Evaluation of a Colombian oregano oil (Lippia origanoides Kunth) and a novel yeast product from Pichia guilliermondii, alone or in combination, on rumen fermentation, methanogenesis and the microbiome in the rumen simulation technique
In this study, Lippia origanoides Kunth, native to the Alto Patía region in Southwest Colombia, and Pichia guilliermondii LV196, an inactivated yeast from the germplasm bank of Agrosavia (Colombian Agricultural Research Corporation), alone or combined, were tested for their long-term effect on rumen...
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Frontiers in Animal Science
2024
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Acceso en línea: | https://www.frontiersin.org/articles/10.3389/fanim.2022.951789 http://hdl.handle.net/20.500.12324/38782 |
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Arreglo y sistemas de cultivo - F08 Orégano Fermentación acética Lippia Metano Levadura Hortalizas y plantas aromáticas http://aims.fao.org/aos/agrovoc/c_34066 http://aims.fao.org/aos/agrovoc/c_27442 http://aims.fao.org/aos/agrovoc/c_37446 http://aims.fao.org/aos/agrovoc/c_4784 http://aims.fao.org/aos/agrovoc/c_8480 |
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Arreglo y sistemas de cultivo - F08 Orégano Fermentación acética Lippia Metano Levadura Hortalizas y plantas aromáticas http://aims.fao.org/aos/agrovoc/c_34066 http://aims.fao.org/aos/agrovoc/c_27442 http://aims.fao.org/aos/agrovoc/c_37446 http://aims.fao.org/aos/agrovoc/c_4784 http://aims.fao.org/aos/agrovoc/c_8480 Ramos Morales, Eva Bolton, Emily Lyons, Laura Carreño, David Jones, Eleanor Mayorga Mogollón, Olga Lucía Ariza Nieto, Claudia Janeth Newbold, Charles James Evaluation of a Colombian oregano oil (Lippia origanoides Kunth) and a novel yeast product from Pichia guilliermondii, alone or in combination, on rumen fermentation, methanogenesis and the microbiome in the rumen simulation technique |
description |
In this study, Lippia origanoides Kunth, native to the Alto Patía region in Southwest Colombia, and Pichia guilliermondii LV196, an inactivated yeast from the germplasm bank of Agrosavia (Colombian Agricultural Research Corporation), alone or combined, were tested for their long-term effect on rumen fermentation and methanogenesis whilst also characterising their effect on bacterial and methanogen communities. Whereas essential oils act through selective inhibition of microbial groups, yeasts are thought to work through the selective stimulation of key microbes in the rumen. We hypothesized that yeast supplementation could modulate the antimicrobial effect of a high thymol-containing oregano oil, allowing a more efficient feed utilization whilst decreasing methane production. When added to a rumen simulating fermentor (RUSITEC), L. origanoides Kunth at 132 µL/d had a detrimental effect on rumen fermentation which was accompanied by a reduction in the relative abundance of protozoa and fungi and a profound impact on the bacterial and archaeal communities. P. guilliermondii LV196 at 0.5 g/L, however, had no effect on fermentation parameters or nutrient utilization, and neither changes in microbial abundances or in the structure of bacterial and archaeal communities were observed. P. guilliermondii LV196 did not stimulate microbial numbers nor activity and, consequently we could not test whether it could have counterbalanced the antimicrobial effect of the essential oil. Future studies need to both investigate lower levels of essential oil addition, but also to re-examine the effects of P. guillermondii in the rumen and/or to replace it with other yeast of known biological activity when combined with oils extracted from L. origanoides Kunth. |
