Editor's Choice Improved growth and morphological plasticity of Free

Abstract

Some microbes display pleomorphism, showing variable cell shapes in a single culture, whereas others differentiate to adapt to changed environmental conditions. The pleomorphic archaeon commonly forms discoid-shaped (‘plate’) cells in culture, but may also be present as rods, and can develop into motile rods in soft agar, or longer filaments in certain biofilms. Here we report improvement of growth in both semi-defined and complex media by supplementing with eight trace element micronutrients. With these supplemented media, transient development of plate cells into uniformly shaped rods was clearly observed during the early log phase of growth; cells then reverted to plates for the late log and stationary phases. In media prepared with high-purity water and reagents, without supplemental trace elements, rods and other complex elongated morphologies (‘pleomorphic rods’) were observed at all growth stages of the culture; the highly elongated cells sometimes displayed a substantial tubule at one or less frequently both poles, as well as unusual tapered and highly curved forms. Polar tubules were observed forming by initial mid-cell narrowing or tubulation, causing a dumbbell-like shape, followed by cell division towards one end. Formation of the uniform early log-phase rods, as well as the pleomorphic rods and tubules were dependent on the function of the tubulin-like cytoskeletal protein, CetZ1. Our results reveal the remarkable morphological plasticity of cells in response to multiple culture conditions, and should facilitate the use of this species in further studies of archaeal biology.

Funding
This study was supported by the:
  • National Science Foundation (Award 1817518)
    • Principle Award Recipient: MechthildPohlschroder
  • Australian Research Council (Award DP160101076)
    • Principle Award Recipient: IainGeoffrey Duggin
  • Australian Research Council (Award FT160100010)
    • Principle Award Recipient: IainGeoffrey Duggin
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.001012
2021-01-18
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/167/2/micro001012.html?itemId=/content/journal/micro/10.1099/mic.0.001012&mimeType=html&fmt=ahah

