1887

Abstract

While the cell wall strictly controls cell size and morphology in bacteria, spheroplasts lack cell walls and can become enlarged in growth medium under optimal conditions. Optimal conditions depend on the bacterial species. We frequently observed extreme enlargement of spheroplasts of the radiation-resistant bacterium Deinococcus grandis in Difco Marine Broth 2216, but not in TGY broth (a commonly used growth medium for Deinococcus). Thorough investigation of media components showed that the presence of Mg or Ca promoted extreme spheroplast enlargement, synthesizing the outer membrane. Our findings strongly suggest that Mg or Ca enlarges spheroplasts, which could change the lipid composition of the spheroplast membrane.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000716
2018-09-17
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/164/11/1361.html?itemId=/content/journal/micro/10.1099/mic.0.000716&mimeType=html&fmt=ahah

References

  1. Young KD. The selective value of bacterial shape. Microbiol Mol Biol Rev 2006; 70:660–703 [View Article][PubMed]
    [Google Scholar]
  2. Young KD. Bacterial morphology: why have different shapes?. Curr Opin Microbiol 2007; 10:596–600 [View Article][PubMed]
    [Google Scholar]
  3. Schulz HN, Brinkhoff T, Ferdelman TG, Mariné MH, Teske A et al. Dense populations of a giant sulfur bacterium in Namibian shelf sediments. Science 1999; 284:493–495 [View Article][PubMed]
    [Google Scholar]
  4. Cunningham JA, Thomas CW, Bengtson S, Marone F, Stampanoni M et al. Experimental taphonomy of giant sulphur bacteria: implications for the interpretation of the embryo-like Ediacaran Doushantuo fossils. Proc Biol Sci 2012; 279:1857–1864 [View Article][PubMed]
    [Google Scholar]
  5. Typas A, Banzhaf M, van den Berg van Saparoea B, Verheul J, Biboy J et al. Regulation of peptidoglycan synthesis by outer-membrane proteins. Cell 2010; 143:1097–1109 [View Article][PubMed]
    [Google Scholar]
  6. Ranjit DK, Young KD. The Rcs stress response and accessory envelope proteins are required for de novo generation of cell shape in Escherichia coli. J Bacteriol 2013; 195:2452–2462 [View Article][PubMed]
    [Google Scholar]
  7. Egan AJ, Jean NL, Koumoutsi A, Bougault CM, Biboy J et al. Outer-membrane lipoprotein LpoB spans the periplasm to stimulate the peptidoglycan synthase PBP1B. Proc Natl Acad Sci USA 2014; 111:8197–8202 [View Article][PubMed]
    [Google Scholar]
  8. Ranjit DK, Young KD. Colanic acid intermediates prevent de novo shape recovery of Escherichia coli spheroplasts, calling into question biological roles previously attributed to colanic acid. J Bacteriol 2016; 198:1230–1240 [View Article][PubMed]
    [Google Scholar]
  9. Ranjit DK, Jorgenson MA, Young KD. PBP1B glycosyltransferase and transpeptidase activities play different essential roles during the de novo regeneration of rod morphology in Escherichia coli. J Bacteriol 2017; 199:e00612 [View Article][PubMed]
    [Google Scholar]
  10. Kuroda T, Okuda N, Saitoh N, Hiyama T, Terasaki Y et al. Patch clamp studies on Ion pumps of the cytoplasmic membrane of Escherichia coli. J Biol Chem 1998; 273:16897–16904 [View Article]
    [Google Scholar]
  11. Nakamura K, Ikeda S, Matsuo T, Hirata A, Takehara M et al. Patch clamp analysis of the respiratory chain in Bacillus subtilis. Biochim Biophys Acta 2011; 1808:1103–1107 [View Article][PubMed]
    [Google Scholar]
  12. Bendezú FO, de Boer PA. Conditional lethality, division defects, membrane involution, and endocytosis in mre and mrd shape mutants of Escherichia coli. J Bacteriol 2008; 190:1792–1811 [View Article][PubMed]
    [Google Scholar]
  13. Takahashi S, Nishida H. Quantitative analysis of chromosomal and plasmid DNA during the growth of spheroplasts of Escherichia coli. J Gen Appl Microbiol 2015; 61:262–265 [View Article][PubMed]
    [Google Scholar]
  14. Takahashi S, Takayanagi A, Takahashi Y, Oshima T, Nishida H. Comparison of transcriptomes of enlarged spheroplasts of Erythrobacter litoralis and Lelliottia amnigena. AIMS Microbiol 2016; 2:152–189
    [Google Scholar]
  15. Corry B, Martinac B. Bacterial mechanosensitive channels: experiment and theory. Biochim Biophys Acta 2008; 1778:1859–1870 [View Article][PubMed]
    [Google Scholar]
  16. Martinac B, Rohde PR, Cranfield CG, Nomura T. Patch clamp electrophysiology for the study of bacterial ion channels in giant spheroplasts of E. coli. Methods Mol Biol 2013; 966:367–380 [View Article][PubMed]
    [Google Scholar]
  17. Takahashi S, Nishida H. Growth of Enterobacter amnigenus and Escherichia coli spheroplasts in marine broth containing penicillin. Bull Toyama Pref Univ 2016; 26:27–30
    [Google Scholar]
  18. Takahashi S, Nishida H. Comparison of gene expression among normally divided cells, elongated cells, spheroplasts at the beginning of growth, and enlarged spheroplasts at 43 h of growth in Lelliottia amnigena. Gene Rep 2017; 7:87–90 [View Article]
