Host/microbe interactions revealed through "omics" in the symbiosis between the Hawaiian bobtail squid euprymna scolopes and the bioluminescent bacterium Vibrio fischeri

Biological Bulletin

Volumn 223, Issue 1, 2012, Pages 103-111

  Rader, Bethany A ^a   Nyholm, Spencer V ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM; BIOLUMINESCENCE; CEPHALOPOD; COLONIZATION; GENOME; HOST-SYMBIONT INTERACTION; IMMUNE SYSTEM; SYMBIOSIS;

BACTERIA (MICROORGANISMS); EUPRYMNA SCOLOPES; SEPIOLIDAE; VIBRIO FISCHERI;

EID: 84866402357     PISSN: 00063185     EISSN: None     Source Type: Journal    
DOI: 10.1086/BBLv223n1p103     Document Type: Article

References (68)

1. Altura, M. A., E. Stabb, W. Goldman, M. Apicella, and M. J. McFall-Ngai. 2011. Attenuation of host NO production by MAMPs potentiates development of the host in the squid-vibrio symbiosis. Cell. Microbiol. 13: 527-537.
2. Antunes, L. C., A. L. Schaefer, R. B. Ferreira, N. Qin, A. M. Stevens, E. G. Ruby, and E. P. Greenberg. 2007. Transcriptome analysis of the Vibrio fischeri LuxR-LuxI regulon. J. Bacteriol. 189: 8387-8391.
3. Boettcher, K. J., E. G. Ruby, and M. J. McFall-Ngai. 1996. Bioluminescence in the symbiotic squid Euprymna scolopes is controlled by a daily biological rhythm. J. Comp. Physiol. A 1: 65-73.
4. Bose, J. L., C. S. Rosenberg, and E. V. Stabb. 2008. Effects of luxCDABEG induction in Vibrio fischeri: enhancement of symbiotic colonization and conditional attenuation of growth in culture. Arch. Microbiol. 190: 169-183.
5. Callahan, S. M., and P. V. Dunlap. 2000. LuxR-and acyl-homoserinelactone-controlled non-lux genes define a quorum-sensing regulon in Vibrio fischeri. J. Bacteriol. 182: 2811-2822.
6. Castillo, M. G., M. S. Goodson, and M. J. McFall-Ngai. 2009. Identification and molecular characterization of a complement-C3 molecule in a lophotrochozoan, the Hawaiian bobtail squid Euprymna scolopes. Dev. Comp. Immunol. 33: 669-676.
7. Chun, C. K., E. Scheetz, M. de Fatima Bonaldo, B. Brown, A Clemens, W. J. Crookes-Goodson, K. Crouch, T. DeMartini, M. Eyestone, M. S. Goodson et al. 2006. An annotated cDNA library of juvenile Euprymna scolopes with and without colonization by the symbiont Vibrio fischeri. BMC Genomics 7: 154-164.
8. Chun, C. K., J. V. Troll, I. Koroleva, B. Brown, L. Manzella, E. Snir, H. Almabrazi, T. E. Scheetz, M. Bonaldo, T. L. Casavant, M. B. Soares, E. G. Ruby, and M. J. McFall-Ngai. 2008. Effects of colonization, luminescence and autoinducer on global host transcription in the developing squid-vibrio symbiosis. Proc. Natl. Acad. Sci. USA 105: 11323-11328.
9. Collins A. J., T. R. Schleicher, B. A. Rader, and S. V. Nyholm. 2012. Understanding the role of host hemocytes in a squid/Vibrio symbiosis using transcriptomics and proteomics. Front. Immunol. 3 (91).
10. Davidson, S. K., T. A. Koropatnick, R. Kossmehl, L. Sycuro, and M. J. McFall-Ngai. 2004. NO means 'yes' in the squid-vibrio symbiosis: nitric oxide (NO) during the initial stages of a beneficial association. Cell. Microbiol. 6: 1139-1151.
11. Doino Lemus, J, and M. J. McFall-Ngai. 2000. Alterations in the proteome of the Euprymna scolopes light organ in response to symbiotic Vibrio fischeri. Appl. Environ. Microbiol. 66: 4091-4097.
12. Foster, J. S., M. A. Apicella and M. J. McFall-Ngai. 2000. Vibrio fischeri lipopolysaccharide induces developmental apoptosis, but not complete morphogenesis, of the Euprymna scolopes symbiotic light organ. Dev. Biol. 226: 242-254.
13. Gerardo, N. M., B. Altincicek, C. Anselme, H. Atamian, S. M. Barribeau, M. de Vos, E. J. Duncan, J. D. Evans, T. Gabaldón, M. Ghanim et al. 2010. Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biol. 11: R21.
