1887

Abstract

The photosynthetic alphaproteobacterium S1H is part of the Micro-Ecological Life Support System Alternative (MELiSSA) project that is aiming to develop a closed life support system for oxygen, water and food production to support human life in space in forthcoming long-term space exploration missions. In the present study, S1H was cultured in a rotating wall vessel (RWV), simulating partial microgravity conditions on Earth. The bacterium showed a significant response to cultivation in simulated microgravity at the transcriptomic, proteomic and metabolic levels. In simulated microgravity conditions three -acyl--homoserine lactones (C10-HSL, C12-HSL and 3-OH-C14-HSL) were detected in concentrations that were twice those detected under normal gravity, while no differences in cell density was detected. In addition, cultivated in modelled microgravity showed higher pigmentation than the normal gravity control, without change in culture oxygenation. When compared to randomized microgravity cultivation using a random positioning machine, significant overlap for the top differentially expressed genes and proteins was observed. Cultivation in this new artificial environment of simulated microgravity showed new properties of this well-known bacterium, including its first, to our knowledge, complete quorum-sensing-related -acylhomoserine lactone profile.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.066415-0
2013-12-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/159/12/2456.html?itemId=/content/journal/micro/10.1099/mic.0.066415-0&mimeType=html&fmt=ahah

References

  1. Anderson B. N., Ding A. M., Nilsson L. M., Kusuma K., Tchesnokova V., Vogel V., Sokurenko E. V., Thomas W. E. ( 2007). Weak rolling adhesion enhances bacterial surface colonization. J Bacteriol 189:1794–1802 [View Article][PubMed]
    [Google Scholar]
  2. Barjaktarović Z., Schütz W., Madlung J., Fladerer C., Nordheim A., Hampp R. ( 2009). Changes in the effective gravitational field strength affect the state of phosphorylation of stress-related proteins in callus cultures of Arabidopsis thaliana . J Exp Bot 60:779–789 [View Article][PubMed]
    [Google Scholar]
  3. Baysse C., Cullinane M., Dénervaud V., Burrowes E., Dow J. M., Morrissey J. P., Tam L., Trevors J. T., O’Gara F. ( 2005). Modulation of quorum sensing in Pseudomonas aeruginosa through alteration of membrane properties. Microbiology 151:2529–2542 [View Article][PubMed]
    [Google Scholar]
  4. Beuls E., Van Houdt R., Leys N., Dijkstra C., Larkin O., Mahillon J. ( 2009). Bacillus thuringiensis conjugation in simulated microgravity. Astrobiology 9:797–805 [View Article][PubMed]
    [Google Scholar]
  5. Boedicker J. Q., Vincent M. E., Ismagilov R. F. ( 2009). Microfluidic confinement of single cells of bacteria in small volumes initiates high-density behavior of quorum sensing and growth and reveals its variability. Angew Chem Int Ed Engl 48:5908–5911 [View Article][PubMed]
    [Google Scholar]
  6. Burton E. O., Read H. W., Pellitteri M. C., Hickey W. J. ( 2005). Identification of acyl-homoserine lactone signal molecules produced by Nitrosomonas europaea strain Schmidt. Appl Environ Microbiol 71:4906–4909 [View Article][PubMed]
    [Google Scholar]
  7. Carnes E. C., Lopez D. M., Donegan N. P., Cheung A., Gresham H., Timmins G. S., Brinker C. J. ( 2010). Confinement-induced quorum sensing of individual Staphylococcus aureus bacteria. Nat Chem Biol 6:41–45 [View Article][PubMed]
    [Google Scholar]
  8. Case R. J., Labbate M., Kjelleberg S. ( 2008). AHL-driven quorum-sensing circuits: their frequency and function among the Proteobacteria . ISME J 2:345–349 [View Article][PubMed]
    [Google Scholar]
  9. Connell J. L., Wessel A. K., Parsek M. R., Ellington A. D., Whiteley M., Shear J. B. ( 2010). Probing prokaryotic social behaviors with bacterial “lobster traps”. MBio 1:e00202-10 [View Article][PubMed]
    [Google Scholar]
  10. Crabbé A., De Boever P., Van Houdt R., Moors H., Mergeay M., Cornelis P. ( 2008). Use of the rotating wall vessel technology to study the effect of shear stress on growth behaviour of Pseudomonas aeruginosa PA01. Environ Microbiol 10:2098–2110 [View Article][PubMed]
