Please wait a minute...
Journal of Integrative Agriculture  2020, Vol. 19 Issue (5): 1323-1331    DOI: 10.1016/S2095-3119(19)62854-6
Special Issue: 动物营养合辑Animal Nutrition
Animal Science · Veterinary Medicine Advanced Online Publication | Current Issue | Archive | Adv Search |
Effect of transferring lignocellulose-degrading bacteria from termite to rumen fluid of sheep on in vitro gas production, fermentation parameters, microbial populations and enzyme activity
Ayoub AZIZI1, Afrooz SHARIFI2, Hasan FAZAELI3, Arash AZARFAR1, Arjan JONKER4, Ali KIANI1 
1 Department of Animal Science, Faculty of Agriculture, Lorestan University, Khorramabad 6815144316, Iran
2 Animal Science Research Department, Khuzestan Agricultural and Natural Resources Research and Education Center, Ahvaz 613353341, Iran
3 Animal Science Research Institute, Agriculture, Education and Extension Organization, Karaj 315, Iran
4 Grasslands Research Centre, AgResearch Ltd., Palmerston North 4442, New Zealand
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
Abstract  
The digestive tract of termite (Microcerotermes diversus) contains a variety of lignocellulose-degrading bacteria with exocellulases enzyme activity, not found in the rumen, which could potentially improve fiber degradation in the rumen.  The objectives of the current study were to determine the effect of inoculation of rumen fluid (RF) with three species of bacteria isolated from termite digestive tract, Bacillus licheniformis, Ochrobactrum intermedium, and Microbacterium paludicola, on in vitro gas production (IVGP), fermentation parameters, nutrient disappearance, microbial populations, and hydrolytic enzyme activities with fibrous wheat straw (WS) and date leaf (DL) as incubation substrate.  Inoculation of RF with either of three termite bacteria increased (P<0.05) ammonia-N concentration compared with the control group (free of termite gut bacteria).  Termite bacteria inoculation had no effect (P>0.05) on gas production characteristics, dry matter, organic matter and neutral detergent fiber disappearance, pH, and concentration and composition of volatile fatty acids.  Population of proteolytic bacteria and protozoa, but not cellulolytic bacteria, were increased (P<0.05) when RF was inoculated with termite bacteria with both WS and DL substrates.  Inoculation of RF with termite bacteria increased protease activity, while activities of carboxymethyl-cellulase, microcrystalline-cellulase, α-amylase and filter paper degrading activity remained unchanged (P>0.05).  Overall, the results of this study indicated that transferring lignocellulose-degrading bacteria, isolated from digestive tract of termite, to rumen liquid increased protozoa and proteolytic bacteria population and consequently increased protease activity and ammonia-N concentration in vitro, however, no effect on fermentation and fiber degradation parameters were detected.  These results suggest that the termite bacteria might be rapidly lysed by the rumen microbes before beneficial effects on the rumen fermentation process could occur.
Keywords:  enzyme activity        gas production        lignocellulose-degrading bacteria        microbial population        termite bacteria  
Received: 19 March 2019   Accepted:
Fund: The authors thank Lorestan University, Iran, for its financial support.
Corresponding Authors:  Correspondence Ayoub Azizi, E-mail: azizi.ay@lu.ac.ir, azizi.msc.modarese@gmail.com    

Cite this article: 

Ayoub AZIZI, Afrooz SHARIFI, Hasan FAZAELI, Arash AZARFAR, Arjan JONKER, Ali KIANI. 2020.

Effect of transferring lignocellulose-degrading bacteria from termite to rumen fluid of sheep on in vitro gas production, fermentation parameters, microbial populations and enzyme activity
. Journal of Integrative Agriculture, 19(5): 1323-1331.

Agarwal N. 2000: Estimation of fiber degrading enzyme. In: Chaudhary L C, Agarwal N, Kamra D N, Agarwal D K, eds., Feed Microbiology. CAS Animal Nutrition, IVRI, Izatnagar, India. pp. 278–291.
Allison M J, Cook H M, Jones R J. 1983. Detoxification of 3-hydroxy-4(1H)-pyridone, the goitrogenic metabolite of mimosine, by rumen bacteria from Hawaiian goats. In: XVII Conference on Rumen Function. Chicago, IL, USA.
Allison M J, Mayberry WR, Mcsweeney C S, Stahl D A. 1992. Synergistes jonesii, gen. nov., sp. nov.: A rumen bacterium that degrades toxic pyridinediols. Systematic and Applied Microbiology, 15, 522–529.
