Rumen microbial degradation of bromoform from red seaweed (Asparagopsis taxiformis) and the impact on rumen fermentation and methanogenic archaea

Background: The red macroalgae Asparagopsis is an effective methanogenesis inhibitor due to the presence of halogenated methane (CH) analogues, primarily bromoform (CHBr). This study aimed to investigate the degradation process of CHBr from A. taxiformis in the rumen and whether this process is diet...

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Autores: Romero Márquez, Pedro J., Belanche, A., Jiménez Jiménez, Elisabeth, Hueso, Rafael, Ramos Morales, Eva, Salwen, J.K., Kebreab, E., Yáñez Ruiz, David R.
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/342377
Acceso en línea:http://hdl.handle.net/10261/342377
Access Level:acceso abierto
Palabra clave:Bromoform metabolism
Dibromomethane metabolism
Methane mitigation
Methanogens
Rumen microbiota
Seaweed
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spelling Rumen microbial degradation of bromoform from red seaweed (Asparagopsis taxiformis) and the impact on rumen fermentation and methanogenic archaeaRomero Márquez, Pedro J.Belanche, A.Jiménez Jiménez, ElisabethHueso, RafaelRamos Morales, EvaSalwen, J.K.Kebreab, E.Yáñez Ruiz, David R.Bromoform metabolismDibromomethane metabolismMethane mitigationMethanogensRumen microbiotaSeaweedBackground: The red macroalgae Asparagopsis is an effective methanogenesis inhibitor due to the presence of halogenated methane (CH) analogues, primarily bromoform (CHBr). This study aimed to investigate the degradation process of CHBr from A. taxiformis in the rumen and whether this process is diet-dependent. An in vitro batch culture system was used according to a 2 × 2 factorial design, assessing two A. taxiformis inclusion rates [0 (CTL) and 2% DM diet (AT)] and two diets [high-concentrate (HC) and high-forage diet (HF)]. Incubations lasted for 72 h and samples of headspace and fermentation liquid were taken at 0, 0.5, 1, 3, 6, 8, 12, 16, 24, 48 and 72 h to assess the pattern of degradation of CHBr into dibromomethane (CHBr) and fermentation parameters. Additionally, an in vitro experiment with pure cultures of seven methanogens strains (Methanobrevibacter smithii, Methanobrevibacter ruminantium, Methanosphaera stadtmanae, Methanosarcina barkeri, Methanobrevibacter millerae, Methanothermobacter wolfei and Methanobacterium mobile) was conducted to test the effects of increasing concentrations of CHBr (0.4, 2, 10 and 50 µmol/L). Results: The addition of AT significantly decreased CH production (P = 0.002) and the acetate:propionate ratio (P = 0.003) during a 72-h incubation. The concentrations of CHBr showed a rapid decrease with nearly 90% degraded within the first 3 h of incubation. On the contrary, CHBr concentration quickly increased during the first 6 h and then gradually decreased towards the end of the incubation. Neither CHBr degradation nor CHBr synthesis were affected by the type of diet used as substrate, suggesting that the fermentation rate is not a driving factor involved in CHBr degradation. The in vitro culture of methanogens showed a dose-response effect of CHBr by inhibiting the growth of M. smithii, M. ruminantium, M. stadtmanae, M. barkeri, M. millerae, M. wolfei, and M. mobile. Conclusions: The present work demonstrated that CHBr from A. taxiformis is quickly degraded to CHBr in the rumen and that the fermentation rate promoted by different diets is not a driving factor involved in CHBr degradation.This work was funded by Blue Ocean Barns. AB has a Ramón y Cajal research contract (RYC2019-027764-I) funded by the Spanish State Research Agency (AEI).Peer reviewedBioMed CentralBlue Ocean BarnsConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2024202420232024info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/342377reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI//RYC2019-027764-Ihttp://dx.doi.org/10.1186/s40104-023-00935-zSíinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3423772026-05-22T06:33:51Z
dc.title.none.fl_str_mv Rumen microbial degradation of bromoform from red seaweed (Asparagopsis taxiformis) and the impact on rumen fermentation and methanogenic archaea
title Rumen microbial degradation of bromoform from red seaweed (Asparagopsis taxiformis) and the impact on rumen fermentation and methanogenic archaea
spellingShingle Rumen microbial degradation of bromoform from red seaweed (Asparagopsis taxiformis) and the impact on rumen fermentation and methanogenic archaea
Romero Márquez, Pedro J.
