An expansin-like protein expands forage cell walls and synergistically increases hydrolysis, digestibility and fermentation of livestock feeds by fibrolytic enzymes
Autoři:
Andres A. Pech-Cervantes aff001; Ibukun M. Ogunade aff001; Yun Jiang aff001; Muhammad Irfan aff003; Kathy G. Arriola aff001; Felipe X. Amaro aff001; Claudio F. Gonzalez aff003; Nicolas DiLorenzo aff001; John J. Bromfield aff001; Diwakar Vyas aff001; Adegbola T. Adesogan aff001
Působiště autorů:
Department of Animal Sciences, University of Florida, Gainesville, FL, United States of America
aff001; Division of Food and Animal Science, Kentucky State University, Frankfort, KY, United States of America
aff002; Department of Microbiology and Cell Science, Interdisciplinary Center for Biotechnology Research, University of Florida, Gainesville, FL, United States of America
aff003
Vyšlo v časopise:
PLoS ONE 14(11)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0224381
Souhrn
Bacterial expansin-like proteins have synergistically increased cellulose hydrolysis by cellulolytic enzymes during the initial stages of biofuel production, but they have not been tested on livestock feeds. The objectives of this study were to: isolate and express an expansin-like protein (BsEXLX1), to verify its disruptive activity (expansion) on cotton fibers by immunodetection (Experiment 1), and to determine the effect of dose, pH and temperature for BsEXLX1 and cellulase to synergistically hydrolyze filter paper (FP) and carboxymethyl cellulose (CMC) under laboratory (Experiment 2) and simulated ruminal (Experiment 3) conditions. In addition, we determined the ability of BsEXLX1 to synergistically increase hydrolysis of corn and bermudagrass silages by an exogenous fibrolytic enzyme (EFE) (Experiment 4) and how different doses of BsEXLX1 and EFE affect the gas production (GP), in vitro digestibility and fermentation of a diet for dairy cows (Experiment 5). In Experiment 1, immunofluorescence-based examination of cotton microfiber treated without or with recombinant expansin-like protein expressed from Bacillus subtilis (BsEXLX1) increased the surface area by > 100% compared to the untreated control. In Experiment 2, adding BsEXLX1 (100 μg/g FP) to cellulase (0.0148 FPU) increased release of reducing sugars compared to cellulase alone by more than 40% (P < 0.01) at optimal pH (4.0) and temperature (50°C) after 24 h. In Experiment 3 and 4, adding BsEXLX1 to cellulase or EFE, synergistically increased release of reducing sugars from FP, corn and bermudagrass silages under simulated ruminal conditions (pH 6.0, 39°C). In Experiment 5, increasing the concentration of BsEXLX1 linearly increased (P < 0.01) GP from fermentation of a diet for dairy cows by up to 17.8%. Synergistic effects between BsEXLX1 and EFE increased in vitro NDF digestibility of the diet by 23.3% compared to the control. In vitro digestibility of hemicellulose and butyrate concentration were linearly increased by BsEXLX1 compared to the control. This study demonstrated that BsEXLX1 can improve the efficacy of cellulase and EFE at hydrolyzing pure substrates and dairy cow feeds, respectively.
Klíčová slova:
Maize – Diet – Filter paper – Recombinant proteins – Cellulose – Fermentation – Hydrolysis – Cellulases
Zdroje
1. Beauchemin K a, Colombatto D, Morgavi DP, Yang WZ. Use of Exogenous Fibrolytic Enzymes to Improve Feed Utilization by Ruminants 1, 2. J Anim Sci. 2003; 37–47. 2003.8114_suppl_2E37x
2. Alvarez G, Pinos-Rodriguez JM, Herrera JG, Garcia JC, Gonzalez SS, Barcena R. Effects of exogenous fibrolytic enzymes on ruminal digestibility in steers fed high fiber rations. Livest Sci. Elsevier B.V.; 2009;121: 150–154. doi: 10.1016/j.livsci.2008.05.024
3. Adesogan AT, Ma ZX, Romero JJ, Arriola KG. Ruminant Nutrition Symposium: Improving cell wall digestion and animal performance with fibrolytic enzymes. J Anim Sci. 2014;92: 1317–1330. doi: 10.2527/jas.2013-7273 24663173
4. Romero JJ, Macias EG, Ma ZX, Martins RM, Staples CR, Beauchemin KA. Improving the performance of dairy cattle with a xylanase-rich exogenous enzyme preparation. 2016; 1–11. doi: 10.3168/jds.2015-10082 26947292
