1887

Microbiology Society logo

Volume 162, Issue 7

Mechanisms of extracellular S globule production and degradation in via dynamic cell–globule interactions Free

Abstract

The are anoxygenic phototrophs that produce solid, extracellular elemental sulfur globules as an intermediate step in the oxidation of sulfide to sulfate. These organisms must export sulfur while preventing cell encrustation during S globule formation; during globule degradation they must find and mobilize the sulfur for intracellular oxidation to sulfate. To understand how the address these challenges, we characterized the spatial relationships and physical dynamics of cells and S globules by light and electron microscopy. commonly formed globules at a distance from cells. Soluble polysulfides detected during globule production may allow for remote nucleation of globules. Polysulfides were also detected during globule degradation, probably produced as an intermediate of sulfur oxidation by attached cells. Polysulfides could feed unattached cells, which made up over 80% of the population and had comparable growth rates to attached cells. Given that S is formed remotely from cells, there is a question as to how cells are able to move toward S in order to attach. Time-lapse microscopy shows that is in fact capable of twitching motility, a finding supported by the presence of genes encoding type IV pili. Our results show how is able to avoid mineral encrustation and benefit from globule degradation even when not attached. In the environment, may also benefit from soluble sulfur species produced by other sulfur-oxidizing or sulfur-reducing bacteria as these organisms interact with its biogenic S globules.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): elemental sulfur , green sulfur bacteria , microbe–mineral interactions , microscopy , motility and time-lapse
© 2016 The Authors
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000294
2016-07-01
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/162/7/1125.html?itemId=/content/journal/micro/10.1099/mic.0.000294&mimeType=html&fmt=ahah

