Cargando…

Changes in the membrane lipid composition of a Sulfurimonas species depend on the electron acceptor used for sulfur oxidation

Sulfurimonas species are among the most abundant sulfur-oxidizing bacteria in the marine environment. They are capable of using different electron acceptors, this metabolic flexibility is favorable for their niche adaptation in redoxclines. When oxygen is depleted, most Sulfurimonas spp. (e.g., Sulf...

Descripción completa

Detalles Bibliográficos
Autores principales: Ding, Su, Henkel, Jan V., Hopmans, Ellen C., Bale, Nicole J., Koenen, Michel, Villanueva, Laura, Sinninghe Damsté, Jaap S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9789136/
https://www.ncbi.nlm.nih.gov/pubmed/37938789
http://dx.doi.org/10.1038/s43705-022-00207-3
_version_ 1784858910161633280
author Ding, Su
Henkel, Jan V.
Hopmans, Ellen C.
Bale, Nicole J.
Koenen, Michel
Villanueva, Laura
Sinninghe Damsté, Jaap S.
author_facet Ding, Su
Henkel, Jan V.
Hopmans, Ellen C.
Bale, Nicole J.
Koenen, Michel
Villanueva, Laura
Sinninghe Damsté, Jaap S.
author_sort Ding, Su
collection PubMed
description Sulfurimonas species are among the most abundant sulfur-oxidizing bacteria in the marine environment. They are capable of using different electron acceptors, this metabolic flexibility is favorable for their niche adaptation in redoxclines. When oxygen is depleted, most Sulfurimonas spp. (e.g., Sulfurimonas gotlandica) use nitrate ([Formula: see text] ) as an electron acceptor to oxidize sulfur, including sulfide (HS(-)), S(0) and thiosulfate, for energy production. Candidatus Sulfurimonas marisnigri SoZ1 and Candidatus Sulfurimonas baltica GD2, recently isolated from the redoxclines of the Black Sea and Baltic Sea respectively, have been shown to use manganese dioxide (MnO(2)) rather than [Formula: see text] for sulfur oxidation. The use of different electron acceptors is also dependent on differences in the electron transport chains embedded in the cellular membrane, therefore changes in the membrane, including its lipid composition, are expected but are so far unexplored. Here, we used untargeted lipidomic analysis to reveal changes in the composition of the lipidomes of three representative Sulfurimonas species grown using either [Formula: see text] and MnO(2). We found that all Sulfurimonas spp. produce a series of novel phosphatidyldiazoalkyl-diacylglycerol lipids. Ca. Sulfurimonas baltica GD2 adapts its membrane lipid composition depending on the electron acceptors it utilizes for growth and survival. When carrying out MnO(2)-dependent sulfur oxidation, the novel phosphatidyldiazoalkyl-diacylglycerol headgroup comprises shorter alkyl moieties than when sulfur oxidation is [Formula: see text] -dependent. This is the first report of membrane lipid adaptation when an organism is grown with different electron acceptors. We suggest novel diazoalkyl lipids have the potential to be used as a biomarker for different conditions in redox-stratified systems.
format Online
Article
Text
id pubmed-9789136
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-97891362023-01-04 Changes in the membrane lipid composition of a Sulfurimonas species depend on the electron acceptor used for sulfur oxidation Ding, Su Henkel, Jan V. Hopmans, Ellen C. Bale, Nicole J. Koenen, Michel Villanueva, Laura Sinninghe Damsté, Jaap S. ISME Commun Article Sulfurimonas species are among the most abundant sulfur-oxidizing bacteria in the marine environment. They are capable of using different electron acceptors, this metabolic flexibility is favorable for their niche adaptation in redoxclines. When oxygen is depleted, most Sulfurimonas spp. (e.g., Sulfurimonas gotlandica) use nitrate ([Formula: see text] ) as an electron acceptor to oxidize sulfur, including sulfide (HS(-)), S(0) and thiosulfate, for energy production. Candidatus Sulfurimonas marisnigri SoZ1 and Candidatus Sulfurimonas baltica GD2, recently isolated from the redoxclines of the Black Sea and Baltic Sea respectively, have been shown to use manganese dioxide (MnO(2)) rather than [Formula: see text] for sulfur oxidation. The use of different electron acceptors is also dependent on differences in the electron transport chains embedded in the cellular membrane, therefore changes in the membrane, including its lipid composition, are expected but are so far unexplored. Here, we used untargeted lipidomic analysis to reveal changes in the composition of the lipidomes of three representative Sulfurimonas species grown using either [Formula: see text] and MnO(2). We found that all Sulfurimonas spp. produce a series of novel phosphatidyldiazoalkyl-diacylglycerol lipids. Ca. Sulfurimonas baltica GD2 adapts its membrane lipid composition depending on the electron acceptors it utilizes for growth and survival. When carrying out MnO(2)-dependent sulfur oxidation, the novel phosphatidyldiazoalkyl-diacylglycerol headgroup comprises shorter alkyl moieties than when sulfur oxidation is [Formula: see text] -dependent. This is the first report of membrane lipid adaptation when an organism is grown with different electron acceptors. We suggest novel diazoalkyl lipids have the potential to be used as a biomarker for different conditions in redox-stratified systems. Nature Publishing Group UK 2022-12-24 /pmc/articles/PMC9789136/ /pubmed/37938789 http://dx.doi.org/10.1038/s43705-022-00207-3 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Ding, Su
Henkel, Jan V.
Hopmans, Ellen C.
Bale, Nicole J.
Koenen, Michel
Villanueva, Laura
Sinninghe Damsté, Jaap S.
Changes in the membrane lipid composition of a Sulfurimonas species depend on the electron acceptor used for sulfur oxidation
title Changes in the membrane lipid composition of a Sulfurimonas species depend on the electron acceptor used for sulfur oxidation
title_full Changes in the membrane lipid composition of a Sulfurimonas species depend on the electron acceptor used for sulfur oxidation
title_fullStr Changes in the membrane lipid composition of a Sulfurimonas species depend on the electron acceptor used for sulfur oxidation
title_full_unstemmed Changes in the membrane lipid composition of a Sulfurimonas species depend on the electron acceptor used for sulfur oxidation
title_short Changes in the membrane lipid composition of a Sulfurimonas species depend on the electron acceptor used for sulfur oxidation
title_sort changes in the membrane lipid composition of a sulfurimonas species depend on the electron acceptor used for sulfur oxidation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9789136/
https://www.ncbi.nlm.nih.gov/pubmed/37938789
http://dx.doi.org/10.1038/s43705-022-00207-3
work_keys_str_mv AT dingsu changesinthemembranelipidcompositionofasulfurimonasspeciesdependontheelectronacceptorusedforsulfuroxidation
AT henkeljanv changesinthemembranelipidcompositionofasulfurimonasspeciesdependontheelectronacceptorusedforsulfuroxidation
AT hopmansellenc changesinthemembranelipidcompositionofasulfurimonasspeciesdependontheelectronacceptorusedforsulfuroxidation
AT balenicolej changesinthemembranelipidcompositionofasulfurimonasspeciesdependontheelectronacceptorusedforsulfuroxidation
AT koenenmichel changesinthemembranelipidcompositionofasulfurimonasspeciesdependontheelectronacceptorusedforsulfuroxidation
AT villanuevalaura changesinthemembranelipidcompositionofasulfurimonasspeciesdependontheelectronacceptorusedforsulfuroxidation
AT sinninghedamstejaaps changesinthemembranelipidcompositionofasulfurimonasspeciesdependontheelectronacceptorusedforsulfuroxidation