Animal Bioscience

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
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A lysing polysaccharide monooxygenase from Aspergillus niger effectively facilitated rumen microbial fermentation of rice straw

  • Ting Li (Jiangxi Province Key Laboratory of Animal Nutrition/Engineering Research Center of Feed Development, Jiangxi Agricultural University) ;
  • Kehui OuYang (Jiangxi Province Key Laboratory of Animal Nutrition/Engineering Research Center of Feed Development, Jiangxi Agricultural University) ;
  • Qinghua Qiu (Jiangxi Province Key Laboratory of Animal Nutrition/Engineering Research Center of Feed Development, Jiangxi Agricultural University) ;
  • Xianghui Zhao (Jiangxi Province Key Laboratory of Animal Nutrition/Engineering Research Center of Feed Development, Jiangxi Agricultural University) ;
  • Chanjuan Liu (Jiangxi Province Key Laboratory of Animal Nutrition/Engineering Research Center of Feed Development, Jiangxi Agricultural University)
  • Received : 2024.01.15
  • Accepted : 2024.04.21
  • Published : 2024.10.01
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Abstract

Objective: This study investigated the impact of Aspergillus niger lysing polysaccharide monooxygenase (AnLPMO) on in vitro rumen microbial fermentation of rice straw. Methods: AnLPMO was heterologously expressed in Escherichia coli. Fourier transform infrared spectrometry and X-ray photoelectron spectroscopy analyzed the surface structure of rice straw after AnLPMO treatment. Two in vitro experiments, coupled with 16S high-throughput sequencing and quantitative real-time polymerase chain reaction techniques, assessed the influence of AnLPMO on rumen microbial fermentation of rice straw. Results: AnLPMO exhibited peak activity at 40℃ and pH 6.5, with a preference for rice straw xylan hydrolysis, followed by Avicel. AnLPMO application led to the fractional removal of cellulose and hemicelluloses and a notable reduction in the levels of carbon elements and C-C groups present on the surface of rice straw. Compared to the control (no AnLPMO), supplementing AnLPMO at 1.1 to 2.0 U significantly enhanced in vitro digestibility of dry matter (IVDMD, p<0.01), total gas production (p<0.01), and concentrations of total volatile fatty acids (VFA, p<0.01), acetate (p<0.01), and ammonia-N (p<0.01). Particularly, the 1.4 U AnLPMO group showed a 14.8% increase in IVDMD. In the second experiment, compared to deactivated AnLPMO (1.4 U), supplementing bioactive AnLPMO at 1.4 U increased IVDMD (p = 0.01), total gas production (p = 0.04), and concentrations of total VFA (p<0.01), propionate (p<0.01), and ammonia-N (p<0.01), with a limited 9.6% increase in IVDMD. Supplementing AnLPMO stimulated the growth of ruminal bacterial taxa facilitating fiber degradation, including Proteobacteria, Spirochaetes, Succinivibrio, Rikenellaceae_RC9_Gut_Group, Prevotelaceae_UCG-003, Desulfovibrio, Fibrobacter succinogenes, Ruminococcus albus, R. flavefaciens, Prevotella bryantii, P. ruminicola, and Treponema bryantii. Conclusion: These findings highlight AnLPMO's potential as a feed additive for improving rice straw utilization in ruminant production.

Keywords

Acknowledgement

The current study was funded by the Project of Jiangxi Provincial Department of Education (GJJ2200414), Central Leading Local Science and Technology Development Special Project (20221ZDF03017), Key Research and Development Projects of Jiangxi Province (20232BBF60009), and Natural Science Foundation of Jiangxi Province (20224ACB205007).