format |
article |
author |
Ramos Morales, Eva Bolton, Emily Lyons, Laura Carreño, David Jones, Eleanor Mayorga Mogollón, Olga Lucía Ariza Nieto, Claudia Janeth Newbold, Charles James |
author_facet |
Ramos Morales, Eva Bolton, Emily Lyons, Laura Carreño, David Jones, Eleanor Mayorga Mogollón, Olga Lucía Ariza Nieto, Claudia Janeth Newbold, Charles James |
author_sort |
Ramos Morales, Eva |
title |
Evaluation of a Colombian oregano oil (Lippia origanoides Kunth) and a novel yeast product from Pichia guilliermondii, alone or in combination, on rumen fermentation, methanogenesis and the microbiome in the rumen simulation technique |
title_short |
Evaluation of a Colombian oregano oil (Lippia origanoides Kunth) and a novel yeast product from Pichia guilliermondii, alone or in combination, on rumen fermentation, methanogenesis and the microbiome in the rumen simulation technique |
title_full |
Evaluation of a Colombian oregano oil (Lippia origanoides Kunth) and a novel yeast product from Pichia guilliermondii, alone or in combination, on rumen fermentation, methanogenesis and the microbiome in the rumen simulation technique |
title_fullStr |
Evaluation of a Colombian oregano oil (Lippia origanoides Kunth) and a novel yeast product from Pichia guilliermondii, alone or in combination, on rumen fermentation, methanogenesis and the microbiome in the rumen simulation technique |
title_full_unstemmed |
Evaluation of a Colombian oregano oil (Lippia origanoides Kunth) and a novel yeast product from Pichia guilliermondii, alone or in combination, on rumen fermentation, methanogenesis and the microbiome in the rumen simulation technique |
title_sort |
evaluation of a colombian oregano oil (lippia origanoides kunth) and a novel yeast product from pichia guilliermondii, alone or in combination, on rumen fermentation, methanogenesis and the microbiome in the rumen simulation technique |
publisher |
Frontiers in Animal Science |
publishDate |
2024 |
url |
https://www.frontiersin.org/articles/10.3389/fanim.2022.951789 http://hdl.handle.net/20.500.12324/38782 |
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RepoAGROSAVIA387822024-06-27T13:47:49Z Evaluation of a Colombian oregano oil (Lippia origanoides Kunth) and a novel yeast product from Pichia guilliermondii, alone or in combination, on rumen fermentation, methanogenesis and the microbiome in the rumen simulation technique Ramos Morales, Eva Bolton, Emily Lyons, Laura Carreño, David Jones, Eleanor Mayorga Mogollón, Olga Lucía Ariza Nieto, Claudia Janeth Newbold, Charles James Arreglo y sistemas de cultivo - F08 Orégano Fermentación acética Lippia Metano Levadura Hortalizas y plantas aromáticas http://aims.fao.org/aos/agrovoc/c_34066 http://aims.fao.org/aos/agrovoc/c_27442 http://aims.fao.org/aos/agrovoc/c_37446 http://aims.fao.org/aos/agrovoc/c_4784 http://aims.fao.org/aos/agrovoc/c_8480 In this study, Lippia origanoides Kunth, native to the Alto Patía region in Southwest Colombia, and Pichia guilliermondii LV196, an inactivated yeast from the germplasm bank of Agrosavia (Colombian Agricultural Research Corporation), alone or combined, were tested for their long-term effect on rumen fermentation and methanogenesis whilst also characterising their effect on bacterial and methanogen communities. Whereas essential oils act through selective inhibition of microbial groups, yeasts are thought to work through the selective stimulation of key microbes in the rumen. We