5. Hanna WW and LES. Tropical and subtropical grasses. Forages. Blackwell Publishing; 2007; 245–255.
6. Bernard JK, Castro JJ, Mullis NA, Adesogan AT, West JW, Morantes G. Effect of feeding alfalfa hay or Tifton 85 bermudagrass haylage with or without a cellulase enzyme on performance of Holstein cows. J Dairy Sci. Elsevier; 2010;93: 5280–5285. doi: 10.3168/jds.2010-3111 20965344
7. Archimède H, Eugène M, Marie Magdeleine C, Boval M, Martin C, Morgavi DP, et al. Comparison of methane production between C3 and C4 grasses and legumes. Anim Feed Sci Technol. 2011;166–167: 59–64. doi: 10.1016/j.anifeedsci.2011.04.003
8. Dean DB, Adesogan AT, Krueger N, Littell RC. Effect of fibrolytic enzymes on the fermentation characteristics, aerobic stability, and digestibility of bermudagrass silage. J Dairy Sci. Elsevier; 2005;88: 994–1003. doi: 10.3168/jds.S0022-0302(05)72767-3 15738234
9. Zhang N, Li S, Xiong L, Hong Y, Chen Y. Cellulose-hemicellulose interaction in wood secondary cell-wall. Model Simul Mater Sci Eng. IOP Publishing; 2015;23. doi: 10.1088/0965-0393/23/8/085010
10. Elwakeel E a, Titgemeyer EC, Johnson BJ, Armendariz CK, Shirley JE. Fibrolytic enzymes to increase the nutritive value of dairy feedstuffs. J Dairy Sci. Elsevier; 2007;90: 5226–36. doi: 10.3168/jds.2007-0305 17954763
11. Arriola KG, Kim SC, Staples CR, Adesogan a T. Effect of fibrolytic enzyme application to low- and high-concentrate diets on the performance of lactating dairy cattle. J Dairy Sci. Elsevier; 2011;94: 832–41. doi: 10.3168/jds.2010-3424 21257052
12. Krueger NA, Adesogan AT. Effects of different mixtures of fibrolytic enzymes on digestion and fermentation of bahiagrass hay. Anim Feed Sci Technol. 2008;145: 84–94. doi: 10.1016/j.anifeedsci.2007.05.041
13. Arriola KG, Oliveira AS, Ma ZX, Lean IJ, Giurcanu MC, Adesogan AT. A meta-analysis on the effect of dietary application of exogenous fibrolytic enzymes on the performance of dairy cows. J Dairy Sci. American Dairy Science Association; 2017; http://dx.doi.org/10.3168/jds.2016-12103
14. Tirado-González DN, Miranda-Romero LA, Ruíz-Flores A, Medina-Cuéllar SE, Ramírez-Valverde R, Tirado-Estrada G. Meta-analysis: Effects of exogenous fibrolytic enzymes in ruminant diets. J Appl Anim Res. 2018;46: 771–783. doi: 10.1080/09712119.2017.1399135
15. Liu X, Ma Y, Zhang M. Research advances in expansins and expansion-like proteins involved in lignocellulose degradation. Biotechnol Lett. Springer Netherlands; 2015;37: 1541–1551. doi: 10.1007/s10529-015-1842-0 25957563
16. Ribeiro GO, Gruninger RJ, Badhan A, Mcallister TA. Mining the rumen for fibrolytic feed enzymes Mining the rumen for fibrolytic feed enzymes. 2016; 19–26. doi: 10.2527/af.2016-0019
17. Cosgrove DJ. Loosening of plant cell walls by expansins. Nature. 2000;407: 321–326. doi: 10.1038/35030000 11014181
18. Cosgrove DJ. Plant expansins: diversitty and interactions with plant cell walls. Curr Opin Plant Biol. 2015;25: 162–172. doi: 10.1016/j.pbi.2015.05.014 26057089
19. Bunterngsook B, Mhuantong W, Champreda V, Thamchaiphenet A, Eurwilaichitr L. Identification of novel bacterial expansins and their synergistic actions on cellulose degradation. Bioresour Technol. Elsevier Ltd; 2014;159: 64–71. doi: 10.1016/j.biortech.2014.02.004 24632627