    [Google Scholar]
  11. Crabbé A., Pycke B., Van Houdt R., Monsieurs P., Nickerson C., Leys N., Cornelis P. ( 2010). Response of Pseudomonas aeruginosa PAO1 to low shear modelled microgravity involves AlgU regulation. Environ Microbiol 12:1545–1564[PubMed]
    [Google Scholar]
  12. Fast W., Tipton P. A. ( 2012). The enzymes of bacterial census and censorship. Trends Biochem Sci 37:7–14 [View Article][PubMed]
    [Google Scholar]
  13. Favier-Teodorescu L. ( 2004). Etude cinétique et stoechiométrique de la croissance de Rhodospirillum rubrum en photobioréacteur. Laboratoire de génie chimique et biochimique365 PhD thesis, Université Blaise Pascal; Aubière, France:
    [Google Scholar]
  14. Fuqua C., Greenberg E. P. ( 2002). Listening in on bacteria: acyl-homoserine lactone signalling. Nat Rev Mol Cell Biol 3:685–695 [View Article][PubMed]
    [Google Scholar]
  15. Ghosh R., Hardmeyer A., Thoenen I., Bachofen R. ( 1994). Optimization of the Sistrom culture medium for large-scale batch cultivation of Rhodospirillum rubrum under semiaerobic conditions with maximal yield of photosynthetic membranes. Appl Environ Microbiol 60:1698–1700[PubMed]
    [Google Scholar]
  16. Hammond T. G., Hammond J. M. ( 2001). Optimized suspension culture: the rotating-wall vessel. Am J Physiol Renal Physiol 281:F12–F25[PubMed]
    [Google Scholar]
  17. Hammond T. G., Benes E., O’Reilly K. C., Wolf D. A., Linnehan R. M., Taher A., Kaysen J. H., Allen P. L., Goodwin T. J. ( 2000). Mechanical culture conditions effect gene expression: gravity-induced changes on the space shuttle. Physiol Genomics 3:163–173[PubMed]
    [Google Scholar]
  18. Hendrickx L., De Wever H., Hermans V., Mastroleo F., Morin N., Wilmotte A., Janssen P., Mergeay M. ( 2006). Microbial ecology of the closed artificial ecosystem MELiSSA (Micro-Ecological Life Support System Alternative): reinventing and compartmentalizing the Earth’s food and oxygen regeneration system for long-haul space exploration missions. Res Microbiol 157:77–86 [View Article][PubMed]
    [Google Scholar]
  19. Hense B. A., Kuttler C., Müller J., Rothballer M., Hartmann A., Kreft J. U. ( 2007). Does efficiency sensing unify diffusion and quorum sensing. Nat Rev Microbiol 5:230–239 [View Article][PubMed]
    [Google Scholar]
  20. Horswill A. R., Stoodley P., Stewart P. S., Parsek M. R. ( 2007). The effect of the chemical, biological, and physical environment on quorum sensing in structured microbial communities. Anal Bioanal Chem 387:371–380 [View Article][PubMed]
    [Google Scholar]
  21. Hoson T., Kamisaka S., Masuda Y., Yamashita M., Buchen B. ( 1997). Evaluation of the three-dimensional clinostat as a simulator of weightlessness. Planta 203:Suppl.S187–S197 [View Article][PubMed]
    [Google Scholar]
  22. Hwang W., Lee K. E., Lee J. K., Park B. C., Kim K. S. ( 2008). Genes of Rhodobacter sphaeroides 2.4.1 regulated by innate quorum-sensing signal, 7,8-cis-N-(tetradecenoyl) homoserine lactone. J Microbiol Biotechnol 18:219–227[PubMed]
    [Google Scholar]
  23. Klaus D. M., Todd P., Schatz A. ( 1998). Functional weightlessness during clinorotation of cell suspensions. Adv Space Res 21:1315–1318 [View Article][PubMed]
    [Google Scholar]
  24. Kwon O., Devarakonda S. B., Sankovic J. M., Banerjee R. K. ( 2008). Oxygen transport and consumption by suspended cells in microgravity: a multiphase analysis. Biotechnol Bioeng 99:99–107 [CrossRef]
    [Google Scholar]
  25. Leroy B., Rosier C., Erculisse V., Leys N., Mergeay M., Wattiez R. ( 2010). Differential proteomic analysis using isotope-coded protein-labeling strategies: comparison, improvements and application to simulated microgravity effect on Cupriavidus metallidurans CH34. Proteomics 10:2281–2291 [View Article][PubMed]
    [Google Scholar]
  26. Leys N., Baatout S., Rosier C., Dams A., s’Heeren C., Wattiez R., Mergeay M. ( 2009). The response of Cupriavidus metallidurans CH34 to spaceflight in the international space station. Antonie van Leeuwenhoek 96:227–245 [View Article][PubMed]
    [Google Scholar]
