1887

Abstract

When grown with vaporized alkylphenols such as -cresol as the sole carbon and energy source, several isolated strains formed growth structures like miniature mushrooms, termed here specialized aerial architectures (SAA), that reached sizes of up to 0.8 mm in height. Microscopic examination allowed us to view the distinct developmental stages during the formation of SAA from a selected strain, sp. KL96. Initially, mounds consisting of long rod cells arose from a lawn of cells, and then highly branched structures were formed from the mounds. During the secondary stage of development, branching began after long rod cells grew outward and twisted longitudinally, serving as growth points, and the cells at the base of the mound became short rods that supported upward growth. Cells in the highly fluffy structures were eventually converted, via reductive division, into structures that resembled cocci, with a diameter of approximately 0.5 μm, that were arranged in chains. Most cells inside the SAA underwent a phase variation in order to form wrinkled colonies from cells that originally formed smooth colonies. Approximately 2 months was needed for complete development of the SAA, and viable cells were recovered from SAA that were incubated for more than a year. An extracellular polymeric matrix layer and lipid bodies appeared to play an important role in structural integrity and as a metabolic energy source, respectively. To our knowledge, similar formation of aerial structures for the purpose of substrate utilization has not been reported previously for Gram-positive bacteria.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.029926-0
2009-11-01
2024-12-08
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/11/3788.html?itemId=/content/journal/micro/10.1099/mic.0.029926-0&mimeType=html&fmt=ahah