AOAC (Association of Official Analytical Chemists). 1995. Official Methods of Analysis. 16th ed. Association of Official Analytical Chemists, Washington, D.C, USA.
Azizi-Shotorkhoft A, Mohammadabadi T, Motamedi M, Chaji M. 2016. Isolation and identi?cation of termite gut symbiotic bacteria with lignocellulose-degrading potential, and their effects on the nutritive value for ruminants of some by-products. Animal Feed Science and Technology, 221, 234–242.
Borji M, 2003. The survey possibility of straw polysaccharides and lignin degradation by isolated microbiota from termites. Ph D thesis, Tarbiat Modares University, Tehran, Iran. (in Persian)
Breznak J A, Brune A. 1994. Role of microorganisms in the digestion of lignocellulose by termites. Annual Review of Entomology, 39, 453–487.
Broderick G, Kang J H. 1980. Automated simultaneous determination of ammonia and total amino acids in ruminal fluid and in vitro media. Journal of Dairy Science, 63, 64–75.
Butler J H, Buckerfield J C. 1979. Digestion of lignin by termites. Soil Biology and Biochemistry, 11, 507–511.
Cartwright N J, Holdom K S. 1973. Enzymatic lignin, its release and utilization by bacteria. Microbes, 8, 7–14.
Cottyn B G, Boucque C V. 1968. Rapid method for the gas-chromatographic determination of volatile fatty acids in rumen fluid. Journal of Agriculture and Food Chemistry, 16, 105–107.
Culliney T W, Grace J K. 2000. Prospects for the biological control of subterranean termites (Isoptera: Rhinotermitidae), with special reference to Coptotermes formosanus. Bulletin of Entomological Research, 90, 9–21.
Dehority B A. 2003. Rumen Microbiology. Nottingham University Press, Nottingham, UK.
Fazaeli H, Mohamadzadeh H, Azizi A, Jelan Z A, Liang J B, Rouzbehan Y, Osman A. 2004. Nutritive value of wheat straw treated with Pleurotus fungi. Asian-Australian Journal of Animal Science, 17, 1681–1688.
Galbe M, Zacchi G. 2007. Pretreatment of lignocellulosic materials for efficient bioethanol production. Biofuels, 108, 41–65.
Gregg K, Hamdorf B, Henderson K, Kopecny J, Wong C. 1998. Genetically modificed ruminal bacteria protect sheep from fuoroacetate poisoning. Applied and Environmental Microbiology, 64, 3496–3498.
Guyader J, Eugène M, Nozière P, Morgavi D P, Doreau M, Martin C. 2014. Influence of rumen protozoa on methane emission in ruminants: A meta-analysis approach. Animal, 8, 1816–1825.
Hungate R E. 1966. The Rumen and its Microbes. Academic Press, New York.
Immig I. 1996. The rumen and hindgut as source of ruminant methanogenesis. Environmental Monitoring and Assessment, 42, 57–72.
Kato K, Kozaki S, Sakurananga M. 1998. Degradation of lignin compounds by bacteria from termite guts. Biotechnology Letters, 20, 459–462.
Krause D O, Bunch R J, Conlan L L, Kennedy P M, Smith W J, Mackie R I, McSweeney C S. 2001. Repeated ruminal dosing of Ruminococcus spp. does not result in persistence, but changes in other microbial populations occur that can be measured with quantitative 16S-rRNA-based probes. Microbiology, 147, 1719–1729.
Krause D O, Denman S E, Mackie R I, Morrison M, Rae A L, Attwood G T, McSweeney C S. 2003. Opportunities to improve fiber degradation in the rumen: Microbiology, ecology, and genomics. FEMS Microbiology Reviews, 27, 663–693.
Krause D O, Smith W J M, Ryan F M E, Mackie R I, McSweeney C S. 2000. Use of 16S-rRNA based techniques to investigate the ecological succession of microbial populations in the immature lamb rumen: Tracking of a specific strain of inoculated Ruminococcus and interactions with other microbial populations in vivo. Microbial Ecology, 38, 365–376.
Lowry O H, Rosebrough N J, Farr A L, Randall R J. 1951. Protein measurement with the pholin-phenol reagent. Journal of Biological Chemistry, 193, 262–275.