    [Google Scholar]
  19. Takayanagi A, Takahashi S, Nishida H. Requirement of dark culture condition for enlargement of spheroplasts of the aerobic anoxygenic photosynthetic marine bacterium Erythrobacter litoralis. J Gen Appl Microbiol 2016; 62:14–17 [View Article][PubMed]
    [Google Scholar]
  20. Nakazawa M, Nishida H. Effects of light and oxygen on the enlargement of spheroplasts of the facultative anaerobic anoxygenic photosynthetic bacterium Rhodospirillum rubrum. J Biotech Bioeng 2017; 3:14
    [Google Scholar]
  21. Anderson R, Hansen K. Structure of a novel phosphoglycolipid from Deinococcus radiodurans. J Biol Chem 1985; 260:12219–12223[PubMed]
    [Google Scholar]
  22. Huang Y, Anderson R. Structure of a novel glucosamine-containing phosphoglycolipid from Deinococcus radiodurans. J Biol Chem 1989; 264:18667–18672[PubMed]
    [Google Scholar]
  23. Makarova KS, Aravind L, Wolf YI, Tatusov RL, Minton KW et al. Genome of the extremely radiation-resistant bacterium Deinococcus radiodurans viewed from the perspective of comparative genomics. Microbiol Mol Biol Rev 2001; 65:44–79 [View Article][PubMed]
    [Google Scholar]
  24. Sohlenkamp C, Geiger O. Bacterial membrane lipids: diversity in structures and pathways. FEMS Microbiol Rev 2016; 40:133–159 [View Article][PubMed]
    [Google Scholar]
  25. Oyaizu H, Stackebrandt E, Schleifer KH, Ludwig W, Pohla H et al. A radiation-resistant rod-shaped bacterium, Deinobacter grandis gen. nov., sp. nov., with peptidoglycan containing ornithine. Int J Syst Bacteriol 1987; 37:62–67 [View Article]
    [Google Scholar]
  26. Rainey FA, Nobre MF, Schumann P, Stackebrandt E, da Costa MS. Phylogenetic diversity of the deinococci as determined by 16S ribosomal DNA sequence comparison. Int J Syst Bacteriol 1997; 47:510–514 [View Article][PubMed]
    [Google Scholar]
  27. Satoh K, Tu Z, Ohba H, Narumi I. Development of versatile shuttle vectors for Deinococcus grandis. Plasmid 2009; 62:1–9 [View Article][PubMed]
    [Google Scholar]
  28. Satoh K, Onodera T, Omoso K, Takeda-Yano K, Katayama T et al. Draft genome sequence of the radioresistant bacterium Deinococcus grandis, isolated from freshwater fish in Japan. Genome Announc 2016; 4:e01631 [View Article][PubMed]
    [Google Scholar]
  29. Farci D, Bowler MW, Kirkpatrick J, McSweeney S, Tramontano E et al. New features of the cell wall of the radio-resistant bacterium Deinococcus radiodurans. Biochim Biophys Acta 2014; 1838:1978–1984 [View Article][PubMed]
    [Google Scholar]
  30. Al-Bakri G. Genetic studies on Deinococcus spp. using spheroplasts and gene cloning. A thesis presented for the degree of Doctor of Philosophy, University of Edinburgh; 1985
  31. Chou FI, Tan ST. Salt-mediated multicell formation in Deinococcus radiodurans. J Bacteriol 1991; 173:3184–3190 [View Article][PubMed]
    [Google Scholar]
  32. Mitsui H, Hattori R, Watanabe H, Tonosaki A, Hattori T. Na+-induced structural change of a soil bacterium, S34, and Ca2+ requirement for preserving its original structure. J Bacteriol 1997; 179:3350–3353 [View Article][PubMed]
    [Google Scholar]
  33. Farris C, Sanowar S, Bader MW, Pfuetzner R, Miller SI. Antimicrobial peptides activate the Rcs regulon through the outer membrane lipoprotein RcsF. J Bacteriol 2010; 192:4894–4903 [View Article][PubMed]
    [Google Scholar]
  34. D'Amato RF, Thornsberry C, Baker CN, Kirven LA. Effect of calcium and magnesium ions on the susceptibility of Pseudomonas species to tetracycline, gentamicin polymyxin B, and carbenicillin. Antimicrob Agents Chemother 1975; 7:596–600 [View Article][PubMed]
    [Google Scholar]
  35. Katz L, Baltz RH. Natural product discovery: past, present, and future. J Ind Microbiol Biotechnol 2016; 43:155–176 [View Article][PubMed]
    [Google Scholar]
  36. Campbell EA, Korzheva N, Mustaev A, Murakami K, Nair S et al. Structural mechanism for rifampicin inhibition of bacterial RNA polymerase. Cell 2001; 104:901–912 [View Article][PubMed]
    [Google Scholar]
  37. Lederberg J. Bacterial protoplasts induced by penicillin. Proc Natl Acad Sci USA 1956; 42:574–577 [View Article][PubMed]
    [Google Scholar]
  38. Tada Y, Yamaguchi J. Spheroplast induction in clinical isolates of Serratia marcescens in the presence of Ca2+ or Mg2+. J Clin Microbiol 1987; 25:2154–2158[PubMed]
    [Google Scholar]
  39. Clapham DE. Calcium signaling. Cell 1995; 80:259–268 [View Article][PubMed]
    [Google Scholar]
  40. Dominguez DC. Calcium signalling in bacteria. Mol Microbiol 2004; 54:291–297 [View Article][PubMed]
    [Google Scholar]
  41. Groisman EA, Hollands K, Kriner MA, Lee EJ, Park SY et al. Bacterial Mg2+ homeostasis, transport, and virulence. Annu Rev Genet 2013; 47:625–646 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000716
Loading
/content/journal/micro/10.1099/mic.0.000716
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error