  27. Manti L. ( 2006). Does reduced gravity alter cellular response to ionizing radiation. Radiat Environ Biophys 45:1–8 [View Article][PubMed]
    [Google Scholar]
  28. Marco R., Laván D. A., van Loon J. J., Leandro L. J., Larkin O. J., Dijkstra C., Anthony P., Villa A., Davey M. R. & other authors ( 2007). Drosophila melanogaster, a model system for comparative studies on the responses to real and simulated microgravity. J Gravit Physiol 14:125–126[PubMed]
    [Google Scholar]
  29. Mastroleo F., Leroy B., Van Houdt R., s’Heeren C., Mergeay M., Hendrickx L., Wattiez R. ( 2009a). Shotgun proteome analysis of Rhodospirillum rubrum S1H: integrating data from gel-free and gel-based peptides fractionation methods. J Proteome Res 8:2530–2541 [View Article][PubMed]
    [Google Scholar]
  30. Mastroleo F., Van Houdt R., Leroy B., Benotmane M. A., Janssen A., Mergeay M., Vanhavere F., Hendrickx L., Wattiez R., Leys N. ( 2009b). Experimental design and environmental parameters affect Rhodospirillum rubrum S1H response to space flight. ISME J 3:1402–1419 [View Article][PubMed]
    [Google Scholar]
  31. Mauclaire L., Egli M. ( 2010). Effect of simulated microgravity on growth and production of exopolymeric substances of Micrococcus luteus space and earth isolates. FEMS Immunol Med Microbiol 59:350–356[PubMed]
    [Google Scholar]
  32. Meloni M. A., Galleri G., Pippia P., Cogoli-Greuter M. ( 2006). Cytoskeleton changes and impaired motility of monocytes at modelled low gravity. Protoplasma 229:243–249 [View Article][PubMed]
    [Google Scholar]
  33. Mergeay M., Verstraete W., Dubertret G., Lefort-Tran M., Chipaux C., Binot R. A. ( 1988). ‘MELiSSA’ – A micro-organisms-based model for ‘CELSS’ development. Proceedings of the 3rd European Symposium on Space Thermal Control & Life Support Systems, Nordwijk, The Netherlands, ESA Special Publication no. 288 65–68 Guyenne T. D., Hunt J. European Space Agency;
    [Google Scholar]
  34. Nauman E. A., Ott C. M., Sander E., Tucker D. L., Pierson D., Wilson J. W., Nickerson C. A. ( 2007). Novel quantitative biosystem for modeling physiological fluid shear stress on cells. Appl Environ Microbiol 73:699–705 [View Article][PubMed]
    [Google Scholar]
  35. Nickerson C. A., Ott C. M., Mister S. J., Morrow B. J., Burns-Keliher L., Pierson D. L. ( 2000). Microgravity as a novel environmental signal affecting Salmonella enterica serovar Typhimurium virulence. Infect Immun 68:3147–3152 [View Article][PubMed]
    [Google Scholar]
  36. Nickerson C. A., Ott C. M., Wilson J. W., Ramamurthy R., Pierson D. L. ( 2004). Microbial responses to microgravity and other low-shear environments. Microbiol Mol Biol Rev 68:345–361 [View Article][PubMed]
    [Google Scholar]
  37. Niederman R. A. ( 2013). Membrane development in purple photosynthetic bacteria in response to alterations in light intensity and oxygen tension. Photosynth Res [View Article][PubMed]
    [Google Scholar]
  38. Oguz M. T., Robinson K. G., Layton A. C., Sayler G. S. ( 2006). Volatile fatty acid impacts on nitrite oxidation and carbon dioxide fixation in activated sludge. Water Res 40:665–674 [View Article][PubMed]
    [Google Scholar]
  39. Ortori C. A., Atkinson S., Chhabra S. R., Cámara M., Williams P., Barrett D. A. ( 2007). Comprehensive profiling of N-acylhomoserine lactones produced by Yersinia pseudotuberculosis using liquid chromatography coupled to hybrid quadrupole-linear ion trap mass spectrometry. Anal Bioanal Chem 387:497–511 [View Article][PubMed]
    [Google Scholar]
  40. Pardo S. J., Patel M. J., Sykes M. C., Platt M. O., Boyd N. L., Sorescu G. P., Xu M., van Loon J. J., Wang M. D., Jo H. ( 2005). Simulated microgravity using the Random Positioning Machine inhibits differentiation and alters gene expression profiles of 2T3 preosteoblasts. Am J Physiol Cell Physiol 288:C1211–C1221 [View Article][PubMed]
    [Google Scholar]
  41. Puskas A., Greenberg E. P., Kaplan S., Schaefer A. L. ( 1997). A quorum-sensing system in the free-living photosynthetic bacterium Rhodobacter sphaeroides . J Bacteriol 179:7530–7537[PubMed]
    [Google Scholar]