References

  1. Alvarez H. M., Steinbuchel A. 2002; Triacylglycerols in prokaryotic microorganisms. Appl Microbiol Biotechnol 60:367–376
    [Google Scholar]
  2. Alvarez H. M., Silva R. A., Cesari A. C., Zamit A. L., Peressutti S. R., Reichelt R., Keller U., Malkus U., Rasch C. other authors 2004; Physiological and morphological responses of the soil bacterium Rhodococcus opacus strain PD630 to water stress. FEMS Microbiol Ecol 50:75–86
    [Google Scholar]
  3. Bell K. S., Philp J. C., Aw D. W., Christofi N. 1998; The genus Rhodococcus . J Appl Microbiol 85:195–210
    [Google Scholar]
  4. Branda S. S., Gonzalez-Pastor J. E., Ben-Yehuda S., Losick R., Kolter R. 2001; Fruiting body formation by Bacillus subtilis . Proc Natl Acad Sci U S A 98:11621–11626
    [Google Scholar]
  5. Brun Y. V., Shimkets L. J. 2000 Prokaryotic Development Washington, DC: Am. Soc. Microbiol;
    [Google Scholar]
  6. Chang W. S., Halverson L. J. 2003; Reduced water availability influences the dynamics, development, and ultrastructural properties of Pseudomonas putida biofilms. J Bacteriol 185:6199–6204
    [Google Scholar]
  7. Chater K. F. 2001; Regulation of sporulation in Streptomyces coelicolor A3(2): a checkpoint multiplex?. Curr Opin Microbiol 4:667–673
    [Google Scholar]
  8. Choi K. S., Veeranangouda Y., Cho K. M., Lee S. O., Jo G. R., Cho K., Lee K. 2007; Effect of gacS and gacA mutations on colony architecture, surface motility, biofilm formation and chemical toxicity in Pseudomonas sp. KL28. J Microbiol 45:492–498
    [Google Scholar]
  9. Daniel R. A., Errington J. 2003; Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 113:767–776
    [Google Scholar]
  10. de Carvalho C. C., Wick L. Y., Heipieper H. J. 2009; Cell wall adaptations of planktonic and biofilm Rhodococcus erythropolis cells to growth on C5 to C16 n-alkane hydrocarbons. Appl Microbiol Biotechnol 82:311–320
    [Google Scholar]
  11. DuBois M., Gilles K. A., Hamilton J. K., Rebers P. A., Smith F. 1956; Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
    [Google Scholar]
  12. Dworkin M., Kaiser D. 1985; Cell interactions in myxobacterial growth and development. Science 230:18–24
    [Google Scholar]
  13. Enos-Berlage J. L., McCarter L. L. 2000; Relation of capsular polysaccharide production and colonial cell organization to colony morphology in Vibrio parahaemolyticus . J Bacteriol 182:5513–5520
    [Google Scholar]
  14. Flardh K., Buttner M. J. 2009; Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat Rev Microbiol 7:36–49
    [Google Scholar]
  15. Goodfellow M. 1989; Section 26: Nocardioform actinomycetes genus Rhodococcus . In Bergey's Manual of Systematic Bacteriology pp 2362–2371 Edited by Holt J. G. Baltimore, MD: Williams and Wilkins;
    [Google Scholar]
  16. Goodfellow M., Williams S. T. 1983; Ecology of actinomycetes. Annu Rev Microbiol 37:189–216
    [Google Scholar]
  17. Goodfellow M., Alderson G., Chun J. 1998; Rhodococcal systematics: problems and developments. Antonie Van Leeuwenhoek 74:3–20
    [Google Scholar]
  18. Jeong J. J., Kim J. H., Kim C. K., Hwang I., Lee K. 2003; 3- and 4-alkylphenol degradation pathway in Pseudomonas sp. strain KL28: genetic organization of the lap gene cluster and substrate specificities of phenol hydroxylase and catechol 2,3-dioxygenase. Microbiology 149:3265–3277
    [Google Scholar]
  19. Kim J. S., Kim J. H., Ryu E. K., Kim J.-K., Kim C.-K., Hwang I., Lee K. 2004; Versatile catabolic properties of the Tn4371-encoded bph pathway in Comamonas testosteroni (formerly Pseudomonas sp.) NCIMB 10643. J Microbiol Biotechnol 14:302–311
    [Google Scholar]
  20. Klausen M., Gjermansen M., Kreft J. U., Tolker-Nielsen T. 2006; Dynamics of development and dispersal in sessile microbial communities: examples from Pseudomonas aeruginosa and Pseudomonas putida model biofilms. FEMS Microbiol Lett 261:1–11
    [Google Scholar]
  21. Larkin M. J., Kulakov L. A., Allen C. C. 2005; Biodegradation and Rhodococcus – masters of catabolic versatility. Curr Opin Biotechnol 16:282–290
    [Google Scholar]
  22. LeBlanc J. C., Goncalves E. R., Mohn W. W. 2008; Global response to desiccation stress in the soil actinomycete Rhodococcus jostii RHA1. Appl Environ Microbiol 74:2627–2636
    [Google Scholar]
  23. Lee K., Veeranagouda Y. 2009; Ultramicrocells form by reductive division in macroscopic Pseudomonas aerial structures. Environ Microbiol 11:1117–1125
    [Google Scholar]
  24. Ma L., Conover M., Lu H., Parsek M. R., Bayles K., Wozniak D. J. 2009; Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Pathog 5:e1000354
    [Google Scholar]
  25. Martinkova L., Uhnakova B., Patek M., Nesvera J., Kren V. 2009; Biodegradation potential of the genus Rhodococcus . Environ Int 35:162–177
    [Google Scholar]
  26. Matsui H., Wagner V. E., Hill D. B., Schwab U. E., Rogers T. D., Button B., Taylor R. M. II, Superfine R., Rubinstein M. other authors 2006; A physical linkage between cystic fibrosis airway surface dehydration and Pseudomonas aeruginosa biofilms. Proc Natl Acad Sci U S A 103:18131–18136
    [Google Scholar]
  27. McLeod M. P., Warren R. L., Hsiao W. W., Araki N., Myhre M., Fernandes C., Miyazawa D., Wong W., Lillquist A. L. other authors 2006; The complete genome of Rhodococcus sp. RHA1 provides insights into a catabolic powerhouse. Proc Natl Acad Sci U S A 103:15582–15587
    [Google Scholar]
  28. Paul J. H., Myers B. 1982; Fluorometric determination of DNA in aquatic microorganisms by use of Hoechst 33258. Appl Environ Microbiol 43:1393–1399
    [Google Scholar]
  29. Roslev P., King G. M. 1993; Application of a tetrazolium salt with a water-soluble formazan as an indicator of viability in respiring bacteria. Appl Environ Microbiol 59:2891–2896
    [Google Scholar]
  30. Sandhu A., Halverson L. J., Beattie G. A. 2009; Identification and genetic characterization of phenol-degrading bacteria from leaf microbial communities. Microb Ecol 57:276–285
    [Google Scholar]
  31. Shapiro J. A. 1998; Thinking about bacterial populations as multicellular organisms. Annu Rev Microbiol 52:81–104
    [Google Scholar]
  32. Shapiro J. A., Hsu C. 1989; Escherichia coli K-12 cell–cell interactions seen by time-lapse video. J Bacteriol 171:5963–5974
    [Google Scholar]
  33. Stanier R. Y., Palleroni N. J., Doudoroff M. 1966; The aerobic pseudomonads: a taxonomic study. J Gen Microbiol 43:159–271
    [Google Scholar]
  34. Sutherland I. W. 2001; The biofilm matrix – an immobilized but dynamic microbial environment. Trends Microbiol 9:222–227
    [Google Scholar]
  35. Warhurst A. M., Fewson C. A. 1994; Biotransformations catalyzed by the genus Rhodococcus . Crit Rev Biotechnol 14:29–73
    [Google Scholar]
  36. Whyte L. G., Slagman S. J., Pietrantonio F., Bourbonniere L., Koval S. F., Lawrence J. R., Inniss W. E., Greer C. W. 1999; Physiological adaptations involved in alkane assimilation at a low temperature by Rhodococcus sp. strain Q15. Appl Environ Microbiol 65:2961–2968
    [Google Scholar]
/content/journal/micro/10.1099/mic.0.029926-0
Loading
/content/journal/micro/10.1099/mic.0.029926-0
Loading

Data & Media loading...

Supplements

Supplementary material 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