashemi S.R., Ashayerizadeh A., 2017. Effects of fermented cottonseed meal on the growth performance, gastrointestinal microflora population and small intestinal morphology in broiler chickens. Br. Poult. Sci. 58, 402–408, https://doi.org/10.1080/000716....
 
26.
Jia X., Peng X., Liu Y., Han Y., 2017. Conversion of cellulose and hemicellulose of biomass simultaneously to acetoin by thermophilic simultaneous saccharification and fermentation. Biotechnol. Biofuels 10, 232, https://doi.org/10.1186/s13068....
 
27.
Kung L., Jr., Taylor C.C., Lynch M.P., Neylon J.M., 2003. The effect of treating alfalfa with Lactobacillus buchneri 40788 on silage fermentation, aerobic stability, and nutritive value for lactating dairy cows. J. Dairy Sci. 86, 336–343, https://doi.org/10.3168/jds.S0....
 
28.
Lee F.H., Wan S.Y., Foo H.L., Loh T.C., Mohamad R., Rahim R.A., Idrus Z., 2019. Comparative study of extracellular proteolytic, cellulolytic, and hemicellulolytic enzyme activities and biotransformation of palm kernel cake biomass by lactic acid bacteria isolated from Malaysian foods. Int. J. Mol. Sci. 20, 4979, https://doi.org/10.3390/ijms20....
 
29.
Mohd Azlan P.M., Jahromi M.F., Ariff M.O., Ebrahimi M., Candyrine S.C.L., Liang J.B., 2018. Aspergillus terreus treated rice straw suppresses methane production and enhances feed digestibility in goats. Trop. Anim. Health Prod. 50, 565–571, https://doi.org/10.1007/s11250....
 
30.
Moniruzzaman M., Bae J.H., Won S.H., Cho S.J., Chang K.H., Bai S.C., 2018. Evaluation of solid-state fermented protein concentrates as a fish meal replacer in the diets of juvenile rainbow trout, Oncorhynchus mykiss. Aquac. Nutr. 24, 1198–1212, https://doi.org/10.1111/anu.12....
 
31.
Mukherjee R., Chakraborty R., Dutta A., 2016. Role of fermentation in improving nutritional quality of soybean meal – a review. Asian-Australas. J. Anim. Sci. 29, 1523–1529, https://doi.org/10.5713/ajas.1....
 
32.
Odinot E., Fine F., Sigoillot J.-C. et al., 2017. a two-step bioconversion process for canolol production from rapeseed meal combining an Aspergillus niger feruloyl esterase and the fungus Neolentinus lepideus. Microorganisms 5, 67, https://doi.org/10.3390/microo....
 
33.
Ohara A., dos Santos J.G., Figueira Angelotti J.A., Menezes Barbosa P.d.P., Goncalves Dias F.F., Bagagli M.P., Sato H.H., Soares de Castro R.J., 2018. a multicomponent system based on a blend of agroindustrial wastes for the simultaneous production of industrially applicable enzymes by solid-state fermentation. Food Sci. Technol. 38, suppl. 1, 131–137, https://doi.org/10.1590/1678-4....
 
34.
Olukomaiya O., Fernando C., Mereddy R., Li X., Sultanbawa Y., 2019. Solid-state fermented plant protein sources in the diets of broiler chickens: a review. Anim. Nutr. 5, 319–330, https://doi.org/10.1016/j.anin....
 
35.
Orts A., Tejada M., Parrado J., Paneque P., Garcia C., Hernandez T., Gomez-Parrales I., 2019. Production of biostimulants from okara through enzymatic hydrolysis and fermentation with Bacillus licheniformis: comparative effect on soil biological properties. Environ. Technol. 40, 2073–2084, https://doi.org/10.1080/095933....
 
36.
Pedraza L., Flores A., Toribio H., Quintero R., Le Borgne S., Moss-Acosta C., Martinez A., 2016. Sequential thermochemical hydrolysis of corncobs and enzymatic saccharification of the whole slurry followed by fermentation of solubilized sugars to ethanol with the ethanologenic strain Escherichia coli MS04. Bioenergy Res. 9, 1046–1052, https://doi.org/10.1007/s12155....
 
37.
Reddy M.R., Reddy K.S., Chouhan Y.R., Bee H., Reddy G., 2017. Effective feather degradation and keratinase production by Bacillus pumilus GRK for its application as bio-detergent additive. Bioresour. Technol. 243, 254–263, https://doi.org/10.1016/j.bior....
 
38.
Salim A.A., Grbavcic S., Sekuljica N., Vukasinovic-Sekulic M., Jovanovic J., Tanaskovic S.J., Lukovic N., Knezevic-Jugovic Z., 2019. Enzyme production by solid-state fermentation on soybean meal: a comparative study of conventional and ultrasound-assisted extraction methods. Biotechnol. Appl. Biochem. 66, 361–368, https://doi.org/10.1002/bab.17....
 
39.
Schmidt J., Szakacs G., Cenkvari E., Sipocz J., Urbanszki K., Tengerdy R.P., 2001. Enzyme assisted ensiling of alfalfa with enzymes by solid substrate fermentation. Bioresour. Technol. 76, 207–212, https://doi.org/10.1016/S0960-....
 
40.
Shi C., He J., Yu J., Yu B., Mao X., Zheng P., Huang Z., Chen D., 2016. Physicochemical properties analysis and secretome of Aspergillus niger in fermented rapeseed meal. PLoS ONE 11, e0153230, https://doi.org/10.1371/journa....
 