14. Goodson, M. S., M. Kojadinovic, J. V. Troll, T. E. Scheetz, T. L. Cazavant, M. B. Soares, and M. J. McFall-Ngai. 2005. Identifying components of the NF-_B pathway in the beneficial Euprymna scolopes-Vibrio fischeri light organ symbiosis. Appl. Environ. Microbiol. 71: 6934-6946.
15. Grant, P., Y. Zheng, and H. C. Pant. 2006. Squid (Loligo pealei) giant fiber system: a model for studying neurodegeneration and dementia? Biol. Bull. 210: 318-333.
16. Gregory, T. R. 2001. Coincidence, coevolution or causation? DNA content, cell size, and the C-value enigma. Biol. Rev. 76: 65-101.
17. Gregory, T. R. 2012. Animal Genome Size Database. [Online]. Available: http://www.genomesize.com [2012, May 08].
18. Guerrero-Ferreira R. C., and M. K. Nishiguchi. 2010. Differential gene expression in bacterial symbionts from loliginid squids demonstrates variation between mutualistic and environmental niches. Environ. Microbiol. Rep. 2: 514-523.
19. Gyllborg, M. C., J. W. Sahl, D. C. Cronin 3rd, D. A. Rasko, and M. J. Mandel. 2012. Draft genome sequence of Vibrio fischeri SR5, a strain isolated from the light organ of the Mediterranean squid Sepiola robusta. J. Bacteriol. 194: 1639.
20. Heath-Heckman, E. A., and M. J. McFall-Ngai. 2011. The occurrence of chitin in the hemocytes of invertebrates. Zoology 114: 191-198.
21. Hussa, E. A., C. L. Darnell, and K. L. Visick. 2008. RscS functions upstream of SypG to control the syp locus and biofilm formation in Vibrio fischeri. J. Bacteriol. 190: 4576-4583.
22. Jones, B. W., and M. K. Nishiguchi. 2004. Counterillumination in the bobtail squid, Euprymna scolopes (Mollusca: Cephalopoda). Mar. Biol. 144: 1151-1155.
23. Jones, B. W., and M. K. Nishiguchi. 2006. Differentially expressed genes reveal adaptations between free-living and symbiotic niches of Vibrio fischeri in a fully established mutualism. Can. J. Microbiol. 52: 1218-1227.
24. Koropatnick, T. A., J. T. Engle, M. A. Apicella, E. V. Stabb, W. E. Goldman, and M. J. McFall-Ngai. 2004. Microbial factor-mediated development in a host-bacterial mutualism. Science 306: 1186-1188.
25. Koropatnick, T. A., J. R. Kimbell, and M. J. McFall-Ngai. 2007. Responses of host hemocytes during the initiation of the squid-vibrio symbiosis. Biol. Bull. 212: 29-39.
26. Krasity, B. C., J. V. Troll, J. P. Weiss, and M. J. McFall-Ngai. 2011. LBP/BPI proteins and their relatives: conservation over evolution and roles in mutualism. Biochem. Soc. Trans. 39: 1039-1044.
27. Lee, K. H., and E. G. Ruby. 1994. Effect of the squid host on the abundance and distribution of symbiotic Vibrio fischeri in nature. Appl. Environ. Microbiol. 60: 1565-1571.
28. Lee, P. N., M. J. McFall-Ngai, P. Callaerts, and H. Gert de Couet. 2009. The Hawaiian bobtail squid (Euprymna scolopes): a model to study the molecular basis of eukaryote-prokaryote mutualism and the development and evolution of morphological novelties in cephalopods. Cold Spring Harb. Protoc. 4: 1-9.
29. Leigh, E. G., Jr. 2010. The evolution of mutualism. J. Evol. Biol. 23: 2507-2528.
30. Lin, Y. P., S. P. McDonough, Y. Sharma, and Y. F. Chang. 2010. The terminal immunoglobulin-like repeats of LigA and LigB of Leptospira enhance their binding to gelatin binding domain of fibronectin and host cells. PLoS One 5(6): e11301.
31. Lupp, C., and E. G. Ruby. 2005. Vibrio fischeri uses two quorumsensing systems for the regulation of early and late colonization factors. J. Bacteriol. 187: 3620-3629.