20. Bunterngsook B, Eurwilaichitr L, Thamchaipenet A, Champreda V. Binding characteristics and synergistic effects of bacterial expansins on cellulosic and hemicellulosic substrates. Bioresour Technol. Elsevier Ltd; 2015;176: 129–135. doi: 10.1016/j.biortech.2014.11.042 25460993
21. Saloheimo M, Paloheimo M, Hakola S, Pere J, Swanson B, Nyyssönen E, et al. Swollenin, a Trichoderma reesei protein with sequence similarity to the plant expansins, exhibits disruption activity on cellulosic materials. Eur J Biochem. 2002;269: 4202–4211. doi: 10.1046/j.1432-1033.2002.03095.x 12199698
22. Silveira RL, Skaf MS. Molecular dynamics of the Bacillus subtilis expansin EXLX1: interaction with substrates and structural basis of the lack of activity of mutants †. Phys Chem Chem Phys. Royal Society of Chemistry; 2016;18: 3510–3521. doi: 10.1039/c5cp06674c 26751268
23. Georgelis N, Tabuchi A, Nikolaidis N, Cosgrove DJ. Structure-function analysis of the bacterial expansin EXLX1. J Biol Chem. 2011;286: 16814–16823. doi: 10.1074/jbc.M111.225037 21454649
24. Georgelis N, Nikolaidis N, Cosgrove DJ. Bacterial expansins and related proteins from the world of microbes. Appl Microbiol Biotechnol. 2015;99: 3807–3823. doi: 10.1007/s00253-015-6534-0 25833181
25. Kim ES, Lee HJ, Bang W-G, Choi I-G, Kim KH. Functional characterization of a bacterial expansin from Bacillus subtilis for enhanced enzymatic hydrolysis of cellulose. Biotechnol Bioeng. 2009;102: 1342–53. doi: 10.1002/bit.22193 19058186
26. Halavaty AS, Rich RL, Chen C, Joo JC, Minasov G, Dubrovska I, et al. Structural and functional analysis of betaine aldehyde dehydrogenase from Staphylococcus aureus. Acta Crystallogr Sect D Biol Crystallogr. International Union of Crystallography; 2015;71: 1159–1175. doi: 10.1107/S1399004715004228 25945581
27. Pagliai FA, Gonzalez CF, Lorca GL. Identification of a ligand binding pocket in LdtR from Liberibacter asiaticus. Front Microbiol. 2015;6: 1–13. doi: 10.3389/fmicb.2015.00001
28. Mamiatis T, Fritsch EF, Sambrook J, Engel J. Molecular cloning–A laboratory manual. New York: Cold Spring Harbor Laboratory. 1982, 545 S., 42 $. Acta Biotechnol. Akademie-Verlag; 1985;5: 104. doi: 10.1002/abio.370050118
29. Denicol AC, Dobbs KB, McLean KM, Carambula SF, Loureiro B, Hansen PJ. Canonical WNT signaling regulates development of bovine embryos to the blastocyst stage. Sci Rep. 2013;3: 1266. doi: 10.1038/srep01266 23405280
30. Tovar-Herrera OE, Batista-García RA, Sánchez-Carbente MDR, Iracheta-Cárdenas MM, Arévalo-Niño K, Folch-Mallol JL. A novel expansin protein from the white-rot fungus Schizophyllum commune. PLoS One. 2015;10: 1–17. doi: 10.1371/journal.pone.0122296 25803865
31. Borreani G, Tabacco E. The relationship of silage temperature with the microbiological status of the face of corn silage bunkers. J Dairy Sci. Elsevier; 2010;93: 2620–2629. doi: 10.3168/jds.2009-2919 20494171
32. Alzahal O, Kebreab E, France J, Froetschel M, Mcbride BW. Ruminal Temperature May Aid in the Detection of Subacute Ruminal Acidosis. J Dairy Sci. Elsevier; 2008;91: 202–207. doi: 10.3168/jds.2007-0535 18096941
33. Adney B, Nrel JB. Measurement of Cellulase Activities Laboratory Analytical Procedure (LAP) Issue Date: 08 / 12 / 1996 Measurement of Cellulase Activities Laboratory Analytical Procedure (LAP). Renew Energy. 2008; 8.
