Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-19T12:32:08.845Z Has data issue: false hasContentIssue false
  • English
  • Français

Role of Hfq in an animal–microbe symbiosis under simulated microgravity conditions

Published online by Cambridge University Press:  25 October 2013

Kyle C. Grant ,
Christina L.M. Khodadad  and
Jamie S. Foster
Kyle C. Grant
Affiliation:
Department of Microbiology and Cell Science, University of Florida, Space Life Science Laboratory at Exploration Park, Merritt Island, FL 32953, USA
Christina L.M. Khodadad
Affiliation:
Department of Microbiology and Cell Science, University of Florida, Space Life Science Laboratory at Exploration Park, Merritt Island, FL 32953, USA
Jamie S. Foster*
Affiliation:
Department of Microbiology and Cell Science, University of Florida, Space Life Science Laboratory at Exploration Park, Merritt Island, FL 32953, USA
*
e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Microgravity has a profound impact on the physiology of pathogenic microbes; however, its effects on mutualistic microbes are relatively unknown. To examine the effects of microgravity on those beneficial microbes that associate with animal tissues, we used the symbiosis between the bobtail squid Euprymna scolopes and a motile, luminescent bacterium, Vibrio fischeri as a model system. Specifically, we examined the role of Hfq, an RNA-binding protein known to be an important global regulator under space flight conditions, in the squid–vibrio symbiosis under simulated microgravity. To mimic a reduced gravity environment, the symbiotic partners were co-incubated in high-aspect-ratio rotating wall vessel bioreactors and examined at various stages of development. Results indicated that under simulated microgravity, hfq expression was down-regulated in V. fischeri. A mutant strain defective in hfq showed no colonization phenotype, indicating that Hfq was not required to initiate the symbiosis with the host squid. However, the hfq mutant showed attenuated levels of apoptotic cell death, a key symbiosis phenotype, within the host light organ suggesting that Hfq does contribute to normal light organ morphogenesis. Results also indicated that simulated microgravity conditions accelerated the onset of cell death in wild-type cells but not in the hfq mutant strains. These data suggest that Hfq plays an important role in the mutualism between V. fischeri and its animal host and that its expression can be negatively impacted by simulated microgravity conditions.

