Eicosapentaenoic Acid Plays a Beneficial Role in Membrane Organization and Cell Division of a Cold-Adapted Bacterium, Shewanella livingstonensis Ac10

ABSTRACT Shewanella livingstonensis Ac10, a psychrotrophic gram-negative bacterium isolated from Antarctic seawater, produces eicosapentaenoic acid (EPA) as a component of phospholipids at low temperatures. EPA constitutes about 5% of the total fatty acids of cells grown at 4°C. We found that five g...

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Published in:Journal of Bacteriology
Main Authors: Kawamoto, Jun, Kurihara, Tatsuo, Yamamoto, Kentaro, Nagayasu, Makiko, Tani, Yasushi, Mihara, Hisaaki, Hosokawa, Masashi, Baba, Takeshi, Sato, Satoshi B., Esaki, Nobuyoshi
Format: Article in Journal/Newspaper
Language:English
Published: American Society for Microbiology 2009
Subjects:
Online Access:http://dx.doi.org/10.1128/jb.00881-08
https://journals.asm.org/doi/pdf/10.1128/JB.00881-08
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spelling crasmicro:10.1128/jb.00881-08 2024-09-15T17:47:33+00:00 Eicosapentaenoic Acid Plays a Beneficial Role in Membrane Organization and Cell Division of a Cold-Adapted Bacterium, Shewanella livingstonensis Ac10 Kawamoto, Jun Kurihara, Tatsuo Yamamoto, Kentaro Nagayasu, Makiko Tani, Yasushi Mihara, Hisaaki Hosokawa, Masashi Baba, Takeshi Sato, Satoshi B. Esaki, Nobuyoshi 2009 http://dx.doi.org/10.1128/jb.00881-08 https://journals.asm.org/doi/pdf/10.1128/JB.00881-08 en eng American Society for Microbiology https://journals.asm.org/non-commercial-tdm-license Journal of Bacteriology volume 191, issue 2, page 632-640 ISSN 0021-9193 1098-5530 journal-article 2009 crasmicro https://doi.org/10.1128/jb.00881-08 2024-08-19T04:06:07Z ABSTRACT Shewanella livingstonensis Ac10, a psychrotrophic gram-negative bacterium isolated from Antarctic seawater, produces eicosapentaenoic acid (EPA) as a component of phospholipids at low temperatures. EPA constitutes about 5% of the total fatty acids of cells grown at 4°C. We found that five genes, termed orf2, orf5, orf6, orf7 , and orf8 , are specifically required for the synthesis of EPA by targeted disruption of the respective genes. The mutants lacking EPA showed significant growth retardation at 4°C but not at 18°C. Supplementation of a synthetic phosphatidylethanolamine that contained EPA at the sn -2 position complemented the growth defect. The EPA-less mutant became filamentous, and multiple nucleoids were observed in a single cell at 4°C, indicating that the mutant has a defect in cell division. Electron microscopy of the cells by high-pressure freezing and freeze-substitution revealed abnormal intracellular membranes in the EPA-less mutant at 4°C. We also found that the amounts of several membrane proteins were affected by the depletion of EPA. While polyunsaturated fatty acids are often considered to increase the fluidity of the hydrophobic membrane core, diffusion of a small hydrophobic molecule, pyrene, in the cell membranes and large unilamellar vesicles prepared from the lipid extracts was very similar between the EPA-less mutant and the parental strain. These results suggest that EPA in S. livingstonensis Ac10 is not required for bulk bilayer fluidity but plays a beneficial role in membrane organization and cell division at low temperatures, possibly through specific interaction between EPA and proteins involved in these cellular processes. Article in Journal/Newspaper Antarc* Antarctic ASM Journals (American Society for Microbiology) Journal of Bacteriology 191 2 632 640
institution Open Polar
collection ASM Journals (American Society for Microbiology)
op_collection_id crasmicro
language English
