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Cold adaptation of eicosapentaenoic acid-less mutant of Shewanella livingstonensis Ac10 involving uptake and remodeling of synthetic phospholipids containing various polyunsaturated fatty acids

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Abstract

An Antarctic psychrotrophic bacterium, Shewanella livingstonensis Ac10, produces cis-5,8,11,14,17-eicosapentaenoic acid (EPA), a long-chain polyunsaturated fatty acid (LPUFA), as a component of membrane phospholipids at low temperatures. The EPA-less mutant generated by disruption of the EPA synthesis gene becomes cold-sensitive. We studied whether the cold sensitivity could be suppressed by supplementation of various LPUFAs. The EPA-less mutant was cultured at 6°C in the presence of synthetic phosphatidylethanolamines (PEs) that contained oleic acid at the sn-1 position and various C20 fatty acids with different numbers of double bonds from zero to five or cis-4,7,10,13,16,19-docosahexaenoic acid (DHA) at the sn-2 position. Mass spectrometric analyses revealed that all these fatty acids became components of various PE and phosphatidylglycerol species together with shorter partner fatty acids, indicating that large-scale remodeling followed the incorporation of synthetic PEs. As the number of double bonds in the sn-2 acyl chain decreased, the growth rate decreased and the cells became filamentous. The growth was restored to the wild-type level only when the medium was supplemented with phospholipids containing EPA or DHA. We found that about a half of DHA was converted into EPA. The results suggest that intact EPA is best required for cold adaptation of this bacterium.

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Abbreviations

EPA:

cis-5,8,11,14,17-Eicosapentaenoic acid

DHA:

cis-4,7,10,13,16,19-Docosahexaenoic acid

PE:

Phosphatidylethanolamine

PG:

Phosphatidylglycerol

LPUFA:

Long-chain polyunsaturated fatty acid

ESI-MS:

Electrospray ionization mass spectrometry

GC-MS:

Gas chromatography-mass spectrometry

LB:

Luria-Bertani

T m :

Phase transition temperature

2-acyl-GPE:

2-Acylglycerophosphoethanolamine

20:0:

Eicosanoic acid

20:1:

cis-11-Eicosenoic acid

20:2:

cis-11,14-Eicosadienoic acid

20:3:

cis-8,11,14-Eicosatrienoic acid

20:4:

cis-5,8,11,14-Eicosatetraenoic acid (arachidonic acid)

20:5:

cis-5,8,11,14,17-Eicosapentaenoic acid

22:6:

cis-4,7,10,13,16,19-Docosahexaenoic acid

18:1:

cis-9-Octadecenoic acid (oleic acid)

18:2:

cis-9,12-Octadecadienoic acid (linoleic acid)

α-18:3:

cis-9,12,15-Octadecatrienoic acid (α-linolenic acid)

γ-18:3:

cis-6,9,12-Octadecatrienoic acid (γ-linolenic acid)

15:0:

Pentadecanoic acid

16:1:

Hexadecenoic acid

17:0:

Heptadecanoic acid

17:1:

Heptadecenoic acid

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Acknowledgments

This work was supported in part by the Global COE Program “Integrated Materials Science” (#B-09) (to N. E.), Grants-in-Aid for Scientific Research (B) 17404021 and 19404020 from JSPS (to T. K.), and a grant for Research for Promoting Technological Seeds from JST (to T. K.).

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Authors and Affiliations

  1. Institute for Chemical Research, Kyoto University, Uji, Kyoto, 611-0011, Japan

    Sho Sato, Tatsuo Kurihara, Jun Kawamoto & Nobuyoshi Esaki

  2. Faculty of Fisheries Sciences, Hokkaido University, Hakodate, Hokkaido, 041-8611, Japan

    Masashi Hosokawa

  3. Graduate School of Science, Kyoto University, Kyoto, 606-8502, Japan

    Satoshi B. Sato

Authors
  1. Sho Sato
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  2. Tatsuo Kurihara
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  3. Jun Kawamoto
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  4. Masashi Hosokawa
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  5. Satoshi B. Sato
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  6. Nobuyoshi Esaki
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Corresponding authors

Correspondence to Tatsuo Kurihara or Nobuyoshi Esaki.

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Communicated by L. Huang.

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Sato, S., Kurihara, T., Kawamoto, J. et al. Cold adaptation of eicosapentaenoic acid-less mutant of Shewanella livingstonensis Ac10 involving uptake and remodeling of synthetic phospholipids containing various polyunsaturated fatty acids. Extremophiles 12, 753–761 (2008). https://doi.org/10.1007/s00792-008-0182-6

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  • DOI: https://doi.org/10.1007/s00792-008-0182-6

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