41.
Su L.-W., Cheng Y.-H., Hsiao F.S.-H., Han J.-C., Yu Y.-H., 2018. Optimization of mixed solid-state fermentation of soybean meal by Lactobacillus species and Clostridium butyricum. Pol. J. Microbiol. 67, 297–305, https://doi.org/10.21307/pjm-2....
 
42.
Tang X., Xiang R., Chen S., Yang S., Liu H., Fang R., Li A., 2018. Effects of fermented cottonseed meal and enzymatic hydrolyzed cottonseed meal on amino acid digestibility and metabolic energy in white leghorn rooster. Pak. J. Zool. 50, 957–962, https://doi.org/10.17582/journ....
 
43.
Teng P.Y., Chang C.L., Huang C.M., Chang S.C., Lee T.T., 2017. Effects of solid-state fermented wheat bran by Bacillus amyloliquefaciens and Saccharomyces cerevisiae on growth performance and intestinal microbiota in broiler chickens. Ital. J. Anim. Sci. 16, 552–562, https://doi.org/10.1080/182805....
 
44.
Tie Y., Li L., Liu J., Liu C., Fu J., Xiao X., Wang G., Wang J., 2020. Two-step biological approach for treatment of rapeseed meal. J. Food Sci. 85, 340–348, https://doi.org/10.1111/1750-3....
 
45.
Vong W.C., Hua X.Y., Liu S.-Q., 2018. Solid-state fermentation with Rhizopus oligosporus and Yarrowia lipolytica improved nutritional and flavor properties of okara. LWT 90, 316–322, https://doi.org/10.1016/j.lwt.....
 
46.
Wang K., Niu M., Song D., Liu Y., Wu Y., Zhao J., Li S., Lu B., 2019. Evaluation of biochemical and antioxidant dynamics during the co-fermentation of dehusked barley with Rhizopus oryzae and Lactobacillus plantarum. J. Food Biochem. 44, e13106, https://doi.org/10.1111/jfbc.1....
 
47.
Wang L., Ou M.S., Nieves I., Erickson J.E., Vermerris W., Ingram L.O., Shanmugam K.T., 2015a. Fermentation of sweet sorghum derived sugars to butyric acid at high titer and productivity by a moderate thermophile Clostridium thermobutyricum at 50 °C. Bioresour. Technol. 198, 533–539, https://doi.org/10.1016/j.bior....
 
48.
Wang L., Zhang B., Han J., Zheng Y., Li J., Shan A., 2015b. Optimization of hydrolysis condition of blood meal by Bacillus subtilis with response surface methodology. Int. Biodeterior. Biodegradation. 104, 112–117, https://doi.org/10.1016/j.ibio....
 
49.
Wang L., Zhou H., He R., Xu W., Mai K., He G., 2016. Effects of soybean meal fermentation by Lactobacillus plantarum P8 on growth, immune responses, and intestinal morphology in juvenile turbot (Scophthalmus maximus L.). Aquaculture 464, 87–94, https://doi.org/10.1016/j.aqua....
 
50.
Wang Z., Cui Y., Liu P., Zhao Y., Wang L., Liu Y., Xie J., 2017. Small peptides isolated from enzymatic hydrolyzate of fermented soybean meal promote endothelium-independent vasorelaxation and ACE inhibition. J. Agric. Food Chem. 65, 10844–10850, https://doi.org/10.1021/acs.ja....
 
51.
Wiseman M., McBride B., Li J., Wey D., Zhu J., de Lange C.F.M., 2017. Effects of steeped or fermented distillers dried grains with solubles on growth performance in weanling pigs. J. Anim. Sci. 95, 3563–3578, https://doi.org/10.2527/jas.20....
 
52.
Xiong J.L., Wang Z.J., Miao L.H., Meng F.T., Wu L.Y., 2016. Growth performance and toxic response of broilers fed diets containing fermented or unfermented cottonseed meal. J. Anim. Feed Sci. 25, 348–353, https://doi.org/10.22358/jafs/....
 
53.
Yang J., Wu X.-b., Chen H.-l., Sun-waterhouse D., Zhong H.-b., Cui C., 2019. a value-added approach to improve the nutritional quality of soybean meal byproduct: Enhancing its antioxidant activity through fermentation by Bacillus amyloliquefaciens SWJS22. Food Chem. 272, 396–403, https://doi.org/10.1016/j.food....
 
54.
Yasar S., Tosun R., 2018. Predicting chemical, enzymatic and nutritional properties of fermented barley (Hordeum vulgare L.) by second derivate spectra analysis from attenuated total reflectance-Fourier transform infrared data and its nutritional value in Japanese quails. Arch. Anim. Nutr. 72, 407–423, https://doi.org/10.1080/174503....
 
55.
Zeng C., Zhao R., Ma M., Zeng Z., Gong D., 2017. Mutagenesis and characterization of a Bacillus amyloliquefaciens strain for Cinnamomum camphora seed kernel oil extraction by aqueous enzymatic method. AMB Express 7, 154, https://doi.org/10.1186/s13568....
 
56.
Zheng Y., Zhang H., Wang D., Gao P., Shan A., 2014. Strain development and optimized fermentation conditions for blood meal using Aspergillus niger and Aspergillus oryzae. J. Microbiol. Methods 101, 70–80, https://doi.org/10.1016/j.mime....
 
57.
Zhu J., Gao M., Zhang R. et al., 2017. Effects of soybean meal fermented by L. plantarum, B. subtilis and S. cerevisiae on growth, immune function and intestinal morphology in weaned piglets. Microb. Cell Factories 16, 191, https://doi.org/10.1186/s12934....
 
 
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