hypothesized that yeast supplementation could modulate the antimicrobial effect of a high thymol-containing oregano oil, allowing a more efficient feed utilization whilst decreasing methane production. When added to a rumen simulating fermentor (RUSITEC), L. origanoides Kunth at 132 µL/d had a detrimental effect on rumen fermentation which was accompanied by a reduction in the relative abundance of protozoa and fungi and a profound impact on the bacterial and archaeal communities. P. guilliermondii LV196 at 0.5 g/L, however, had no effect on fermentation parameters or nutrient utilization, and neither changes in microbial abundances or in the structure of bacterial and archaeal communities were observed. P. guilliermondii LV196 did not stimulate microbial numbers nor activity and, consequently we could not test whether it could have counterbalanced the antimicrobial effect of the essential oil. Future studies need to both investigate lower levels of essential oil addition, but also to re-examine the effects of P. guillermondii in the rumen and/or to replace it with other yeast of known biological activity when combined with oils extracted from L. origanoides Kunth. Orégano-Origanum vulgare 2024-01-19T16:53:43Z 2024-01-19T16:53:43Z 2022-06-25 2022 article Artículo científico http://purl.org/coar/resource_type/c_2df8fbb1 info:eu-repo/semantics/article https://purl.org/redcol/resource_type/ART http://purl.org/coar/version/c_970fb48d4fbd8a85 https://www.frontiersin.org/articles/10.3389/fanim.2022.951789 2673-6225 http://hdl.handle.net/20.500.12324/38782 10.3389/fanim.2022.951789 reponame:Biblioteca Digital Agropecuaria de Colombia instname:Corporación colombiana de investigación agropecuaria AGROSAVIA eng Frontiers in Animal Science 3 3 1 13 Arango, J., Ruden, A., Martinez-Baron, D., Loboguerrero, A. M., Berndt, A., Chacón, M., et al. (2020). Ambition meets reality: Achieving GHG emission reduction targets in the livestock sector of Latin America. Front. Sustain. Food Syst. 4. doi: 10.3389/fsufs.2020.00065 Bass, B. E., Tsai, T.-C., Yang, H., Perez, V., Holzgraefe, D., Chewning, J., et al. (2019). Influence of a whole yeast product (Pichia guilliermondii) fed throughout gestation and lactation on performance and immune parameters of the sow and litter. J. Anim. Sci. 97, 1671–1678. doi: 10.1093/jas/skz060 Belanche, A., Doreau, M., Edwards, J. E., Moorby, J. M., Pinloche, E., and Newbold, C. J. (2012). Shifts in the rumen microbiota due to the type of carbohydrate and level of protein ingested by dairy cattle are associated with changes in rumen fermentation. J. Nutr. 142, 1684–1689. doi: 10.3945/ jn.112.159574 Belanche, A., Pinloche, E., Preskett, D., and Newbold, C. J. (2016). Effects and mode of action of chitosan and ivy fruit saponins on the microbiome, fermentation and methanogenesis in the rumen simulation technique. FEMS Microbiol. Ecol. 92, 1. doi: 10.1093/femsec/fiv160 Benchaar, C., Calsamiglia, S., Chaves, A. V., Fraser, G. R., Colombatto, D., McAllister, T. A., et al. (2008). A review of plant-derived essential oils in ruminant nutrition and production. Anim. Feed Sci. Technol. 145, 209–228. doi: 10.1016/ j.anifeedsci.2007.04.014 Benchaar, C., and Greathead, H. (2011). Essential oils and opportunities to mitigate enteric methane emissions from ruminants. Anim. Feed Sci. Technol. 166– 167, 338–355. doi: 10.1016/j.anifeedsci.2011.04.024 Benjamini, Y., and Hochberg, Y. (1955). Controlling the false discovery rate— a practical and powerful approach to multiple testing. J. R. Stat. Soc Ser. B Stat. Methodol. 