Advertisement

Extremophiles

, Volume 23, Issue 3, pp 319–326 | Cite as

Response of neutrophilic Shewanella violacea to acid stress: growth rate, organic acid production, and gene expression

  • Lisa Lisdiana
  • Hisashi Ômura
  • Sotaro Fujii
  • Yoshihiro SambongiEmail author
Original Paper
  • 125 Downloads

Abstract

Neutrophilic Shewanella violacea is isolated from deep-sea sediments and its response to high pressure and high salinity has been investigated. Here, the pure effects of acidic pH on S. violacea physiology were examined, aiming at further understanding of its stress response mechanism. S. violacea could grow at initial pH of 5.0–7.0 without pH adjustment during the test at atmospheric pressure, and the lowest growth rate was obtained at pH 5.0. The pH of the same growth culture with an initial pH of 5.0 rose toward a neutral pH of ~ 7.0 at the exponential growth phase, indicating that S. violacea has a mechanism for acid neutralization. When S. violacea cells were grown at the fixed pH of 5.0, about five times higher concentrations of butyric and isovaleric acids were produced than at pH 7.0. The expression level of the genes encoding three enzymes for isovaleric acid synthesis from l-leucine was also found to be upregulated in S. violacea cells grown at the fixed pH of 5.0 compared with at pH 7.0 through RNA-seq analysis. Therefore, S. violacea at least produces isovaleric acid in its response to acid stress, which further deepens our understanding of the stress response mechanism inherent in this bacterium.

Keywords

Acid neutralization Acid stress Isovaleric acid pH Shewanella violacea 

Abbreviations

SPME-GC/MS

Solid-phase microextraction and gas chromatography coupled with mass spectrometry

Notes

Acknowledgements

This work was supported by Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (Nos. 26240045 and 16K07692 to Y.S.), a Grant from the Japan Society for the Promotion of Science (No. 25–1446 to S.F.), and a Grant-in-Aid for Fundamental Research from the Graduate School of Biosphere Science, Hiroshima University to S.F. L.L. was very grateful to the Indonesia Endowment Fund for Education, Ministry of Finance, Republic of Indonesia, for the scholarship.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

792_2019_1083_MOESM1_ESM.docx (150 kb)
Supplementary material 1 (DOCX 150 kb)

