Novel energy conservation strategies and behavior of Pelotomaculum schinkii driving syntrophic propionate catabolism

Detalhes bibliográficos
Autor(a) principal: Hidalgo, Catalina A
Data de Publicação: 2018
Outros Autores: Nobu, Masaru K, Narihiro, Takashi, Tamaki, Hideyuki, Liu, Wen-Tso, Kamagata, Yoichi, Stams, Alfons Johannes Maria, Imachi, Hiroyuki, Sousa, Diana Zita Machado
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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spelling 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)
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