References

  1. Beliaev A. S., Saffarini D. A. 1998; Shewanella putrefaciens mtrB encodes an outer membrane protein required for Fe(III) and Mn(IV) reduction. J Bacteriol 180:6292–6297[PubMed]
     [Google Scholar]
  2. Berry J. L., Pelicic V. 2015; Exceptionally widespread nanomachines composed of type IV pilins: the prokaryotic Swiss Army knives. FEMS Microbiol Rev 39:fuu001 [View Article][PubMed]
     [Google Scholar]
  3. Brocher J. 2015; The BioVoxxel image processing and analysis toolbox. In European BioImage Analysis SymposiumParis, France
     [Google Scholar]
  4. Brune D. C. 1995; Isolation and characterization of sulfur globule proteins from Chromatium vinosum and Thiocapsa roseopersicina . Arch Microbiol 163:391–399[PubMed] [CrossRef]
     [Google Scholar]
  5. Bryant D. A., Frigaard N. U. 2006; Prokaryotic photosynthesis and phototrophy illuminated. Trends Microbiol 14:488–496 [View Article][PubMed]
     [Google Scholar]
  6. Burrows L. L. 2012; Pseudomonas aeruginosa twitching motility: type IV pili in action. Annu Rev Microbiol 66:493–520 [View Article][PubMed]
     [Google Scholar]
  7. Chan L.-K., Morgan-Kiss R., Hanson T. E. 2008a; Genetic and proteomic studies of sulfur oxidation in Chlorobium tepidum (syn. Chlorobaculum tepidum). In Sulfur Metabolism in Phototrophic Organisms pp. 357–373 Springer; [CrossRef]
     [Google Scholar]
  8. Chan L.-K., Morgan-Kiss R., Hanson T. E. 2008b; Sulfur oxidation in Chlorobium tepidum (syn. Chlorobaculum tepidum): genetic and proteomic analyses. In Microbial Sulfur Metabolism pp. 117–126 Edited by Dahl C., Friedrich C. G. Berlin/Heidelberg: Springer; [CrossRef]
     [Google Scholar]
  9. Chan L.-K., Weber T. S., Morgan-Kiss R. M., Hanson T. E. 2008c; A genomic region required for phototrophic thiosulfate oxidation in the green sulfur bacterium Chlorobium tepidum (syn. Chlorobaculum tepidum). Microbiology 154:818–829 [View Article]
     [Google Scholar]
  10. Chan C. S., Fakra S. C., Emerson D., Fleming E. J., Edwards K. J. 2011; Lithotrophic iron-oxidizing bacteria produce organic stalks to control mineral growth: implications for biosignature formation. ISME J 5:717–727 [View Article][PubMed]
     [Google Scholar]
  11. Chaudhuri R. G., Paria S. 2010; Synthesis of sulfur nanoparticles in aqueous surfactant solutions. J Colloid Interface Sci 343:439–446 [View Article][PubMed]
     [Google Scholar]
  12. Dahl C., Prange A. 2006; Bacterial sulfur globules: occurrence, structure and metabolism. In Inclusions in Prokaryotes , pp. 21–51 Edited by Shively J. M. Berlin/Heidelberg: Springer; [CrossRef]
     [Google Scholar]
  13. Donà C. 2011; Mobilization of sulfur by green sulfur bacteria: physiological and molecular studies on Chlorobaculum parvum DSM 263 . Chemie der Universität Bremen, Bremen:
  14. Eckert B., Okazaki R., Steudel R., Takeda N., Tokitoh N., Wong M. 2003; Elemental sulfur and sulfur-rich compounds II. Top Curr Chem 231:32–98
     [Google Scholar]
  15. Franz B., Lichtenberg H., Hormes J., Modrow H., Dahl C., Prange A. 2007; Utilization of solid ‘elemental’ sulfur by the phototrophic purple sulfur bacterium Allochromatium vinosum: a sulfur K-edge X-ray absorption spectroscopy study. Microbiology 153:1268–1274 [View Article][PubMed]
     [Google Scholar]
  16. Franz B., Gehrke T., Lichtenberg H., Hormes J., Dahl C., Prange A. 2009; Unexpected extracellular and intracellular sulfur species during growth of Allochromatium vinosum with reduced sulfur compounds. Microbiology 155:2766–2774 [View Article][PubMed]
     [Google Scholar]
  17. Friedrich C. G., Rother D., Bardischewsky F., Quentmeier A., Fischer J. 2001; Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism?. Appl Environ Microbiol 67:2873–2882 [View Article][PubMed]
     [Google Scholar]
  18. Frigaard N.-U., Dahl C. 2008; Sulfur metabolism in phototrophic sulfur bacteria. Adv Microb Physiol 54:103–200 [CrossRef]
     [Google Scholar]
  19. Fuller S. J., McMillan D. G., Renz M. B., Schmidt M., Burke I. T., Stewart D. I. 2014; Extracellular electron transport-mediated Fe(III) reduction by a community of alkaliphilic bacteria that use flavins as electron shuttles. Appl Environ Microbiol 80:128–137 [View Article][PubMed]
     [Google Scholar]
  20. Garcia A. A., Druschel G. K. 2014; Elemental sulfur coarsening kinetics. Geochem Trans 15: [View Article][PubMed]