Bromoform metabolism
Dibromomethane metabolism
Methane mitigation
Methanogens
Rumen microbiota
Seaweed
title_short Rumen microbial degradation of bromoform from red seaweed (Asparagopsis taxiformis) and the impact on rumen fermentation and methanogenic archaea
title_full Rumen microbial degradation of bromoform from red seaweed (Asparagopsis taxiformis) and the impact on rumen fermentation and methanogenic archaea
title_fullStr Rumen microbial degradation of bromoform from red seaweed (Asparagopsis taxiformis) and the impact on rumen fermentation and methanogenic archaea
title_full_unstemmed Rumen microbial degradation of bromoform from red seaweed (Asparagopsis taxiformis) and the impact on rumen fermentation and methanogenic archaea
title_sort Rumen microbial degradation of bromoform from red seaweed (Asparagopsis taxiformis) and the impact on rumen fermentation and methanogenic archaea
dc.creator.none.fl_str_mv Romero Márquez, Pedro J.
Belanche, A.
Jiménez Jiménez, Elisabeth
Hueso, Rafael
Ramos Morales, Eva
Salwen, J.K.
Kebreab, E.
Yáñez Ruiz, David R.
author Romero Márquez, Pedro J.
author_facet Romero Márquez, Pedro J.
Belanche, A.
Jiménez Jiménez, Elisabeth
Hueso, Rafael
Ramos Morales, Eva
Salwen, J.K.
Kebreab, E.
Yáñez Ruiz, David R.
author_role author
author2 Belanche, A.
Jiménez Jiménez, Elisabeth
Hueso, Rafael
Ramos Morales, Eva
Salwen, J.K.
Kebreab, E.
Yáñez Ruiz, David R.
author2_role author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Blue Ocean Barns
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Bromoform metabolism
Dibromomethane metabolism
Methane mitigation
Methanogens
Rumen microbiota
Seaweed
topic Bromoform metabolism
Dibromomethane metabolism
Methane mitigation
Methanogens
Rumen microbiota
Seaweed
description Background: The red macroalgae Asparagopsis is an effective methanogenesis inhibitor due to the presence of halogenated methane (CH) analogues, primarily bromoform (CHBr). This study aimed to investigate the degradation process of CHBr from A. taxiformis in the rumen and whether this process is diet-dependent. An in vitro batch culture system was used according to a 2 × 2 factorial design, assessing two A. taxiformis inclusion rates [0 (CTL) and 2% DM diet (AT)] and two diets [high-concentrate (HC) and high-forage diet (HF)]. Incubations lasted for 72 h and samples of headspace and fermentation liquid were taken at 0, 0.5, 1, 3, 6, 8, 12, 16, 24, 48 and 72 h to assess the pattern of degradation of CHBr into dibromomethane (CHBr) and fermentation parameters. Additionally, an in vitro experiment with pure cultures of seven methanogens strains (Methanobrevibacter smithii, Methanobrevibacter ruminantium, Methanosphaera stadtmanae, Methanosarcina barkeri, Methanobrevibacter millerae, Methanothermobacter wolfei and Methanobacterium mobile) was conducted to test the effects of increasing concentrations of CHBr (0.4, 2, 10 and 50 µmol/L). Results: The addition of AT significantly decreased CH production (P = 0.002) and the acetate:propionate ratio (P = 0.003) during a 72-h incubation. The concentrations of CHBr showed a rapid decrease with nearly 90% degraded within the first 3 h of incubation. On the contrary, CHBr concentration quickly increased during the first 6 h and then gradually decreased towards the end of the incubation. Neither CHBr degradation nor CHBr synthesis were affected by the type of diet used as substrate, suggesting that the fermentation rate is not a driving factor involved in CHBr degradation. The in vitro culture of methanogens showed a dose-response effect of CHBr by inhibiting the growth of M. smithii, M. ruminantium, M. stadtmanae, M. barkeri, M. millerae, M. wolfei, and M. mobile. Conclusions: The present work demonstrated that CHBr from A. taxiformis is quickly degraded to CHBr in the rumen and that the fermentation rate promoted by different diets is not a driving factor involved in CHBr degradation.
publishDate 2023
dc.date.none.fl_str_mv 2023
2024
2024
2024
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/342377
url http://hdl.handle.net/10261/342377
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/AEI//RYC2019-027764-I
http://dx.doi.org/10.1186/s40104-023-00935-z
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv BioMed Central
publisher.none.fl_str_mv BioMed Central
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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