57, 289–300 Betancourt, L., Hume, M., Rodrıguez, F., Nisbet, D., Sohail, M. U., and ́ Afanador-Tellez, G. (2019). Effects of Colombian oregano essential oil (Lippia origanoides kunth) and eimeria species on broiler production and cecal microbiota. Poult. Sci. 98, 4777–4786. doi: 10.3382/ps/pez193 Calsamiglia, S., Busquet, M., Cardozo, P. W., Castillejos, L., and Ferret, A. (2007). Invited review: Essential oils as modifiers of rumen microbial fermentation. J. Anim. Sci. 90, 2580–2595. doi: 10.3168/jds.2006-644 Chaparro, M. L., Cé spedes, E., Cruz, M., Castillo-Saldarriaga, C. R., and Gómez Alvarez, M. I. (2017). Fluidized bed drying of a granulated prototype based on a potential probiotic yeast Meyerozyma guilliermondii: Selection of process parameters and drying protectant. Rev. Mex. Ing. Quim. 16, 347–357. Cobellis, G., Trabalza-Marinucci, M., and Yu, Z. (2016). Critical evaluation of essential oils as rumen modifiers in ruminant nutrition: A review. Sci. Total Environ., 545–546, 556-568. doi: 10.1016/j.scitotenv.2015.12.103 Czerkawski, J. W., and Breckenridge, G. (1977). Design and development of a long-term rumen simulation technique (RUSITEC). Br. J. Nutr. 38, 371–384. doi: 10.1079/BJN19770102 de la Fuente, G., Belanche, A., Girwood, S. E., Pinloche, E., Wilkinson, T., and Newbold, C. J. (2014). Pros and cons of ion-torrent next generation sequencing versus terminal restriction fragment length polymorphism T-RFLP for studying the rumen bacterial community. PLoS One 9, 1–13. doi: 10.1371/ journal.pone.0101435 Evans, J. D., and Martin, S. A. (2000). Effects of thymol on ruminal microorganisms. Curr. Microbiol. 41, 336–340. doi: 10.1007/s002840010145 Friedman, N., Jami, E., and Mizrahi, I. (2017). Compositional and functional dynamics of the bovine rumen methanogenic community across different developmental stages. Environ. Microbiol. 19, 3365–3373. doi: 10.1111/1462- 2920.13846 Henderson, G., Cox, F., Ganesh, S., Jonker, A., Young, W., and Janssen, P. H. (2015). Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range. Sci. Rep. 5, 14567. doi: 10.1038/srep14567 Kamke, J., Kittelmann, S., Soni, P., Li, Y., Tavendale, M., Ganesh, S., et al. (2016). Rumen metagenome and metatranscriptome analyses of low methane yield sheep reveals a sharpea-enriched microbiome characterised by lactic acid formation and utilisation. Microbiome 4, 56. doi: 10.1186/s40168-016-0201-2 Legendre, P., and Anderson, M. J. (1999). Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol. Monogr. 69, 1–24. doi: 10.1890/0012-9615(1999)069[0001: DBRATM]2.0.CO;2 Macheboeuf, D., Morgavi, D. P., Papon, Y., Mousset, J. L., and Arturo-Schaanc, M. (2008). Dose–response effects of essential oils on in vitro fermentation activity of the rumen microbial population. Anim. Feed Sci. Technol. 145, 335–350. doi: 10.1016/j.anifeedsci.2007.05.044 Marrero, Y., Sosa, D., Rodrıguez, R., and Garc ́ ıa, Y. (2016). Inclusion of ́ Pichia guilliermondii on different culture media, on in vitro fermentation of cynodon nlemfuensis. Cuban J. Agr. Sci. 50, 403–409. McCann, J. C., Elolimy, A. A., and Loor, J. J. (2017). Rumen microbiome, probiotics, and fermentation additives. Vet. Clin. Food Anim. Pract. 33, 539–553. doi: 10.1016/j.cvfa.2017.06.009 McDougall, E. I. (1948). Studies on ruminant saliva. 