References

  1. Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc. Accessed 20 Aug 2018
  2. Audia JP, Webb CC, Foster JW (2001) Breaking through the acid barrier: an orchestrated response to proton stress by enteric bacteria. Int J Med Microbiol 291:97–109CrossRefGoogle Scholar
  3. Bearson S, Bearson B, Foster JW (1997) Acid stress responses in enterobacteria. FEMS Microbiol Lett 147:173–180CrossRefGoogle Scholar
  4. Bearson BL, Lee IS, Casey TA (2009) Escherichia coli O157:h7 glutamate- and arginine-dependent acid-resistance systems protect against oxidative stress during extreme acid challenge. Microbiology 155:805–812CrossRefGoogle Scholar
  5. Biffinger JC, Pietron J, Bretschger O, Nadeau LJ, Johnson GR, Williams CC, Nealson KH, Ringeisen BR (2008) The influence of acidity on microbial fuel cells containing Shewanella oneidensis. Biosens Bioelectron 24:900–905CrossRefGoogle Scholar
  6. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120CrossRefGoogle Scholar
  7. Fujii S, Masanari-Fujii M, Kobayashi S, Kato C, Nishiyama M, Harada Y, Wakai S, Sambongi Y (2018) Commonly stabilized cytochrome c from deep-sea Shewanella and Pseudomonas. Biosci Biotech Biochem 82:792–799CrossRefGoogle Scholar
  8. Fujimori K, Fujii S, Lisdiana L, Wakai S, Yagi H, Sambongi Y (2019) Differences in biochemical properties of two 5′-nucleotidases from deep- and shallow-sea Shewanella species under various harsh conditions. Biosci Biotech Biochem.  https://doi.org/10.1080/09168451.2019.1578641 Google Scholar
  9. Hau HH, Gralnick JA (2007) Ecology and biotechnology of the genus Shewanella. Annu Rev Microbiol 61:237–258CrossRefGoogle Scholar
  10. Hu XD, Pan BZ, Fu Q, Niu L, Chen MS, Xu ZF (2018) De novo transcriptome assembly of the eight major organs of Sacha Inchi (Plukenetia volubilis) and the identification of genes involved in α-linolenic acid metabolism. BMC Genom 19:380CrossRefGoogle Scholar
  11. Kato C, Sato T, Abe F, Ohmae E, Tamegai H, Nakasone K (2007) Discoveries of deep-sea piezophiles, and their pressure adapted enzymes. In: Proceedings of the 4th international conference on high pressure bioscience and biotechnology 1:114–121Google Scholar
  12. Krulwich TA, Sachs G, Padan E (2011) Molecular aspects of bacterial pH sensing and homeostasis. Nat Rev Microbiol 9:330–343CrossRefGoogle Scholar
  13. Kuribayashi T, Fujii S, Masanari M, Yamanaka M, Wakai S, Sambongi Y (2017) Difference in NaCl tolerance of membrane-bound 5′-nucleotidases purified from deep-sea and brackish water Shewanella species. Extremophiles 21:357–368CrossRefGoogle Scholar
  14. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10(R25):1–11Google Scholar
  15. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Method 25:402–408CrossRefGoogle Scholar
  16. Lund P, Tramonti A, De Biase D (2014) Coping with low pH: molecular strategies in neutralophilic bacteria. FEMS Microbiol Rev 38:1091–1125CrossRefGoogle Scholar
  17. Masanari M, Wakai S, Ishida M, Kato C, Sambongi Y (2014) Correlation between the optimal growth pressures of four Shewanella species and the stabilities of their cytochromes c 5. Extremophiles 18:617–627CrossRefGoogle Scholar
  18. Masanari M, Fujii S, Kawahara K, Oki H, Tsujino H, Maruno T, Kobayashi Y, Ohkubo T, Wakai S, Sambongi Y (2016) Comparative study on stabilization mechanism of monomeric cytochrome c 5 from deep-sea piezophilic Shewanella violacea. Biosci Biotech Biochem 80:2365–2370CrossRefGoogle Scholar
  19. Nakasone K, Ikegami A, Fujii S, Kato C, Horikoshi K (2000) Isolation and piezoresponse of the rpoA gene encoding the RNA polymerase α subunit from the deep-sea piezophilic bacterium Shewanella violacea. FEMS Microbiol Lett 193:261–268Google Scholar
  20. Ng I-S, Ndive CI, Zhou Y, Wu X (2015) Cultural optimization and metal effects of Shewanella xiamenensis BC01growth and swarming motility. Bioresour Bioprocess 2:1–10CrossRefGoogle Scholar
  21. Nogi Y, Kato C, Horikoshi K (1998) Taxonomic studies of deep-sea barophilic Shewanella strains and description of Shewanella violacea sp. nov. Arch Microbiol 170:331–338CrossRefGoogle Scholar
  22. Ohmae E, Kubota K, Nakasone K, Kato C, Gekko K (2004) Pressure-dependent activity of dihydrofolate reductase from a deep-sea bacterium Shewanella violacea strain DSS12. Chem Lett 33:798–799CrossRefGoogle Scholar
  23. Rapaport F, Khanin R, Liang Y, Pirun M, Krek A, Zumbo P, Mason CE, Socci ND, Betel D (2013) Comprehensive evaluation of differential gene expression analysis methods for RNA-seq data. Genome Biol 14:R95CrossRefGoogle Scholar
  24. Serrazanetti DI, Ndagijimana M, Sado-Kamdem SL, Corsetti A, Vogel RF, Ehrmann M, Guerzoni ME (2011) Acid-stress mediated metabolic shift in Lactobacillus sanfranciscensis LSCE1. Appl Environ Microbiol 77:2656–2666CrossRefGoogle Scholar
  25. Slonczewski JL, Fujisawa M, Dopson M, Krulwich TA (2009) Cytoplasmic pH measurement and homeostasis in bacteria and archaea. Adv Microb Physiol 55:1–79CrossRefGoogle Scholar
  26. Takahashi N (2003) Acid-neutralizing activity during amino acid fermentation by porphyromonas gingivalis, Prevotella intermedia and Fusobacterium nucleatum. Oral Microbiol Immunol 18:109–113CrossRefGoogle Scholar
  27. Takahashi N, Salto K, Schachtele CF, Yamada T (1997) Acid tolerance and acid-neutralizing activity of Porphyromonas gingivalis, Prevotella intermedia and Fusobacterium nucleatum. Oral Microbiol Immunol 12:323–328CrossRefGoogle Scholar
  28. Xiao X, Wang P, Zeng X, Bartlett DH, Wang F (2007) Shewanella psychrophile sp. nov. and Shewanella piezotolerans sp. nov., isolated from west Pacific deep-sea sediment. Int J Syst Evol Microbiol 57:60–65CrossRefGoogle Scholar

Copyright information

© Springer Japan KK, part of Springer Nature 2019

Authors and Affiliations

  • Lisa Lisdiana
    • 1
    • 2
  • Hisashi Ômura
    • 1
  • Sotaro Fujii
    • 1
  • Yoshihiro Sambongi
    • 1
    Email author
  1. 1.Graduate School of Biosphere ScienceHiroshima UniversityHigashi-HiroshimaJapan
  2. 2.Department of BiologyUniversitas Negeri SurabayaSurabayaIndonesia

Personalised recommendations