     [Google Scholar]
  21. George G. N., Gnida M., Bazylinski D. A., Prince R. C., Pickering I. J. 2008; X-ray absorption spectroscopy as a probe of microbial sulfur biochemistry: the nature of bacterial sulfur globules revisited. J Bacteriol 190:6376–6383 [View Article][PubMed]
     [Google Scholar]
  22. Gilbert B., Zhang H., Huang F., Finnegan M. P., Waychunas G. A., Banfield J. F. 2003; Special phase transformation and crystal growth pathways observed in nanoparticles. Geochem Trans 4:20–27 [CrossRef]
     [Google Scholar]
  23. Gralnick J. A., Newman D. K. 2007; Extracellular respiration. Mol Microbiol 65:1–11 [View Article][PubMed]
     [Google Scholar]
  24. Gregersen L. H., Bryant D. A., Frigaard N. U. 2011; Mechanisms and evolution of oxidative sulfur metabolism in green sulfur bacteria. Front Microbiol 2: [View Article][PubMed]
     [Google Scholar]
  25. Hanson T. E., Bonsu E., Tuerk A., Marnocha C. L., Powell D. H., Chan C. S. 2015; Chlorobaculum tepidum growth on biogenic S0 as the sole photosynthetic electron donor. Environ Microbiol [View Article][PubMed]
     [Google Scholar]
  26. Hegler F., Schmidt C., Schwarz H., Kappler A. 2010; Does a low-pH microenvironment around phototrophic Fe(II)-oxidizing bacteria prevent cell encrustation by Fe(III) minerals?. FEMS Microbiol Ecol 74:592–600 [View Article][PubMed]
     [Google Scholar]
  27. Holkenbrink C., Barbas S. O., Mellerup A., Otaki H., Frigaard N. U. 2011; Sulfur globule oxidation in green sulfur bacteria is dependent on the dissimilatory sulfite reductase system. Microbiology 157:1229–1239 [View Article][PubMed]
     [Google Scholar]
  28. Kachlany S. C., Planet P. J., Desalle R., Fine D. H., Figurski D. H., Kaplan J. B. 2001; flp-1, the first representative of a new pilin gene subfamily, is required for non-specific adherence of Actinobacillus actinomycetemcomitans. Mol Microbiol 40:542–554 [View Article][PubMed]
     [Google Scholar]
  29. Kleinjan W. E., de Keizer A., Janssen A. J. 2003; Biologically produced sulfur. In Elemental Sulfur and Sulfur-Rich Compounds I , pp. 167–188 Edited by Steudel R. Berlin/Heidelberg: Springer Verlag; [CrossRef]
     [Google Scholar]
  30. Lloyd J. R. 2003; Microbial reduction of metals and radionuclides. FEMS Microbiol Rev 27:411–425[PubMed] [CrossRef]
     [Google Scholar]
  31. Lloyd J. R., Blunt-Harris E. L., Lovley D. R. 1999; The periplasmic 9.6-kilodalton c-type cytochrome of Geobacter sulfurreducens is not an electron shuttle to Fe(III). J Bacteriol 181:7647–7649[PubMed]
     [Google Scholar]
  32. Lovley D. R., Coates J. D., Blunt-Harris E. L., Phillips E. J. P., Woodward J. C. 1996; Humic substances as electron acceptors for microbial respiration. Nature 382:445–448 [View Article]
     [Google Scholar]
  33. Maier B., Wong G. C. 2015; How bacteria use type IV pili machinery on surfaces. Trends Microbiol 23:775–788 [View Article][PubMed]
     [Google Scholar]
  34. Mangold S., Valdés J., Holmes D. S., Dopson M. 2011; Sulfur metabolism in the extreme acidophile Acidithiobacillus caldus . Front Microbiol 2: [View Article][PubMed]
     [Google Scholar]
  35. Marsili E., Baron D. B., Shikhare I. D., Coursolle D., Gralnick J. A., Bond D. R. 2008; Shewanella secretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci U S A 105:3968–3973 [View Article][PubMed]
     [Google Scholar]
  36. Morgan-Kiss R. M., Chan L. K., Modla S., Weber T. S., Warner M., Czymmek K. J., Hanson T. E. 2009; Chlorobaculum tepidum regulates chlorosome structure and function in response to temperature and electron donor availability. Photosynth Res 99:11–21 [View Article][PubMed]
     [Google Scholar]
  37. Myers C. R., Myers J. M. 1992; Localization of cytochromes to the outer membrane of anaerobically grown Shewanella putrefaciens MR-1. J Bacteriol 174:3429–3438[PubMed] [CrossRef]
     [Google Scholar]
  38. Overmann J., Garcia-Pichel F. 2013; The phototrophic way of life. In The Prokaryotes pp. 203–257 Edited by Rosenberg E., DeLong E. F., Lory S., Stackebrandt E., Thompson F. Berlin/Heidelberg: Springer; [CrossRef]
     [Google Scholar]
  39. Pibernat I. V., Abella C. A. 1996; Sulfide pulsing as the controlling factor of spinae production in Chlorobium limicola strain UdG 6038. Arch Microbiol 165:272–278[PubMed] [CrossRef]
     [Google Scholar]