32. Lupp, C., M. Urbanowski, E. P. Greenberg, and E. G. Ruby. 2003. The Vibrio fischeri quorum-sensing systems ain and lux sequentially induce luminescence gene expression and are important for persistence in the squid host. Mol. Microbiol. 50: 319-331.
33. MacDonald, S. J., G. H. Thomas, and A. E. Douglas. 2011. Genetic and metabolic determinants of nutritional phenotype in an insectbacterial symbiosis. Mol. Ecol. 20: 2073-2074.
34. Mandel, M. J. 2010. Models and approaches to dissect host-symbiont specificity. Trends Microbiol. 18: 504-511.
35. Mandel, M. J., E. V. Stabb, and E. G. Ruby. 2008. Comparative genomics-based investigation of resequencing targets in Vibrio fischeri: focus on point miscalls and artefactual expansions. BMC Genomics. 9: 138.
36. Mandel, M. J., M. S. Wollenberg, E. V. Stabb, K. L. Visick, and E. G. Ruby. 2009. A single regulatory gene is sufficient to alter bacterial host range. Nature 458: 215-218.
37. Mandel, M. J., A. L. Shaefer, C. A. Brennan, E. A. C. Heath-Heckman, C. R. DeLoney-Marino, M. J. McFall-Ngai, and E. G. Ruby. 2012. Squid-derived chitin oligosaccharides are a chemotactic signal during colonization by Vibrio fischeri. Appl. Environ. Microbiol. 78: 4620-4626.
38. Mathger, L. M., E. J. Denton, N. J. Marshall, and R. T. Hanlon. 2009. Mechanisms and behavioural functions of structural coloration in cephalopods. J. R. Soc. Interface 6 (Suppl 2): S149-163.
39. McFall-Ngai, M. J. 2002. Unseen forces: the influence of bacteria on animal development. Dev. Biol. 242: 1-14.
40. McFall-Ngai, M. J. 2008. Host-microbe symbiosis: the squid-Vibrio association-a naturally occurring, experimental model of animal/bacterial partnerships. Adv. Exp. Med. Biol. 635: 102-112.
41. McFall-Ngai, M. J., and E. G. Ruby. 1991. Symbiont recognition and subsequent morphogenesis as early events in an animal-bacterial mutualism. Science 254: 1491-1494.
42. McFall-Ngai, M., S. V. Nyholm, and M. G. Castillo. 2010. The role of the immune system in the initiation and persistence of the Euprymna scolopes-Vibrio fischeri symbiosis. Semin. Immunol. 22: 48-53.
43. McFall-Ngai, M., E. A. Heath-Heckman, A. A. Gillette, S. M. Peyer, and E. A. Harvie. 2012. The secret languages of coevolved symbioses: insights from the Euprymna scolopes-Vibrio fischeri symbiosis. Semin. Immunol. 24: 3-8.
44. Miyashiro, T., and E. G. Ruby. 2012. Shedding light on bioluminescence regulation in Vibrio fischeri. Mol. Microbiol. 84: 795-806.
45. Nishiguchi, M. K., E. G. Ruby, and M. J. McFall-Ngai. 1998. Competitive dominance during colonization is an indicator of coevolution in an animal-bacterial symbiosis. Appl. Environ. Microbiol. 64: 3209-3213.
46. Nyholm, S. V., and M. J. McFall-Ngai. 1998. Sampling the light-organ microenvironment of Euprymna scolopes: description of a population of host cells in association with the bacterial symbiont Vibrio fischeri. Biol. Bull. 195: 89-97.
47. Nyholm, S. V., and M. J. McFall-Ngai. 2003. Dominance of Vibrio fischeri in secreted mucus outside the light organ of Euprymna scolopes: the first site of symbiont specificity. Appl. Environ. Microbiol. 69: 3932-3937.
48. Nyholm, S. V., and M. J. McFall-Ngai. 2004. The winnowing: establishing the squid-Vibrio symbiosis. Nat. Rev. Microbiol. 2: 1186-1188.
49. Nyholm, S. V., J. J. Stewart, E. G. Ruby, and M. J. McFall-Ngai. 2009. Recognition between symbiotic Vibrio fischeri and the hemocytes of Euprymna scolopes. Environ. Microbiol. 11: 483-493.
50. Partridge, J. C. 2012. Sensory ecology: giant eyes for giant predators? Curr. Biol. 22: R268-270.