Keywords

Euprymna scolopesHfqmicrogravitysymbiosisVibrio fischeri
Type
Research Article
Information
International Journal of Astrobiology , Volume 13 , Issue 1 , January 2014 , pp. 53 - 61
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Altura, M.A., Heath-Heckman, E.A., Gillette, A., Kremer, N., Krachler, A.M., Brennan, C., Ruby, E.G., Orth, K. & McFall-Ngai, M.J. (2013). Environ. Microbiol. DOI: 10.1111/1462-2920.12179.Google Scholar
Arunasri, K., Adil, M., Venu Charan, K., Suvro, C., Himabindu Reddy, S. & Shivaji, S. (2013). PLoS ONE 8(3), e57860.Google Scholar
Barra-Bily, L., Pandey, S.P., Trautwetter, A., Blanco, C. & Walker, G.C. (2010). J. Bacteriol. 192(6), 1710–1718.Google Scholar
Benoit, M. & Klaus, D.M. (2007). Adv. Space Res. 39, 1225–1232.Google Scholar
Boettcher, K.J. & Ruby, E.G. (1990). J. Bacteriol. 172(7), 3701–3706.Google Scholar
Boettcher, K.J., Ruby, E.G. & McFall-Ngai, M.J. (1996). J Comp. Physiol. A 179, 65–73.CrossRefGoogle Scholar
Bohn, C., Rigoulay, C. & Bouloc, P. (2007). BMC Microbiol. 7, 10.Google Scholar
Chao, Y. & Vogel, J. (2010). Curr. Opin. Microbiol. 13(1), 24–33.Google Scholar
Chopra, V., Fadl, A.A., Sha, J., Chopra, S., Galindo, C.L. & Chopra, A.K. (2006). J. Toxicol. Environ. Health A 69(14), 1345–1370.Google Scholar
Christiansen, J.K., Larsen, M.H., Ingmer, H., Sogaard-Andersen, L. & Kallipolitis, B.H. (2004). J. Bacteriol. 186(11), 3355–3362.Google Scholar
Ciferri, O., Tiboni, O., Di Pasquale, G., Orlandoni, A.M. & Marchesi, M.L. (1986). Naturwissenschaften 73(7), 418–421.Google Scholar
Crabbé, A. et al. (2011). Appl. Environ. Microbiol. 77(4), 1221–1230.Google Scholar
Crucian, B.E., Stowe, R.P., Pierson, D.L. & Sams, C.F. (2008). Aviat. Space Environ. Med. 79(9), 835–843.CrossRefGoogle Scholar
Dethlefsen, L., McFall-Ngai, M. & Relman, D.A. (2007). Nature 449(7164), 811–818.Google Scholar
Ding, Y., Davis, B.M. & Waldor, M.K. (2004). Mol. Microbiol. 53(1), 345–354.Google Scholar
Doino, J.A. & McFall-Ngai, M. (1995). Biol. Bull. 189, 347–355.Google Scholar
Fierer, N., Jackson, J.A., Vilgalys, R. & Jackson, R.B. (2005). Appl. Environ. Microbiol. 71(7), 4117–4120.Google Scholar
Foster, J.S. & McFall-Ngai, M.J. (1998). Dev. Genes Evol. 208(6), 295–303.Google Scholar
Foster, J.S., Apicella, M.A. & McFall-Ngai, M.J. (2000). Dev. Biol. 226(2), 242–254.CrossRefGoogle Scholar
Foster, J.S., Kerney, K.R., Parrish, M.L., Khodadad, C.L.M. & Ahrendt, S.R. (2011). Grav. Space Biol. 25, 44–47.Google Scholar
Foster, J.S., Khodadad, C.L., Ahrendt, S.R. & Parrish, M.L. (2013). Sci. Rep. 3, 1340.Google Scholar
Gao, M., Barnett, M.J., Long, S.R. & Teplitski, M. (2010). Mol. Plant Microbe Interact 23(4), 355–365.Google Scholar
Geng, J. et al. (2009). PLoS ONE 4(7), e6213.Google Scholar
Graf, J. & Ruby, E.G. (1998). Proc. Natl. Acad. Sci. USA 95(4), 1818–1822.Google Scholar
Guisbert, E., Rhodius, V.A., Ahuja, N., Witkin, E. & Gross, C.A. (2007). J. Bacteriol. 189(5), 1963–1973.CrossRefGoogle Scholar
Hammer, B.K. & Bassler, B.L. (2007). Proc. Natl. Acad. Sci. USA 104(27), 11145–11149.Google Scholar
Horneck, G., Klaus, D.M. & Mancinelli, R.L. (2010). Microbiol. Mol. Biol. Rev. 74(1), 121–156.Google Scholar
Human Microbiome Consortium (2012). Nature 486(7402), 207–214.Google Scholar
Infanger, M. et al. (2006). Cell Tissue Res. 324(2), 267–277.Google Scholar
Kim, W. et al. (2013). PLoS ONE 8(4), e62437.CrossRefGoogle Scholar
Klaus, D., Simske, S., Todd, P. & Stodieck, L. (1997). Microbiology 143(Pt 2), 449–455.Google Scholar
Koropatnick, T.A., Engle, J.T., Apicella, M.A., Stabb, E.V., Goldman, W.E. & McFall-Ngai, M.J. (2004). Science 306(5699), 1186–1188.Google Scholar
Lee, K.H. & Ruby, E.G. (1994). Appl. Environ. Microbiol. 60(5), 1565–1571.Google Scholar
Lupp, C. & Ruby, E.G. (2005). J. Bacteriol. 187(11), 3620–3629.Google Scholar
Lynch, S.V. & Matin, A. (2005). Biologist 52(2), 80–92.Google Scholar
Mattoni, R. (1968). Bioscience 18, 602–608.Google Scholar
Mauclaire, L. & Egli, M. (2010). FEMS Immunol. Med. Microbiol. 59(3), 350–356.Google Scholar
Mazmanian, S.K., Liu, C.H., Tzianabos, A.O. & Kasper, D.L. (2005). Cell 122(1), 107–118.CrossRefGoogle Scholar