34. Chang A, Scheer M, Grote A, Schomburg I. BRENDA, AMENDA and FRENDA the enzyme information system&: new content and tools in 2009. 2009;37: 588–592. doi: 10.1093/nar/gkn820 18984617
35. Romero JJ, Zarate M a, Arriola KG, Gonzalez CF, Silva-Sanchez C, Staples CR, et al. Screening exogenous fibrolytic enzyme preparations for improved in vitro digestibility of bermudagrass haylage. J Dairy Sci. 2015;98: 2555–67. doi: 10.3168/jds.2014-8059 25682133
36. Romero JJ, Zarate MA, Adesogan AT. Effect of the dose of exogenous fibrolytic enzyme preparations on preingestive fiber hydrolysis, ruminal fermentation, and in vitro digestibility of bermudagrass haylage. J Dairy Sci. Elsevier; 2015;98: 406–417. doi: 10.3168/jds.2014-8285 25468699
37. Forage fiber analyses. Agric Handb No 379. 1997; 12–20. doi: 10.1593/neo.08450
38. Mauricio RM, Mould FL, Dhanoa MS, Owen E, Channa KS, Theodorou MK, et al. A semi-automated n vitro gas production technique for ruminant feedstuff evaluation. Anim Feed Sci Technol. 1999;79: 321–330. doi: 10.1016/S0377-8401(99)00033-4
39. Muck RE, Dickerson JT. Storage temperature effects on proteolysis in alfalfa silage. Trans ASAE. American Society of Agricultural and Biological Engineers; 1988;31: 1005–1009.
40. Adesogan AT, Krueger NK, Kim SC. A novel, wireless, automated system for measuring fermentation gas production kinetics of feeds and its application to feed characterization. Anim Feed Sci Technol. 2005;123–124 Pa: 211–223. doi: 10.1016/j.anifeedsci.2005.04.058
41. McDonald I. A revised model for the estimation of protein degradability in the rumen. J Agric Sci. Cambridge University Press; 1981;96: 251–252.
42. Cosgrove DJ, Li LC, Cho HT, Hoffmann-Benning S, Moore RC, Blecker D. The growing world of expansins. Plant Cell Physiol. 2002;43: 1436–1444. doi: 10.1093/pcp/pcf180 12514240
43. Yennawar NH, Li L-C, Dudzinski DM, Tabuchi A, Cosgrove DJ. Crystal structure and activities of EXPB1 (Zea m 1), a beta-expansin and group-1 pollen allergen from maize. Proc Natl Acad Sci U S A. 2006;103: 14664–14671. doi: 10.1073/pnas.0605979103 16984999
44. Georgelis N, Nikolaidis N, Cosgrove DJ. Biochemical analysis of expansin-like proteins from microbes. Carbohydr Polym. Elsevier Ltd.; 2014;100: 17–23. doi: 10.1016/j.carbpol.2013.04.094 24188833
45. Kim IJ, Ko HJ, Kim TW, Nam KH, Choi IG, Kim KH. Binding characteristics of a bacterial expansin (BsEXLX1) for various types of pretreated lignocellulose. Appl Microbiol Biotechnol. 2013;97: 5381–5388. doi: 10.1007/s00253-012-4412-6 23053073
46. Offermann LR, Giangrieco I, Perdue ML, Zuzzi S, Santoro M, Tamburrini M, et al. Elusive Structural, Functional, and Immunological Features of Act d 5, the Green Kiwifruit Kiwellin. J Agric Food Chem. 2015;63: 6567–6576. doi: 10.1021/acs.jafc.5b02159 26146952
47. Hall M, Bansal P, Lee JH, Realff MJ, Bommarius AS. Cellulose crystallinity—A key predictor of the enzymatic hydrolysis rate. FEBS J. 2010;277: 1571–1582. doi: 10.1111/j.1742-4658.2010.07585.x 20148968
48. Bera-Maillet, Christel Ribot Y, Forano E. Fiber-Degrading Systems of Different Strains of the Genus Fibrobacter Christel Be. 2004;70: 2172–2179. doi: 10.1128/AEM.70.4.2172
49. Morgavi DP, Beauchemin KA, Nsereko VL, Rode LM, McAllister TA, Wang Y. Trichoderma enzymes promote Fibrobacter succinogenes S85 adhesion to, and degradation of, complex substrates but not pure cellulose. J Sci Food Agric. 2004;84: 1083–1090. doi: 10.1002/jsfa.1790