References

  1. Singh R, Srivastava M, Shukla A. Environmental sustainability of bioethanol production from rice straw in India: a review. Renew Sustain Energy Rev 2016;54:202-16. https://doi.org/10.1016/j.rser.2015.10.005
  2. Aquino D, Del Barrio A, Trach NX, et al. Rice straw-based fodder for ruminants. In: Gummert M, Hung NV, Chivenge P, Douthwaite B, editors. Sustainable Rice Straw Management. Cham, Switzerland: Springer; 2020. pp. 111-29. https://doi.org/10.1007/978-3-030-32373-8_7
  3. Kim W, Yahaya MS, Goto M. Effects of steam explosion on the chemical composition and rumen degradability of rice (Oryza sativa L.) straw. Grassl Sci 2005;51:139-44. https://doi.org/10.1111/j.1744-697X.2005.00019.x
  4. Sarnklong C, Cone JW, Pellikaan W, Hendriks WH. Utilization of rice straw and different treatments to improve its feed value for ruminants: a review. Asian-Australas J Anim Sci 2010;23:680-92. https://doi.org/10.5713/ajas.2010.80619
  5. Vandhana TM, Reyre JL, Sushmaa D, Berrin JG, Bissaro B, Madhuprakash J. On the expansion of biological functions of lytic polysaccharide monooxygenases. New Phytol 2022;233:2380-96. https://doi.org/10.1111/nph.17921
  6. Frommhagen M, Sforza S, Westphal AH, et al. Discovery of the combined oxidative cleavage of plant xylan and cellulose by a new fungal polysaccharide monooxygenase. Biotechnol Biofuels 2015;8:101. https://doi.org/10.1186/s13068-015-0284-1
  7. Srivastava S, Jhariya U, Purohit HJ, Dafale NA. Synergistic action of lytic polysaccharide monooxygenase with glycoside hydrolase for lignocellulosic waste valorization: a review. Biomass Convers Biorefin 2023;13:8727-45. https://doi.org/10.1007/s13399-021-01736-y
  8. Moon M, Lee JP, Park GW, Lee JS, Park HJ, Min K. Lytic polysaccharide monooxygenase (LPMO)-derived saccharification of lignocellulosic biomass. Bioresour Technol 2022;359:127501. https://doi.org/10.1016/j.biortech.2022.127501
  9. Hu D, Zhao X. Characterization of a new xylanase found in the rumen metagenome and its effects on the hydrolysis of wheat. J Agric Food Chem 2022;70:6493-502. https://doi.org/10.1021/acs.jafc.2c00827
  10. Zhang W, Pan K, Liu C, et al. Recombinant Lentinula edodes xylanase improved the hydrolysis and in vitro ruminal fermentation of soybean straw by changing its fiber structure. Int J Biol Macromol 2020;151:286-92. https://doi.org/10.1016/j.ijbiomac.2020.02.187
  11. Sommart K, Parker DS, Rowlinson P, Wanapat M. Fermentation characteristics and microbial protein synthesis in an in vitro system using cassava, rice straw and dried ruzi grass as substrates. Asian-Australas J Anim Sci 2000;13:1084-93. https://doi.org/10.5713/ajas.2000.1084
  12. Weatherburn MW. Phenol-hypochlorite reaction for determination of ammonia. Anal Chem 1967;39:971-4. https://doi.org/10.1021/ac60252a045
  13. Chen XL, Wang JK, Wu YM, Liu JX. Effects of chemical treatments of rice straw on rumen fermentation characteristics, fibrolytic enzyme activities and populations of liquidand solid-associated ruminal microbes in vitro. Anim Feed Sci Technol 2008;141:1-14. https://doi.org/10.1016/j.anifeedsci.2007.04.006
  14. Koike S, Yabuki H, Kobayashi Y. Interaction of rumen bacteria as assumed by colonization patterns on untreated and alkali-treated rice straw. Anim Sci J 2014;85:524-31. https://doi.org/10.1111/asj.12176
  15. Aski AL, Borghei A, Zenouzi A, Ashrafi N, Taherzadeh MJ. Effect of steam explosion on the structural modification of rice straw for enhanced biodegradation and biogas production. Bioresources 2019;14:464-85. https://doi.org/10.15376/biores.14.1.464-485
  16. Chen L, Li J, Lu M, Guo X, Zhang H, Han L. Integrated chemical and multi-scale structural analyses for the processes of acid pretreatment and enzymatic hydrolysis of corn stover. Carbohydr Polym 2016;141:1-9. https://doi.org/10.1016/j.carbpol.2015.12.079
  17. Chundawat SPS, Venkatesh B, Dale BE. Effect of particle size based separation of milled corn stover on AFEX pretreatment and enzymatic digestibility. Biotechnol Bioeng 2007;96:219-31. https://doi.org/10.1002/bit.21132
  18. Zhao L, Boluk Y. XPS and IGC characterization of steam treated triticale straw. Appl Surf Sci 2010;257:180-5. https://doi.org/10.1016/j.apsusc.2010.06.060
  19. Cao W, Wang Z, Zeng Q, Shen C. 13C NMR and XPS characterization of anion adsorbent with quaternary ammonium groups prepared from rice straw, corn stalk and sugarcane bagasse. Appl Surf Sci 2016;389:404-10. https://doi.org/10.1016/j.apsusc.2016.07.095
  20. Sain M, Panthapulakkal S. Bioprocess preparation of wheat straw fibers and their characterization. Ind Crops Prod 2006;23:1-8. https://doi.org/10.1016/j.indcrop.2005.01.006
  21. Pu XX, Zhang XM, Li QS, et al. Comparison of in situ ruminal straw fiber degradation and bacterial community between buffalo and Holstein fed with high-roughage diet. Front Microbiol 2023;13:1079056. https://doi.org/10.3389/fmicb.2022.1079056