Marten G C, Barnes R F. 1980. Prediction of energy digestibility of forages with in vitro rumen fermentation and fungal enzyme systems. In: Pigden W J, Balch C C, Graham M, eds., Standardization of Analytical Methodology for Feeds. International Development Research Center, Ottawa, ON, Canada. pp. 61–71.
McSweeny C S, Allison M J, Mackie R I. 1993. Amino acid utilization by the ruminal bacterium Synergistes jonesii strain 78-1. Archives of Microbiology, 159, 131–135.
Menke K H, Raab L, Salewski A, Steingass H, Fritz D, Schneider W. 1979. The estimation of the digestibility and metabolizable energy content of ruminant feedstuffs from the gas production when they are incubated with rumen liquor in vitro. Journal of Agricultural Science (Camb.), 92, 217–222.
Millen D D, Arrigoni M B, Pacheco R D L. 2016. Rumenology.Springer International Publishing, Switzerland.
Miller J L. 1959. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Analytical Chemistry, 31, 426–428.
Nasehi M, Torbatinejad N M, Zerehdaran S, Safaei A R. 2014. Effect of Pleurotus florida fungi on chemical composition and rumen degradability of wheat and barley straw. Iranian Journal of Applied Animal Science, 4, 257–261.
NRC (National Research Council). 2007. Nutrient Requirements of Small Ruminants: Sheep, Goats, Cervids, and New World Camelids. National Academy of Sciences, Washington, D.C, USA.
Ørskov E R, McDonald I. 1979. The estimation of protein degradability in the rumen from incubation measurements weighed according to rate of passage. Journal of Agricultural Science, 92, 499–503.
Robertson J B, Van Soest P J. 1981. The detergent system of analysis and its application to human foods. In: James W P T, Theander O, eds., The Analysis of Dietary Fiber in Food. Marcel Dekker, NY, USA. pp. 123–158.
Sharp R, Hazlewood G P, Gilbert H J, Donnell A G. 1994. Unmodified and recombinant strains of Lactobacillus plantarum are rapidly lost from the rumen by protozoal predation. Journal of Applied Bacteriology, 76, 110–117.
Siu R G H. 1951. Microbial Decomposition of Cellulose. Reinhold Publishing Corp, New York. p. 531.
Van Soest P J. 1982. Nutritional Ecology of the Ruminant. Cornell University Press, Corvallis, OR, USA. pp. 253–280.
Van Soest P J, Robertson J B, Lewis B A. 1991. Methods for dietary ?ber, neutral detergent ?ber and non-starch polysaccharides in relation to animal nutrition. Journal of Dairy Science, 74, 3583–3597.
Theodorou M K, Williams B A, Dhanoa M S, McAllan A B, France J. 1994. A simple gas production method using a pressure transducer to determine the fermentation kinetics of ruminant feeds. Animal Feed Science and Technology, 48, 185–197. 
Wallace R J, McPherson C A. 1987. Factors affecting the rate of breakdown of bacterial protein in rumen fluid. British Journal of Nutition, 58, 313–323.
Williams A G, Coleman G S. 1991. The Rumen Protozoa. Springer-Verlag, New York.
 
[1] ZHENG Ben-chuan, ZHOU Ying, CHEN Ping, ZHANG Xiao-na, DU Qing, YANG Huan, WANG Xiao-chun, YANG Feng, XIAO Te, LI Long, YANG Wen-yu, YONG Tai-wen. Maizelegume intercropping promote N uptake through changing the root spatial distribution, legume nodulation capacity, and soil N availability[J]. >Journal of Integrative Agriculture, 2022, 21(6): 1755-1771.
[2] ZHOU Lei, XU Sheng-tao, Carlos M. MONREAL, Neil B. MCLAUGHLIN, ZHAO Bao-ping, LIU Jing-hui, HAO Guo-cheng. Bentonite-humic acid improves soil organic carbon, microbial biomass, enzyme activities and grain quality in a sandy soil cropped to maize (Zea mays L.) in a semi-arid region[J]. >Journal of Integrative Agriculture, 2022, 21(1): 208-221.
[3] YANG Ya-jun, XU Hong-xing, WU Zhi-hong, LU Zhong-xian. Effects of inhibitors on the protease profiles and degradation of activated Cry toxins in larval midgut juices of Cnaphalocrocis medinalis (Lepidoptera: Pyralidae)[J]. >Journal of Integrative Agriculture, 2021, 20(8): 2195-2203.