50. Himmel ME, Ding S, Johnson DK, Adney WS. Biomass Recalcitrance: Science (80-). 2007; 804–808.
51. Mandebvu P, West JW, Froetschel MA, Hatfield RD, Gates RN, Hill GM. Effect of enzyme or microbial treatment of bermudagrass forages before ensiling on cell wall composition, end products of silage fermentation and in situ digestion kinetics. Anim Feed Sci Technol. 1999;77: 317–329. doi: 10.1016/S0377-8401(98)00247-8
52. McAllister TA, Phillippe RC, Rode LM, Cheng KJ. Effect of the protein matrix on the digestion of cereal grains by ruminal microorganisms. J Anim Sci. 1993;71: 205–212. doi: 10.2527/1993.711205x 7681053
53. Elghandour MMY, Salem AZM, Gonzalez-Ronquillo M, Bórquez JL, Gado HM, Odongo NE, et al. Effects of exogenous enzymes on in vitro gas production kinetics and ruminal fermentation of four fibrous feeds. Anim Feed Sci Technol. 2013;179: 46–53. doi: 10.1016/j.anifeedsci.2012.11.010
54. Jalilvand G, Odongo NE, López S, Naserian A, Valizadeh R, Shahrodi FE, et al. Effects of different levels of an enzyme mixture on in vitro gas production parameters of contrasting forages. Anim Feed Sci Technol. 2008;146: 289–301. doi: 10.1016/j.anifeedsci.2008.01.007
55. Colombatto D, Mould FL, Bhat MK, Owen E. Use of fibrolytic enzymes to improve the nutritive value of ruminant diets A biochemical and in vitro rumen degradation assessment. Anim Feed Sci Technol. 2003;107: 201–209. doi: 10.1016/S0377-8401(03)00126-3
56. Kerff F, Amoroso A, Herman R, Sauvage E, Petrella S, Filée P, et al. Crystal structure and activity of Bacillus subtilis YoaJ (EXLX1), a bacterial expansin that promotes root colonization. Proc Natl Acad Sci U S A. 2008;105: 16876–16881. doi: 10.1073/pnas.0809382105 18971341
57. Phakachoed N, Suksombat W, Colombatto D, Beauchemin KA. Use of fibrolytic enzymes additives to enhance in vitro ruminal fermentation of corn silage. Livest Sci. Elsevier; 2013;157: 100–112. doi: 10.1016/j.livsci.2013.06.020
58. Eun JS, Beauchemin KA. Assessment of the efficacy of varying experimental exogenous fibrolytic enzymes using in vitro fermentation characteristics. Anim Feed Sci Technol. 2007;132: 298–315. doi: 10.1016/j.anifeedsci.2006.02.014
59. Miettinen H, Huhtanen P. Effects of the ratio of ruminal propionate to butyrate on milk yield and blood metabolites in dairy cows. J Dairy Sci. Elsevier; 1996;79: 851–61. doi: 10.3168/jds.S0022-0302(96)76434-2 8792285
60. Hegarty RS, Gerdes R. Hydrogen production and transfer in the rumen. 1999;12: 37–44.
61. Kebreab E, Dijkstra J, Bannink A, France J. Recent advances in modeling nutrient utilization in ruminants. J Anim Sci. 2009;87. doi: 10.2527/jas.2008-1313 18820154
62. Giraldo LA, Ranilla MJ, Tejido ML, Carro MD. Influence of exogenous fibrolytic enzymes and fumarate on methane production, microbial growth and fermentation in Rusitec fermenters. Br J Nutr. 2007;98: 753–761. doi: 10.1017/S0007114507744446 17475087
63. Chung Y-H, Zhou M, Holtshausen L, Alexander TW, McAllister TA, Guan LL, et al. A fibrolytic enzyme additive for lactating Holstein cow diets: Ruminal fermentation, rumen microbial populations, and enteric methane emissions. J Dairy Sci. Elsevier; 2012;95: 1419–1427. doi: 10.3168/jds.2011-4552 22365224
64. Togtokhbayar N, Cerrillo MA, Rodr??guez GB, Elghandour MMMY, Salem AZM, Urankhaich C, et al. Effect of exogenous xylanase on rumen in vitro gas production and degradability of wheat straw. Anim Sci J. 2015;86: 765–771. doi: 10.1111/asj.12364 25923062
Článok vyšiel v časopise
PLOS One
2019 Číslo 11
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Úspěšná resuscitativní thorakotomie v přednemocniční neodkladné péči
- Dlouhodobá recidiva a komplikace spojené s elektivní operací břišní kýly
Najčítanejšie v tomto čísle
- A daily diary study on maladaptive daydreaming, mind wandering, and sleep disturbances: Examining within-person and between-persons relations
- A 3’ UTR SNP rs885863, a cis-eQTL for the circadian gene VIPR2 and lincRNA 689, is associated with opioid addiction
- A substitution mutation in a conserved domain of mammalian acetate-dependent acetyl CoA synthetase 2 results in destabilized protein and impaired HIF-2 signaling
- Molecular validation of clinical Pantoea isolates identified by MALDI-TOF