Novel energy conservation strategies and behavior of Pelotomaculum schinkii driving syntrophic propionate catabolism
Autor(a) principal: | |
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Data de Publicação: | 2018 |
Outros Autores: | , , , , , , , |
Tipo de documento: | Artigo |
Idioma: | eng |
Título da fonte: | Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
Texto Completo: | http://hdl.handle.net/1822/57410 |
Resumo: | Under methanogenic conditions, short-chain fatty acids are common byproducts from degradation of organic compounds and conversion of these acids is an important component of the global carbon cycle. Due to the thermodynamic difficulty of propionate degradation, this process requires syntrophic interaction between a bacterium and partner methanogen; however, the metabolic strategies and behavior involved are not fully understood. In this study, the first genome analysis of obligately syntrophic propionate degraders (Pelotomaculum schinkii HH and P. propionicicum MGP) and comparison with other syntrophic propionate degrader genomes elucidated novel components of energy metabolism behind Pelotomaculum propionate oxidation. Combined with transcriptomic examination of P. schinkii behavior in co-culture with Methanospirillum hungatei, we found that formate may be the preferred electron carrier for P. schinkii syntrophy. Propionate-derived menaquinol may be primarily re-oxidized to formate, and energy was conserved during formate generation through newly proposed proton-pumping formate extrusion. P. schinkii did not overexpress conventional energy metabolism associated with a model syntrophic propionate degrader Syntrophobacter fumaroxidans MPOB (i.e., CoA transferase, Fix, and Rnf). We also found that P. schinkii and the partner methanogen may also interact through flagellar contact and amino acid and fructose exchange. These findings provide new understanding of syntrophic energy acquisition and interactions. This article is protected by copyright. All rights reserved. |
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Novel energy conservation strategies and behavior of Pelotomaculum schinkii driving syntrophic propionate catabolismScience & TechnologyUnder methanogenic conditions, short-chain fatty acids are common byproducts from degradation of organic compounds and conversion of these acids is an important component of the global carbon cycle. Due to the thermodynamic difficulty of propionate degradation, this process requires syntrophic interaction between a bacterium and partner methanogen; however, the metabolic strategies and behavior involved are not fully understood. In this study, the first genome analysis of obligately syntrophic propionate degraders (Pelotomaculum schinkii HH and P. propionicicum MGP) and comparison with other syntrophic propionate degrader genomes elucidated novel components of energy metabolism behind Pelotomaculum propionate oxidation. Combined with transcriptomic examination of P. schinkii behavior in co-culture with Methanospirillum hungatei, we found that formate may be the preferred electron carrier for P. schinkii syntrophy. Propionate-derived menaquinol may be primarily re-oxidized to formate, and energy was conserved during formate generation through newly proposed proton-pumping formate extrusion. P. schinkii did not overexpress conventional energy metabolism associated with a model syntrophic propionate degrader Syntrophobacter fumaroxidans MPOB (i.e., CoA transferase, Fix, and Rnf). We also found that P. schinkii and the partner methanogen may also interact through flagellar contact and amino acid and fructose exchange. These findings provide new understanding of syntrophic energy acquisition and interactions. This article is protected by copyright. All rights reserved.We thank Steven Aalvink for scanning electron microscopy analysis and WEMC for making the system available. The research leading to these results has received funding from the European Research Council under the European Union’s Seventh Framework Programme (FP/2007-2013) / ERC Grant Agreement n. [323009] and a Gravitation Grant (Project 024.002.002) of the Netherlands Ministry of Education, Culture and Science and the Netherlands Organisation for Scientific Research (NWO). This work was also supported by The Japan Society for the Promotion of Science with Grant-in-Aid for Scientific Research No. 18H03367 to MK Nobu and 17H05239 and 18H01576 to T Narihiro.info:eu-repo/semantics/publishedVersionWiley-BlackwellUniversidade do MinhoHidalgo, Catalina ANobu, Masaru KNarihiro, TakashiTamaki, HideyukiLiu, Wen-TsoKamagata, YoichiStams, Alfons Johannes MariaImachi, HiroyukiSousa, Diana Zita Machado2018-122018-12-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/1822/57410engHidalgo, Catalina A; Nobu, Masaru K; Narihiro, Takashi; Tamaki, Hideyuki; Liu, Wen-Tso; Kamagata, Yoichi; Stams, A. J. M.; Imachi, Hiroyuki; Sousa, Diana Z., Novel energy conservation strategies and behavior of Pelotomaculum schinkii driving syntrophic propionate catabolism. Environmental Microbiology, 20(12), 4503-4511, 20181462-29121462-292010.1111/1462-2920.1438830126076http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1462-2920info:eu-repo/semantics/openAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2023-07-21T12:45:31Zoai:repositorium.sdum.uminho.pt:1822/57410Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T19:43:22.943181Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse |
dc.title.none.fl_str_mv |
Novel energy conservation strategies and behavior of Pelotomaculum schinkii driving syntrophic propionate catabolism |
title |
Novel energy conservation strategies and behavior of Pelotomaculum schinkii driving syntrophic propionate catabolism |
spellingShingle |
Novel energy conservation strategies and behavior of Pelotomaculum schinkii driving syntrophic propionate catabolism Hidalgo, Catalina A Science & Technology |
title_short |
Novel energy conservation strategies and behavior of Pelotomaculum schinkii driving syntrophic propionate catabolism |
title_full |
Novel energy conservation strategies and behavior of Pelotomaculum schinkii driving syntrophic propionate catabolism |
title_fullStr |
Novel energy conservation strategies and behavior of Pelotomaculum schinkii driving syntrophic propionate catabolism |
title_full_unstemmed |
Novel energy conservation strategies and behavior of Pelotomaculum schinkii driving syntrophic propionate catabolism |
title_sort |
Novel energy conservation strategies and behavior of Pelotomaculum schinkii driving syntrophic propionate catabolism |
author |
Hidalgo, Catalina A |
author_facet |
Hidalgo, Catalina A Nobu, Masaru K Narihiro, Takashi Tamaki, Hideyuki Liu, Wen-Tso Kamagata, Yoichi Stams, Alfons Johannes Maria Imachi, Hiroyuki Sousa, Diana Zita Machado |
author_role |
author |
author2 |
Nobu, Masaru K Narihiro, Takashi Tamaki, Hideyuki Liu, Wen-Tso Kamagata, Yoichi Stams, Alfons Johannes Maria Imachi, Hiroyuki Sousa, Diana Zita Machado |
author2_role |
author author author author author author author author |
dc.contributor.none.fl_str_mv |
Universidade do Minho |
dc.contributor.author.fl_str_mv |
Hidalgo, Catalina A Nobu, Masaru K Narihiro, Takashi Tamaki, Hideyuki Liu, Wen-Tso Kamagata, Yoichi Stams, Alfons Johannes Maria Imachi, Hiroyuki Sousa, Diana Zita Machado |
dc.subject.por.fl_str_mv |
Science & Technology |
topic |
Science & Technology |
description |
Under methanogenic conditions, short-chain fatty acids are common byproducts from degradation of organic compounds and conversion of these acids is an important component of the global carbon cycle. Due to the thermodynamic difficulty of propionate degradation, this process requires syntrophic interaction between a bacterium and partner methanogen; however, the metabolic strategies and behavior involved are not fully understood. In this study, the first genome analysis of obligately syntrophic propionate degraders (Pelotomaculum schinkii HH and P. propionicicum MGP) and comparison with other syntrophic propionate degrader genomes elucidated novel components of energy metabolism behind Pelotomaculum propionate oxidation. Combined with transcriptomic examination of P. schinkii behavior in co-culture with Methanospirillum hungatei, we found that formate may be the preferred electron carrier for P. schinkii syntrophy. Propionate-derived menaquinol may be primarily re-oxidized to formate, and energy was conserved during formate generation through newly proposed proton-pumping formate extrusion. P. schinkii did not overexpress conventional energy metabolism associated with a model syntrophic propionate degrader Syntrophobacter fumaroxidans MPOB (i.e., CoA transferase, Fix, and Rnf). We also found that P. schinkii and the partner methanogen may also interact through flagellar contact and amino acid and fructose exchange. These findings provide new understanding of syntrophic energy acquisition and interactions. This article is protected by copyright. All rights reserved. |
publishDate |
2018 |
dc.date.none.fl_str_mv |
2018-12 2018-12-01T00:00:00Z |
dc.type.status.fl_str_mv |
info:eu-repo/semantics/publishedVersion |
dc.type.driver.fl_str_mv |
info:eu-repo/semantics/article |
format |
article |
status_str |
publishedVersion |
dc.identifier.uri.fl_str_mv |
http://hdl.handle.net/1822/57410 |
url |
http://hdl.handle.net/1822/57410 |
dc.language.iso.fl_str_mv |
eng |
language |
eng |
dc.relation.none.fl_str_mv |
Hidalgo, Catalina A; Nobu, Masaru K; Narihiro, Takashi; Tamaki, Hideyuki; Liu, Wen-Tso; Kamagata, Yoichi; Stams, A. J. M.; Imachi, Hiroyuki; Sousa, Diana Z., Novel energy conservation strategies and behavior of Pelotomaculum schinkii driving syntrophic propionate catabolism. Environmental Microbiology, 20(12), 4503-4511, 2018 1462-2912 1462-2920 10.1111/1462-2920.14388 30126076 http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1462-2920 |
dc.rights.driver.fl_str_mv |
info:eu-repo/semantics/openAccess |
eu_rights_str_mv |
openAccess |
dc.format.none.fl_str_mv |
application/pdf |
dc.publisher.none.fl_str_mv |
Wiley-Blackwell |
publisher.none.fl_str_mv |
Wiley-Blackwell |
dc.source.none.fl_str_mv |
reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação instacron:RCAAP |
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Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
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RCAAP |
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RCAAP |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
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