McFall-Ngai, M.J. & Ruby, E.G. (1991). Science 254(5037), 1491–1494.Google Scholar
McFall-Ngai, M., Nyholm, S.V. & Castillo, M.G. (2010). Semin. Immunol. 22(1), 48–53.Google Scholar
Montgomery, M.K. & McFall-Ngai, M. (1994). Development 120(7), 1719–1729.Google Scholar
Nickerson, C.A., Ott, C.M., Mister, S.J., Morrow, B.J., Burns-Keliher, L. & Pierson, D.L. (2000). Infect. Immun. 68(6), 3147–3152.Google Scholar
Nickerson, C.A., Ott, C.M., Wilson, J.W., Ramamurthy, R., LeBlanc, C.L., Honer zu Bentrup, K., Hammond, T. & Pierson, D.L. (2003). J. Microbiol. Methods 54(1), 1–11.Google Scholar
Nickerson, C.A., Ott, C.M., Wilson, J.W., Ramamurthy, R. & Pierson, D.L. (2004). Microbiol. Mol. Biol. Rev. 68(2), 345–361.Google Scholar
Nickerson, C.A., Richter, E.G. & Ott, C.M. (2007). J. Neuroimmune Pharmacol. 2(1), 26–31.Google Scholar
Nyholm, S.V., Stabb, E.V., Ruby, E.G. & McFall-Ngai, M.J. (2000). Proc. Natl. Acad. Sci. USA 97(18), 10231–10235.Google Scholar
Pacello, F., Rotilio, G. & Battistoni, A. (2012). Open Microbiol. J. 6, 53–64.CrossRefGoogle Scholar
Rakoff-Nahoum, S., Paglino, J., Eslami-Varzaneh, F., Edberg, S. & Medzhitov, R. (2004). Cell 118(2), 229–241.Google Scholar
Robertson, G.T. & Roop, R.M. Jr. (1999). Mol. Microbiol. 34(4), 690–700.Google Scholar
Rosenzweig, J.A. & Chopra, A.K. (2012). Front. Cell Infect. Microbiol. 2, 107.CrossRefGoogle Scholar
Ruby, E.G. & Asato, L.M. (1993). Arch. Microbiol. 159(2), 160–167.CrossRefGoogle Scholar
Ruby, E.G. et al. (2005). Proc. Natl. Acad. Sci. USA 102(8), 3004–3009.CrossRefGoogle Scholar
Sarker, S., Ott, C.M., Barrila, J. & Nickerson, C.A. (2010). Grav. Space Biol. 23, 75–78.Google Scholar
Schwarz, R.P., Goodwin, T.J. & Wolf, D.A. (1992). J. Tiss. Cult. Meth. 14, 51–58.Google Scholar
Shakhnovich, E.A., Davis, B.M. & Waldor, M.K. (2009). Mol. Microbiol. 74(2), 347–363.Google Scholar
Sittka, A., Pfeiffer, V., Tedin, K. & Vogel, J. (2007). Mol. Microbiol. 63(1), 193–217.Google Scholar
Sittka, A., Lucchini, S., Papenfort, K., Sharma, C.M., Rolle, K., Binnewies, T.T., Hinton, J.C. & Vogel, J. (2008). PLoS Genet. 4(8), e1000163.Google Scholar
Sonnenfeld, G., Foster, M., Morton, D., Bailliard, F., Fowler, N.A., Hakenewerth, A.M., Bates, R. & Miller, E.S. Jr. (1998). J. Appl. Physiol. 85(4), 1429–1433.Google Scholar
Sonnleitner, E., Hagens, S., Rosenau, F., Wilhelm, S., Habel, A., Jager, K.E. & Blasi, U. (2003). Microb. Pathog. 35(5), 217–228.Google Scholar
Sonnleitner, E., Schuster, M., Sorger-Domenigg, T., Greenberg, E.P. & Blasi, U. (2006). Mol. Microbiol. 59(5), 1542–1558.Google Scholar
Stabb, E.V. & Visick, K.L. (2013). A bioluminescent light organ symbiont of the bobtail squid Euprymna scolopes . In The Prokaryotes, 4th edn, ed. Rosenberg, E., Delong, E.F., Stackebrandt, E., Lory, S. & Thompson, F., Springer-Verlag, Berlin-Heidelberg, pp. 497–532.Google Scholar
Taylor, G.R. (1974). Annu. Rev. Microbiol. 28, 121–137.Google Scholar
Tixador, R., Richoilley, G., Gasset, G., Templier, J., Bes, J.C., Moatti, N. & Lapchine, L. (1985). Aviat. Space Environ. Med. 56(8), 748–751.Google Scholar
Torres-Quesada, O., Oruezabal, R.I., Peregrina, A., Jofre, E., Lloret, J., Rivilla, R., Toro, N. & Jimenez-Zurdo, J.I. (2010). BMC Microbiol. 10, 71.Google Scholar
Valentin-Hansen, P., Eriksen, M. & Udesen, C. (2004). Mol. Microbiol. 51(6), 1525–1533.Google Scholar
Vukanti, R., Model, M.A. & Leff, L.G. (2012). BMC Microbiol. 12, 4.Google Scholar
Wilson, J.W., Ramamurthy, R., Porwollik, S., McClelland, M., Hammond, T., Allen, P., Ott, C.M., Pierson, D.L. & Nickerson, C.A. (2002). Proc. Natl. Acad. Sci. USA 99(21), 13807–13812.Google Scholar
Wilson, J.W. et al. (2007). Proc. Natl. Acad. Sci. USA 104(41), 16299–16304.Google Scholar
Wilson, J.W. et al. (2008). PLoS ONE 3(12), e3923.Google Scholar
Wolf, D.A. & Schwarz, R.P. (1991). NASA Tech. Pap. 3143, 1–12.Google Scholar
Zayzafoon, M., Gathings, W.E. & McDonald, J.M. (2004). Endocrinology 145(5), 2421–2432.Google Scholar
Zayzafoon, M., Meyers, V.E. & McDonald, J.M. (2005). Immunol. Rev. 208, 267–280.Google Scholar