References

  1. Mullakhanbhai MF, Larsen H. Halobacterium volcanii spec. nov., a dead sea Halobacterium with a moderate salt requirement. Arch Microbiol 1975; 104:207–214 [View Article][PubMed]
    [Google Scholar]
  2. Bisson-Filho AW, Zheng J, Garner E. Archaeal imaging: leading the hunt for new discoveries. Mol Biol Cell 2018; 29:1675–1681 [View Article][PubMed]
    [Google Scholar]
  3. Delmas S, Duggin IG, Allers T. DNA damage induces nucleoid compaction via the Mre11-Rad50 complex in the archaeon Haloferax volcanii . Mol Microbiol 2013; 87:168–179 [View Article][PubMed]
    [Google Scholar]
  4. Liao Y, Ithurbide S, de Silva RT, Erdmann S, Duggin IG. Archaeal cell biology: diverse functions of tubulin-like cytoskeletal proteins at the cell envelope. Emerg Top Life Sci 2018; 2:547–559
    [Google Scholar]
  5. Chimileski S, Franklin MJ, Papke RT. Biofilms formed by the archaeon Haloferax volcanii exhibit cellular differentiation and social motility, and facilitate horizontal gene transfer. BMC Biol 2014; 12:65 [View Article][PubMed]
    [Google Scholar]
  6. Duggin IG, Aylett CH, Walsh JC, Michie KA, Wang Q et al. CetZ tubulin-like proteins control archaeal cell shape. Nature 2015; 519:362–365 [View Article][PubMed]
    [Google Scholar]
  7. Abdul Halim MF, Karch KR, Zhou Y, Haft DH, Garcia BA et al. Permuting the PGF signature motif blocks both Archaeosortase-Dependent C-terminal cleavage and prenyl lipid attachment for the Haloferax volcanii S-layer glycoprotein. J Bacteriol 2015; 198:808–815 [View Article][PubMed]
    [Google Scholar]
  8. Abdul-Halim MF, Schulze S, DiLucido A, Pfeiffer F, Bisson Filho AW et al. Lipid anchoring of Archaeosortase substrates and Midcell growth in haloarchaea. mBio 2020; 11:e00349-20 [View Article][PubMed]
    [Google Scholar]
  9. Allers T, Barak S, Liddell S, Wardell K, Mevarech M. Improved strains and plasmid vectors for conditional overexpression of His-tagged proteins in Haloferax volcanii . Appl Environ Microbiol 2010; 76:1759–1769 [View Article][PubMed]
    [Google Scholar]
  10. Allers T, Ngo HP, Mevarech M, Lloyd RG. Development of additional selectable markers for the halophilic archaeon Haloferax volcanii based on the leuB and trpA genes. Appl Environ Microbiol 2004; 70:943–953 [View Article][PubMed]
    [Google Scholar]
  11. Ducret A, Quardokus EM, Brun YV. MicrobeJ, a tool for high throughput bacterial cell detection and quantitative analysis. Nat Microbiol 2016; 1:16077 [View Article][PubMed]
    [Google Scholar]
  12. Li Z, Kinosita Y, Rodriguez-Franco M, Nußbaum P, Braun F et al. Positioning of the motility machinery in halophilic archaea. mBio 2019; 10:e00377–19 [View Article][PubMed]
    [Google Scholar]
  13. Cline SW, Schalkwyk LC, Doolittle WF. Transformation of the archaebacterium Halobacterium volcanii with genomic DNA. J Bacteriol 1989; 171:4987–4991 [View Article][PubMed]
    [Google Scholar]
  14. Hattori T, Shiba H, Ashiki K-ichi, Araki T, Nagashima YK et al. Anaerobic growth of haloarchaeon Haloferax volcanii by denitrification is controlled by the transcription regulator NarO. J Bacteriol 2016; 198:1077–1086 [View Article][PubMed]
    [Google Scholar]
  15. Maurer S, Ludt K, Soppa J. Characterization of copy number control of two Haloferax volcanii replication origins using deletion mutants and haloarchaeal artificial chromosomes. J Bacteriol 2018; 200: 01 01 2018 [View Article][PubMed]
    [Google Scholar]
  16. Nissenbaum A. Minor and trace elements in dead sea water. Chem Geol 1977; 19:99–111 [View Article]
    [Google Scholar]
  17. Young KD. Bacterial morphology: why have different shapes?. Curr Opin Microbiol 2007; 10:596–600 [View Article][PubMed]
    [Google Scholar]
  18. Justice SS, Hunstad DA, Cegelski L, Hultgren SJ. Morphological plasticity as a bacterial survival strategy. Nat Rev Microbiol 2008; 6:162–168 [View Article][PubMed]
    [Google Scholar]
  19. Stretton S, Danon SJ, Kjelleberg S, Goodman AE. Changes in cell morphology and motility in the marine Vibrio sp. strain S14 during conditions of starvation and recovery. FEMS Microbiol Lett 1997; 146:23–29 [View Article]
    [Google Scholar]
  20. Klein EA, Schlimpert S, Hughes V, Brun YV, Thanbichler M et al. Physiological role of stalk lengthening in Caulobacter crescentus. Commun Integr Biol 2013; 6:e24561 [View Article][PubMed]
    [Google Scholar]
  21. Wagner JK, Setayeshgar S, Sharon LA, Reilly JP, Brun YV. A nutrient uptake role for bacterial cell envelope extensions. Proc Natl Acad Sci U S A 2006; 103:11772–11777 [View Article][PubMed]
    [Google Scholar]
  22. Megaw J, Gilmore BF. Archaeal persisters: persister cell formation as a stress response in Haloferax volcanii . Front Microbiol 2017; 8:1589 [View Article][PubMed]
    [Google Scholar]
  23. Le Dain AC, Saint N, Kloda A, Ghazi A, Martinac B. Mechanosensitive ion channels of the archaeon Haloferax volcanii. J Biol Chem 1998; 273:12116–12119 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.001012
Loading
/content/journal/micro/10.1099/mic.0.001012
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

MOVIE

Supplementary material 3

MOVIE

Supplementary material 4

MOVIE

Supplementary material 5

MOVIE

Supplementary material 6

MOVIE

Most cited Most Cited RSS feed