1. the composition and output of sheep’s saliva. Biochem. J. 43, 99–109. doi: 10.1042/bj0430099 McIntosh, F. M., Williams, P., Losa, R., Wallace, R. J., Beever, D. A., and Newbold, C. J. (2003). Effects of essential oils on ruminal microorganisms and their protein metabolism. appl. environ. Microbiol 69, 5011–5014. doi: 10.1128/ AEM.69.8.5011-5014.2003 Miller-Webster, T., Hoover, W. H., Holt, M., and Nocek, J. E. (2002). Influence of yeast culture on ruminal microbial metabolism in continuous culture. J. Dairy Sci. 85, 2009–2014. doi: 10.3168/jds.S0022-0302(02)74277-X Moallem, U., Lehrer, H., Livshitz, L., Zachut, M., and Yakoby, S. (2009). The effects of live yeast supplementation to dairy cows during the hot season on production, feed efficiency, and digestibility. J. Dairy Sci. 92, 343–351. doi: 10.3168/ jds.2007-0839 Moss, A. R., Jouany, J. P., and Newbold, C. J. (2000). Methane production by ruminants: Its contribution to global warming. Ann. Zootech. 49, 231–253. doi: 10.1051/animres:2000119 Newbold, C. J., and Ramos-Morales, E. (2020). Review: Ruminal microbiome and microbial metabolome: effects of diet and ruminant host. Animal 14, 78–86. doi: 10.1017/S1751731119003252 Newbold, C. J., Wallace, R. J., and Mcintosh, F. M. (1996). Mode of action of the yeast saccharomyces cerevisiae as a feed additive for ruminants. Br. J. Nutr. 76, 249–261. doi: 10.1079/BJN19960029 Pastén, M. G., Montenegro, N. C., Trejo, L. C., Flores, S. V., Bunting, L. D., and Acetoze, G. (2021). Effects of supplementation with a Pichia guilliermondii yeast cell product or essential oils on performance and health of dairy calves during an experimental coccidial infection. Appl. Anim. Sci. 37, 519–524. doi: 10.15232/ aas.2021-02186 Patra, A. K. (2011). Effects of essential oils on rumen fermentation, microbial ecology and ruminant production. Asian J. Anim. Vet. Adv. 6, 416–428. doi: 10.3923/ajava.2011.416.428 Patra, A. K., and Yu, Z. (2012). Effects of essential oils on methane production and fermentation by, and abundance and diversity of, rumen microbial populations. Appl. Environ. Microbiol. 78, 4271–4280. doi: 10.1128/AEM.00309-12 Patra, A. K., and Yu, Z. (2014). Combinations of nitrate, saponin, and sulfate additively reduce methane production by rumen cultures in vitro while not adversely affecting feed digestion, fermentation or microbial communities. Bioresour. Technol. 155, 129–135. doi: 10.1016/j.biortech.2013.12.099 Ramos-Morales, E., Tibble-Howlings, J., Lyons, L., Ogbu, M. O., Murphy, P. J., Braganca, R., et al. (2019). Slight changes in the chemical structure of haemanthamine greatly influence the effect of the derivatives on rumen fermentation in vitro. Sci. Rep. 9, 2440. doi: 10.1038/s41598-019-38977-x Robinson, P. H., and Erasmus, L. J. (2009). Effects of analyzable diet components on responses of lactating dairy cows to saccharomyces cerevisiae based yeast products: A systematic review of the literature. Anim. Feed Sci. Technol. 149, 185– 198. doi: 10.1016/j.anifeedsci.2008.10.003 Rodrıguez, T., Chaparro, M., Go ́ ́mez, M., Castillo, C., Garcıa, A., Ariza, C., et al. ́ (2015). A novel yeast strain Meyerozyma guilliermondii isolated from native fruits from Colombia ecosystems as a prospective probiotic to be used in dairy systems. Proceedings of the 2015 Congress on Gastrointestinal Function. Chigago. pg 56, Rodrıguez Quiroz, T. A. (2014). ́ Estudio del efecto del aceite esencial de orégano de monte (Lippia origanoides) del alto patıa sobre la metanoge ́ ́nesis y la actividad fibrolıtica del ecosistema rumin ́ al. [master´s thesis] (Colombia: Universidad Nacional de Colombia). Available at: https://repositorio.unal.edu.co/handle/unal/ 75189. Seedorf, H., Kittelmann, S., Henderson, G., and Hanssen, P. H. (2014). RIM-DB: a taxonomic framework for community structure analysis of methanogenic archaea from the rumen and other intestinal environments. Peer J. 2, e494. doi: 10.7717/ peerj.494 Shanmugasundaram, R., and Selvaraj, R. K. (2012). Effect of killed whole yeast cell prebiotic supplementation on broiler performance and intestinal immune cell parameters. Poult. Sci. 91, 107–111. doi: 10.3382/ps.2011-01732 Shurson, G. C. (2018). Yeast and yeast derivatives in feed additives and ingredients: Sources, characteristics, animal responses, and quantification methods. Anim. Feed Sci. Technol. 