  42. Pycke B. ( 2009). The fate and effects of micropollutants in a biological life support system. Faculteit Biol-ingenieurswetenschappen187 PhD thesis, Universiteit Gent; Belgium:
    [Google Scholar]
  43. Reading N. C., Sperandio V. ( 2006). Quorum sensing: the many languages of bacteria. FEMS Microbiol Lett 254:1–11 [View Article][PubMed]
    [Google Scholar]
  44. Shaw P. D., Ping G., Daly S. L., Cha C., Cronan J. E. Jr, Rinehart K. L., Farrand S. K. ( 1997). Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. Proc Natl Acad Sci U S A 94:6036–6041 [View Article][PubMed]
    [Google Scholar]
  45. Shiner E. K., Rumbaugh K. P., Williams S. C. ( 2005). Inter-kingdom signaling: deciphering the language of acyl homoserine lactones. FEMS Microbiol Rev 29:935–947 [View Article][PubMed]
    [Google Scholar]
  46. Sistrom W. R. ( 1960). A requirement for sodium in the growth of Rhodopseudomonas sphaeroides . J Gen Microbiol 22:778–785 [View Article][PubMed]
    [Google Scholar]
  47. Sonnenfeld G. ( 2005). The immune system in space, including Earth-based benefits of space-based research. Curr Pharm Biotechnol 6:343–349 [View Article][PubMed]
    [Google Scholar]
  48. Tsao Y.-M. D., Boyd E., Wolf D. A., Spaulding G. ( 1994). Fluid dynamics within a rotating bioreactor in space and Earth environments. J Spacecr Rockets 31:937–943 [View Article]
    [Google Scholar]
  49. Tucker D. L., Ott C. M., Huff S., Fofanov Y., Pierson D. L., Willson R. C., Fox G. E. ( 2007). Characterization of Escherichia coli MG1655 grown in a low-shear modeled microgravity environment. BMC Microbiol 7:15 [View Article][PubMed]
    [Google Scholar]
  50. Vallenet D., Labarre L., Rouy Z., Barbe V., Bocs S., Cruveiller S., Lajus A., Pascal G., Scarpelli C., Médigue C. ( 2006). MaGe: a microbial genome annotation system supported by synteny results. Nucleic Acids Res 34:53–65 [View Article][PubMed]
    [Google Scholar]
  51. Vukanti R., Mintz E., Leff L. ( 2008). Changes in gene expression of E. coli under conditions of modeled reduced gravity. Microgravity Sci Technol 20:41–57 [View Article]
    [Google Scholar]
  52. Walther I., Pippia P., Meloni M. A., Turrini F., Mannu F., Cogoli A. ( 1998). Simulated microgravity inhibits the genetic expression of interleukin-2 and its receptor in mitogen-activated T lymphocytes. FEBS Lett 436:115–118 [View Article][PubMed]
    [Google Scholar]
  53. Wang Y., Mulligan C., Denyer G., Delom F., Dagna-Bricarelli F., Tybulewicz V. L., Fisher E. M., Griffiths W. J., Nizetic D., Groet J. ( 2009). Quantitative proteomics characterization of a mouse embryonic stem cell model of Down syndrome. Mol Cell Proteomics 8:585–595 [View Article][PubMed]
    [Google Scholar]
  54. Watson W. T., Minogue T. D., Val D. L., von Bodman S. B., Churchill M. E. ( 2002). Structural basis and specificity of acyl-homoserine lactone signal production in bacterial quorum sensing. Mol Cell 9:685–694 [View Article][PubMed]
    [Google Scholar]
  55. Wilson J. W., Ott C. M., Höner zu Bentrup K., Ramamurthy R., Quick L., Porwollik S., Cheng P., McClelland M., Tsaprailis G. & other authors ( 2007). Space flight alters bacterial gene expression and virulence and reveals a role for global regulator Hfq. Proc Natl Acad Sci U S A 104:16299–16304 [View Article][PubMed]
    [Google Scholar]
  56. Wilson J. W., Ott C. M., Quick L., Davis R., Höner zu Bentrup K., Crabbé A., Richter E., Sarker S., Barrila J. & other authors ( 2008). Media ion composition controls regulatory and virulence response of Salmonella in spaceflight. PLoS ONE 3:e3923 [View Article][PubMed]
    [Google Scholar]
  57. Yates E. A., Philipp B., Buckley C., Atkinson S., Chhabra S. R., Sockett R. E., Goldner M., Dessaux Y., Cámara M. & other authors ( 2002). N-acylhomoserine lactones undergo lactonolysis in a pH-, temperature-, and acyl chain length-dependent manner during growth of Yersinia pseudotuberculosis and Pseudomonas aeruginosa . Infect Immun 70:5635–5646 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.066415-0
Loading
/content/journal/micro/10.1099/mic.0.066415-0
Loading

Data & Media loading...

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