51. Rader, B. A., N. Kremer, M. A. Apicella, W. E. Goldman, and M. J. McFall-Ngai. 2012. Modulation of symbiont lipid A signaling by host alkaline phosphatases in the squid-vibrio symbiosis. MBio 3(3): e00093-12.
52. Rodhouse, P. G., and C. M. Nigmatullin, 1996. Role as consumers. Philos. Trans. R. Soc. Lond. B 351: 1003-1022.
53. Ruby, E. G. 1999. The Euprymna scolopes-Vibrio fischeri symbiosis: a biomedical model for the study of bacterial colonization of animal tissue. J. Mol. Microbiol. Biotechnol. 1: 13-21.
54. Ruby, E. G., M. Urbanowski, J. Campbell, A. Dunn, M. Faini, R. Gunsalus, P. Lostroh, C. Lupp, J. McCann, D. Millikan et al. 2005. Complete genome sequencing of Vibrio fischeri: a symbiotic bacterium with pathogenic congeners. Proc. Natl. Acad. Sci. USA 102: 3004-3009.
55. Schleicher, T. R., and S. V. Nyholm. 2011. Characterizing the host and symbiont proteomes in the association between the Bobtail squid Euprymna scolopes, and the bacterium, Vibrio fischeri. PLoS One 6: e25649.
56. Sims, D. W., M. J. Genner, A. J. Southward, and S. J. Hawkins 2001. Timing of squid migration reflects North Atlantic climate variability. Proc. Biol. Soc. 268: 2607-2611.
57. Smale, M. J. 1996. Cephalopods as prey. IV. Fishes. Philos. Trans. R. Soc. Lond. B 351: 1067-1081.
58. Thompson, F. L., T. Ida, and J. Swings. 2004. Biodiversity of vibrios. Microbiol. Mol. Biol. Rev. 68: 403-431.
59. Tong, D., N. S. Rozas, T. H. Oakley, J. Mitchell, N. J. Colley, and M. J. McFall-Ngai. 2009. Light perception in a bioluminescent organ. Proc. Natl. Acad. Sci. USA 106: 9836-9841.
60. Troll, J. V., D. M. Adin, A. M. Wier, N. Paquette, N. Silverman, W. E. Goldman, F. J. Stadermann, E. V. Stabb, and M. J. McFall-Ngai. 2009. Peptidoglycan induces loss of a nuclear peptidoglycan recognition protein during host tissue development in a beneficial animalbacterial symbiosis. Cell. Microbiol. 11: 1114-1127.
61. Troll, J. V., E. H. Bent, N. Pacquette, A. M. Wier, W. E. Goldman, N. Silverman, and M. J. McFall-Ngai. 2010. Taming the symbiont for coexistence: a host PGRP neutralizes a bacterial symbiont toxin. Environ. Microbiol. 12: 2190-2203.
62. Visick, K. L., and E. G. Ruby. 1998. The periplasmic, group III catalase of Vibrio fischeri is required for normal symbiotic competence and is induced both by oxidative stress and by approach to stationary phase. J. Bacteriol. 180: 2087-2092.
63. Visick, K. L., and L. M. Skoufos. 2001. Two-component sensor required for normal symbiotic colonization of Euprymna scolopes by Vibrio fischeri. J. Bacteriol. 183: 835-842.
64. Visick, K. L., J. Foster, J. Doino, M. J. McFall-Ngai, and E. G. Ruby. 2000. Vibrio fischeri lux genes play an important role in colonization and development of the host light organ. J. Bacteriol. 182: 4578-4586.
65. Wang, Y., Y. S. Dufourd, H. K. Carlson, T. J. Donohue, M. A. Marletta, and E. G. Ruby. 2010. H-Nox-mediated nitric oxide sensing modulates symbiotic colonization by Vibrio fischeri. Proc. Natl. Acad. Sci. USA 107: 8375-8380.
66. Weis, V. M., A. L. Small, and M. J. McFall-Ngai. 1996. A peroxidase related to the mammalian antimicrobial protein myeloperoxidase in the Euprymna-Vibrio mutualism. Proc. Natl. Acad. Sci. USA 93: 13683-13688.
67. Wier, A. M., S. V. Nyholm, M. J. Mandel, R. P. Massengo-Tiasse, A. L. Schaefer, I. Koroleva, S. Splinter-Bondurant, B. Brown, L. Manzella, E. Snir et al. 2010. Transcriptional patterns in both host and bacterium underlie a daily rhythm of anatomical and metabolic change in a beneficial symbiosis. Proc. Natl. Acad. Sci. USA 109: 2259-2264. 13688.
68. Wernegreen, J. J. 2002. Genome evolution in bacterial endosymbionts of insects. Nat. Rev. Genet. 3: 850-861.