description ABSTRACT Shewanella livingstonensis Ac10, a psychrotrophic gram-negative bacterium isolated from Antarctic seawater, produces eicosapentaenoic acid (EPA) as a component of phospholipids at low temperatures. EPA constitutes about 5% of the total fatty acids of cells grown at 4°C. We found that five genes, termed orf2, orf5, orf6, orf7 , and orf8 , are specifically required for the synthesis of EPA by targeted disruption of the respective genes. The mutants lacking EPA showed significant growth retardation at 4°C but not at 18°C. Supplementation of a synthetic phosphatidylethanolamine that contained EPA at the sn -2 position complemented the growth defect. The EPA-less mutant became filamentous, and multiple nucleoids were observed in a single cell at 4°C, indicating that the mutant has a defect in cell division. Electron microscopy of the cells by high-pressure freezing and freeze-substitution revealed abnormal intracellular membranes in the EPA-less mutant at 4°C. We also found that the amounts of several membrane proteins were affected by the depletion of EPA. While polyunsaturated fatty acids are often considered to increase the fluidity of the hydrophobic membrane core, diffusion of a small hydrophobic molecule, pyrene, in the cell membranes and large unilamellar vesicles prepared from the lipid extracts was very similar between the EPA-less mutant and the parental strain. These results suggest that EPA in S. livingstonensis Ac10 is not required for bulk bilayer fluidity but plays a beneficial role in membrane organization and cell division at low temperatures, possibly through specific interaction between EPA and proteins involved in these cellular processes.
format Article in Journal/Newspaper
author Kawamoto, Jun
Kurihara, Tatsuo
Yamamoto, Kentaro
Nagayasu, Makiko
Tani, Yasushi
Mihara, Hisaaki
Hosokawa, Masashi
Baba, Takeshi
Sato, Satoshi B.
Esaki, Nobuyoshi
spellingShingle Kawamoto, Jun
Kurihara, Tatsuo
Yamamoto, Kentaro
Nagayasu, Makiko
Tani, Yasushi
Mihara, Hisaaki
Hosokawa, Masashi
Baba, Takeshi
Sato, Satoshi B.
Esaki, Nobuyoshi
Eicosapentaenoic Acid Plays a Beneficial Role in Membrane Organization and Cell Division of a Cold-Adapted Bacterium, Shewanella livingstonensis Ac10
author_facet Kawamoto, Jun
Kurihara, Tatsuo
Yamamoto, Kentaro
Nagayasu, Makiko
Tani, Yasushi
Mihara, Hisaaki
Hosokawa, Masashi
Baba, Takeshi
Sato, Satoshi B.
Esaki, Nobuyoshi
author_sort Kawamoto, Jun
title Eicosapentaenoic Acid Plays a Beneficial Role in Membrane Organization and Cell Division of a Cold-Adapted Bacterium, Shewanella livingstonensis Ac10
title_short Eicosapentaenoic Acid Plays a Beneficial Role in Membrane Organization and Cell Division of a Cold-Adapted Bacterium, Shewanella livingstonensis Ac10
title_full Eicosapentaenoic Acid Plays a Beneficial Role in Membrane Organization and Cell Division of a Cold-Adapted Bacterium, Shewanella livingstonensis Ac10
title_fullStr Eicosapentaenoic Acid Plays a Beneficial Role in Membrane Organization and Cell Division of a Cold-Adapted Bacterium, Shewanella livingstonensis Ac10
title_full_unstemmed Eicosapentaenoic Acid Plays a Beneficial Role in Membrane Organization and Cell Division of a Cold-Adapted Bacterium, Shewanella livingstonensis Ac10
title_sort eicosapentaenoic acid plays a beneficial role in membrane organization and cell division of a cold-adapted bacterium, shewanella livingstonensis ac10
publisher American Society for Microbiology
publishDate 2009
url http://dx.doi.org/10.1128/jb.00881-08
https://journals.asm.org/doi/pdf/10.1128/JB.00881-08
genre Antarc*
Antarctic
genre_facet Antarc*
Antarctic
op_source Journal of Bacteriology
volume 191, issue 2, page 632-640
ISSN 0021-9193 1098-5530
op_rights https://journals.asm.org/non-commercial-tdm-license
op_doi https://doi.org/10.1128/jb.00881-08
container_title Journal of Bacteriology
container_volume 191
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