  40. Pickering I. J., George G. N., Yu E. Y., Brune D. C., Tuschak C., Overmann J., Beatty J. T., Prince R. C. 2001; Analysis of sulfur biochemistry of sulfur bacteria using X-ray absorption spectroscopy. Biochemistry 40:8138–8145 [View Article][PubMed]
     [Google Scholar]
  41. Prange A., Chauvistré R., Modrow H., Hormes J., Trüper H. G., Dahl C. 2002; Quantitative speciation of sulfur in bacterial sulfur globules: X-ray absorption spectroscopy reveals at least three different species of sulfur. Microbiology 148:267–276 [View Article][PubMed]
     [Google Scholar]
  42. Rethmeier J., Rabenstein A., Langer M., Fischer U. 1997; Detection of traces of oxidized and reduced sulfur compounds in small samples by combination of different high-performance liquid chromatography methods. J Chromatogr A 760:295–302 [View Article]
     [Google Scholar]
  43. Saini G., Chan C. S. 2013; Near-neutral surface charge and hydrophilicity prevent mineral encrustation of Fe-oxidizing micro-organisms. Geobiology 11:191–200 [View Article][PubMed]
     [Google Scholar]
  44. Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S. et al. 2012; Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682 [View Article][PubMed]
     [Google Scholar]
  45. Shi L., Richardson D. J., Wang Z., Kerisit S. N., Rosso K. M., Zachara J. M., Fredrickson J. K. 2009; The roles of outer membrane cytochromes of Shewanella and Geobacter in extracellular electron transfer. Environ Microbiol Rep 1:220–227 [View Article][PubMed]
     [Google Scholar]
  46. Steudel R. 1996; Mechanism for the formation of elemental sulfur from aqueous sulfide in chemical and microbiological desulfurization processes. Ind Eng Chem Res 35:1417–1423 [View Article]
     [Google Scholar]
  47. Steudel R. 2003; Aqueous sulfur sols. In Elemental Sulfur and Sulfur-Rich Compounds I pp. 153–166 Edited by Steudel R. Berlin/Heidelberg: Springer Verlag; [CrossRef]
     [Google Scholar]
  48. Steudel R., Göbel T., Holdt G. 1988; The molecular composition of hydrophilic sulfur sols prepared by acid decomposition of thiosulfate. Z Naturforsch C 43:203–218 [View Article]
     [Google Scholar]
  49. Then J., Trüper H. G. 1984; Utilization of sulfide and elemental sulfur by Ectothiorhodospira halochloris . Arch Microbiol 139:295–298 [View Article]
     [Google Scholar]
  50. Truper H. G., Fischer U. 1982; Anaerobic oxidation of sulphur compounds as electron donors for bacterial photosynthesis. Philos Trans R Soc Lond B Biol Sci 298:529–542 [View Article]
     [Google Scholar]
  51. Trüper H. G., Genovese S. 1968; Characterization of photosynthetic sulfur bacteria causing red water in Lake Faro (Messina, Sicily). Limnol Oceanogr 13:225–232 [View Article]
     [Google Scholar]
  52. Van Gemerden H. 1984; The sulfide affinity of phototrophic bacteria in relation to the location of elemental sulfur. Arch Microbiol 139:289–294 [View Article]
     [Google Scholar]
  53. van Gemerden H. 1986; Production of elemental sulfur by green and purple sulfur bacteria. Arch Microbiol 146:52–56 [View Article]
     [Google Scholar]
  54. Visscher P. T., van Gemerden H. 1988; Growth of Chlorobium limicola f. thiosulfatophilum on polysulfides. In Green Photosynthetic Bacteria pp. 287–294 Edited by Olson J. M., Ormerod J. G., Amesz J., Stackebrandt E., Trüper H. G. Springer; [CrossRef]
     [Google Scholar]
  55. Wahlund T. M., Woese C. R., Castenholz R. W., Madigan M. T. 1991; A thermophilic green sulfur bacterium from New Zealand hot springs, Chlorobium tepidum sp. nov. Arch Microbiol 156:81–90 [View Article]
     [Google Scholar]
  56. Warthmann R., Cypionka H., Pfennig N. 1992; Photoproduction of H2 from acetate by syntrophic cocultures of green sulfur bacteria and sulfur-reducing bacteria. Arch Microbiol 157:343–348 [View Article]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000294
Loading
Mechanisms of extracellular S0 globule production and degradation in Chlorobaculumtepidum via dynamic cell–globule interactions
Microbiology 162, 1125 (2016); https://doi.org/10.1099/mic.0.000294
/content/journal/micro/10.1099/mic.0.000294
/content/journal/micro/10.1099/mic.0.000294
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Supplementary File 2

Supplementary File 3

Supplementary File 4

Supplementary File 5

Most cited Most Cited RSS feed

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