235, 60–76. doi: 10.1016/j.anifeedsci.2017.11.010 Spear, G. T., Sikaroodi, M., Zariffard, M. R., Landay, A. L., French, A. L., and Gillevet, P. M. (2008). Comparison of the diversity of the vaginal microbiota in HIV-infected and HIV-uninfected women with or without bacterial vaginosis. J. Infect. Dis. 198, 1131–1140. doi: 10.1086/591942 Stewart, C. S., and Duncan, S. H. (1985). The effect of avoparcin on cellulolytic bacteria of the ovine rumen. J. Gen. Microbiol. 131 427–35. doi: 10.1099/00221287- 131-3-427 Suntara, C., Cherdthong, A., Uriyapongson, S., Wanapat, M., and Chanjula, P. (2021). Novel crabtree negative yeast from rumen fluids can improve rumen fermentation and milk quality. Sci. Rep. 11, 6236. doi: 10.1038/s41598-021-85643-2 Tapio, I., Snelling, T. J., Strozzi, F., and Wallace, R. J. (2017). The ruminal microbiome associated with methane emissions from ruminant livestock. J. Anim. Sci. Biotechnol. 8, 7. doi: 10.1186/s40104-017-0141-0 Vá squez Carreño, D. R. (2012). El Orégano del monte (Lippia origanoides) del alto patıa: efecto del me ́ ́ todo de obtención de sus extractos sobre la composición y la actividad antioxidante de los mismos. [master´s thesis] (Colombia: Universidad Nacional de Colombia). Available at: https://repositorio.unal.edu.co/handle/unal/11580. Wallace, R. J., McKain, N., Broderick, G. A., Rode, L. M., Walker, N. D., Newbold, C. J., et al. (1997). Peptidases of the rumen bacterium, prevotella ruminicola. Anaerobe 3, 35–42. doi: 10.1006/anae.1996.0065 Wang, Q., Garrity, G. M., Tiedje, J. M., and Cole, J. R. (2007). Naive bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261–5267. doi: 10.1128/AEM.00062-07 Weatherburn, M. W. (1967). Phenol-hypochlorite reaction for determination of ammonia. Anal. Chem. 39, 971–974. doi: 10.1021/ac60252a045 Wright, A.-D. G., and Pimm, C. (2003). Improved strategy for presumptive identification of methanogens using 16S riboprinting. J. Microbiol. Methods 55, 337–349. doi: 10.1016/S0167-7012(03)00169-6 Yu, J., Cai, L., Zhang, J., Yang, A., Wang, Y., Zhang, L., et al. (2020). Effects of thymol supplementation on goat rumen fermentation and rumen microbiota in vitro. Microorganisms 8, 1160. doi: 10.3390/microorganisms 8081160 Yu, Z., and Morrison, M.. (2004). Improved extraction of PCR-quality community DNA from digesta and fecal samples. BioTechniques 36, 808–812. doi: 10.2144/04365ST04 Zhou, R., Wu, J., Lang, X., Liu, L., Casper, D. P., Wang, C., et al. (2020). Effects of oregano essential oil on in vitro ruminal fermentation, methane production, and ruminal microbial community. J. Dairy Sci. 103, 2303–2314. doi: 10.3168/jds.2019- 16611 Zhou, R., Wu, J., Zhang, L., Liu, L., Casper, D. P., Jiao, T., et al. (2019). Effects of oregano essential oil on the ruminal pH and microbial population of sheep. PLoS One 14, e0217054. doi: 10.1371/journal.pone.0217054 Attribution-ShareAlike 4.0 International http://creativecommons.org/licenses/by-sa/4.0/ application/pdf application/pdf Colombia Frontiers in Animal Science Lausana (Suiza) Frontiers in Animal Science; Vol. 3, Núm. 3 (2022): Frontiers in Animal Science (Julio);p. 1 -13. |