  22. Tokuda G, Mikaelyan A, Fukui C, et al. Fiber-associated spirochetes are major agents of hemicellulose degradation in the hindgut of wood-feeding higher termites. Proc Natl Acad Sci U S A 2018;115:E11996-2004. https://doi.org/10.1073/pnas.1810550115
  23. Shah T, Ding L, Ud Din A, et al. Differential effects of natural grazing and feedlot feeding on yak fecal microbiota. Front Vet Sci 2022;9:791245. https://doi.org/10.3389/fvets.2022.791245
  24. Qiu X, Qin X, Chen L, et al. Serum biochemical parameters, rumen fermentation, and rumen bacterial communities are partly driven by the breed and sex of cattle when fed high-grain diet. Microorganisms 2022;10:323. https://doi.org/10.3390/microorganisms10020323
  25. Uddin MK, Mahmud MR, Hasan S, Peltoniemi O, Oliviero C. Dietary micro-fibrillated cellulose improves growth, reduces diarrhea, modulates gut microbiota, and increases butyrate production in post-weaning piglets. Sci Rep 2023;13:6194. https://doi.org/10.1038/s41598-023-33291-z
  26. Shen T, Yue Y, He T, et al. The association between the gut microbiota and Parkinson's disease, a meta-analysis. Front Aging Neurosci 2021;13:636545. https://doi.org/10.3389/fnagi.2021.636545
  27. Shi MJ, Ma ZX, Tian YJ, Ma C, Li YD, Zhang XW. Effects of corn straw treated with CaO on rumen degradation characteristics and fermentation parameters and their correlation with microbial diversity in rumen. Anim Feed Sci Technol 2022;292:115403. https://doi.org/10.1016/j.anifeedsci.2022.115403
  28. Voordouw G. The genus Desulfovibrio: the centennial. Appl Environ Microbiol 1995;61:2813-9. https://doi.org/10.1128/aem.61.8.2813-2819.1995
  29. Vahidi MF, Gharechahi J, Behmanesh M, Ding XZ, Han JL, Salekdeh GH. Diversity of microbes colonizing forages of varying lignocellulose properties in the sheep rumen. PeerJ 2021;9:e10463. https://doi.org/10.7717/peerj.10463
  30. Toit Md, Huch M, Cho GS, Franz CMAP. The genus Streptococcus. In: Holzapfel WH, Wood BJB, editors. Lactic acid bacteria: biodiversity and taxonomy. Hoboken, NJ, USA: John Wiley & Sons, Ltd; 2014. p.457-505. https://doi.org/10.1002/9781118655252.ch28
  31. Pu G, Hou L, Du T, et al. Effects of short-term feeding with high fiber diets on growth, utilization of dietary fiber, and microbiota in pigs. Front Microbiol 2022;13:963917. https://doi.org/10.3389/fmicb.2022.963917
  32. Xu Y, Aung M, Sun Z, et al. Ensiling of rice straw enhances the nutritive quality, improves average daily gain, reduces in vitro methane production and increases ruminal bacterial diversity in growing Hu lambs. Anim Feed Sci Technol 2023;295:115513. https://doi.org/10.1016/j.anifeedsci.2022.115513
  33. Xue B, Wu M, Yue S, et al. Changes in rumen bacterial community induced by the dietary physically effective neutral detergent fiber levels in goat diets. Front Microbiol 2022;13:820509. https://doi.org/10.3389/fmicb.2022.820509
  34. Strompl C, Tindall BJ, Jarvis GN, Lunsdorf H, Moore ERB, Hippe H. A re-evaluation of the taxonomy of the genus Anaerovibrio, with the reclassification of Anaerovibrio glycerini as Anaerosinus glycerini gen. nov., comb. nov., and Anaerovibrio burkinabensis as Anaeroarcus burkinensis [corrig.] gen. nov., comb. nov. Int J Syst Evol Microbiol 1999;49:1861-72. https://doi.org/10.1099/00207713-49-4-1861
  35. Li L, Qu M, Liu C, et al. Expression of a recombinant Lentinula edodes xylanase by Pichia pastoris and its effects on ruminal fermentation and microbial community in in vitro incubation of agricultural straws. Front Microbiol 2018;9:2944. https://doi.org/10.3389/fmicb.2018.02944
  36. Tajima K, Aminov RI, Nagamine T, Matsui H, Nakamura M, Benno Y. Diet-dependent shifts in the bacterial population of the rumen revealed with real-time PCR. Appl Environ Microbiol 2001;67:2766-74. https://doi.org/10.1128/AEM.67.6.2766-2774.2001
  37. Purushe J, Fouts DE, Morrison M, et al. Comparative genome analysis of Prevotella ruminicola and Prevotella bryantii: insights into their environmental niche. Microb Ecol 2010;60:721-9. https://doi.org/10.1007/s00248-010-9692-8
  38. Abdelmegeid MK, Elolimy AA, Zhou Z, Lopreiato V, McCann JC, Loor JJ. Rumen-protected methionine during the peripartal period in dairy cows and its effects on abundance of major species of ruminal bacteria. J Anim Sci Biotechnol 2018;9:17. https://doi.org/10.1186/s40104-018-0230-8
  39. Salfer IJ, Crawford CE, Rottman LW, Harvatine KJ. The effects of feeding rations that differ in neutral detergent fiber and starch within a day on the daily pattern of key rumen microbial populations. JDS Commun 2021;2:334-9. https://doi.org/10.3168/jds.2021-0099
  40. Koike S, Yabuki H, Kobayashi Y. Validation and application of real-time polymerase chain reaction assays for representative rumen bacteria. Anim Sci J 2007;78:135-41. https://doi.org/10.1111/j.1740-0929.2007.00417.x