[4] ZHAO Yong-gan, WANG Shu-juan, LIU Jia, ZHUO Yu-qun, LI Yan, ZHANG Wen-chao. Fertility and biochemical activity in sodic soils 17 years after reclamation with flue gas desulfurization gypsum[J]. >Journal of Integrative Agriculture, 2021, 20(12): 3312-3321.
[5] ZHOU Su-mei, ZHANG Man, ZHANG Ke-ke, YANG Xi-wen, HE De-xian, YIN Jun, WANG Chen-yang. Effects of reduced nitrogen and suitable soil moisture on wheat (Triticum aestivum L.) rhizosphere soil microbiological, biochemical properties and yield in the Huanghuai Plain, China[J]. >Journal of Integrative Agriculture, 2020, 19(1): 234-250.
[6] SHAO Yuan-zhi, ZENG Jiao-ke, TANG Hong, ZHOU Yi, LI Wen. The chemical treatments combined with antagonistic yeast control anthracnose and maintain the quality of postharvest mango fruit[J]. >Journal of Integrative Agriculture, 2019, 18(5): 1159-1169.
[7] CHEN Xu, HAN Xiao-zeng, YOU Meng-yang, YAN Jun, LU Xin-chun, William R. Horwath, ZOU Wen-xiu . Soil macroaggregates and organic-matter content regulate microbial communities and enzymatic activity in a Chinese Mollisol[J]. >Journal of Integrative Agriculture, 2019, 18(11): 2605-2618.
[8] RONG Qin-lei, LI Ruo-nan, HUANG Shao-wen, TANG Ji-wei, ZHANG Yan-cai, WANG Li-ying. Soil microbial characteristics and yield response to partial substitution of chemical fertilizer with organic amendments in greenhouse vegetable production[J]. >Journal of Integrative Agriculture, 2018, 17(06): 1432-1444.
[9] TONG Xiao-lei, WANG Zheng-yang, MA Bai-quan, ZHANG Chun-xia, ZHU Ling-cheng, MA Feng-wang, LI Ming-jun. Structure and expression analysis of the sucrose synthase gene family in apple[J]. >Journal of Integrative Agriculture, 2018, 17(04): 847-856.
[10] LUO Jun-yu, ZHANG Shuai, ZHU Xiang-zhen, LU Li-min, WANG Chun-yi, LI Chun-hua, CUI Jin-jie, ZHOU Zhi-guo . Effects of soil salinity on rhizosphere soil microbes in transgenic Bt cotton fields[J]. >Journal of Integrative Agriculture, 2017, 16(07): 1624-1633.
[11] ZHANG Jing, WANG Hai-bin, LIU Juan, CHEN Hao, DU Yan-xiu, LI Jun-zhou, SUN Hong-zheng, PENG Ting, ZHAO Quan-zhi. Influence of water potential and soil type on conventional japonica super rice yield and soil enzyme activities[J]. >Journal of Integrative Agriculture, 2017, 16(05): 1044-1052.
[12] LIU Ce, LAI Yu-jiao, LU Xiao-nan, GUO Ping-ting, LUO Hai-ling. Effect of lactic acid bacteria inoculants on alfalfa (Medicago sativa L.) silage quality: assessment of degradation (in situ) and gas production (in vitro)[J]. >Journal of Integrative Agriculture, 2016, 15(12): 2834-2841.
[13] MIN Wei, GUO Hui-juan, ZHANG Wen, ZHOU Guang-wei, MA Li-juan, YE Jun, HOU Zhen-an. Irrigation water salinity and N fertilization: Effects on ammonia oxidizer abundance, enzyme activity and cotton growth in a drip irrigated cotton fild[J]. >Journal of Integrative Agriculture, 2016, 15(05): 1121-1131.
[14] SHAO Xing-hua , ZHENG Jian-wei. Soil Organic Carbon, Black Carbon, and Enzyme Activity Under Long- Term Fertilization[J]. >Journal of Integrative Agriculture, 2014, 13(3): 517-524.
[15] YI Bing, ZHOU Yu-fei, GAO Ming-yue, ZHANG Zhuang, HAN Yi, YANG Guang-dong, XU Wenjuan, HUANG Rui-dong. Effect of Drought Stress During Flowering Stage on Starch Accumulation and Starch Synthesis Enzymes in Sorghum Grains[J]. >Journal of Integrative Agriculture, 2014, 13(11): 2399-2406.
No Suggested Reading articles found!