Shaping the microenvironment: Evidence for the influence of a host galaxin on symbiont acquisition and maintenance in the squid-vibrio symbiosis

Environmental Microbiology

Volumn 16, Issue 12, 2014, Pages 3669-3682

  Heath Heckman, Elizabeth A C ^a   Gillette, Amani A ^a   Augustin, René ^a,c   Gillette, Miles X ^a   Goldman, William E ^b   Mcfall Ngai, Margaret J ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF KIEL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; BACTERIA (MICROORGANISMS); CEPHALOPODA; EUPRYMNA SCOLOPES; POSIBACTERIA; VIBRIO; VIBRIO FISCHERI;

ANTIINFECTIVE AGENT; PEPTIDE; PROTEIN; TRANSCRIPTOME;

ALIIVIBRIO FISCHERI; ANIMAL; BACTERIUM; CHEMISTRY; DECAPODIFORMES; DRUG EFFECTS; EPITHELIUM; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MUCUS; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYMBIOSIS;

ALIIVIBRIO FISCHERI; ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIA; DECAPODIFORMES; EPITHELIUM; MUCUS; PEPTIDES; PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SYMBIOSIS; TRANSCRIPTOME;

EID: 84921602424     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12496     Document Type: Article

References (62)

1. Aeckersberg, F., Lupp, C., Feliciano, B., and Ruby, E.G. (2001) Vibrio fischeri outer membrane protein OmpU plays a role in normal symbiotic colonization. J Bacteriol 183: 6590-6597.
2. Altura, M.A., Heath-Heckman, E.A., Gillette, A., Kremer, N., Krachler, A.M., Brennan, C., etal. (2013) The first engagement of partners in the Euprymna scolopes-Vibrio fischeri symbiosis is a two-step process initiated by a few environmental symbiont cells. Environ Microbiol 15: 2937-2950.
3. Blattner, F.R., Plunkett, G., 3rd, Bloch, C.A., Perna, N.T., Burland, V., Riley, M., etal. (1997) The complete genome sequence of Escherichia coli K-12. Science 277: 1453-1462.
4. Boettcher, K.J., and Ruby, E.G. (1990) Depressed light emission by symbiotic Vibrio fischeri of the sepiolid squid Euprymna scolopes. J Bacteriol 172: 3701-3706.
5. Bose, J.L., Rosenberg, C.S., and Stabb, E.V. (2008) Effects of luxCDABEG induction in Vibrio fischeri: enhancement of symbiotic colonization and conditional attenuation of growth in culture. Arch Microbiol 190: 169-183.
6. Bright, M., and Bulgheresi, S. (2010) A complex journey: transmission of microbial symbionts. Nat Rev Microbiol 8: 218-230.
7. Bulgarelli, D., Schlaeppi, K., Spaepen, S., Ver Loren van Themaat, E., and Schulze-Lefert, P. (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64: 807-838.
8. Bulgheresi, S., Gruber-Vodicka, H.R., Heindl, N.R., Dirks, U., Kostadinova, M., Breiteneder, H., etal. (2011) Sequence variability of the pattern recognition receptor mermaid mediates specificity of marine nematode symbioses. ISME J 5: 986-998.
9. Bustin, S.A., Benes, V., Garson, J.A., Hellemans, J., Huggett, J., Kubista, M., etal. (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55: 611-622.
10. Cash, H.L., Whitham, C.V., Behrendt, C.L., and Hooper, L.V. (2006) Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 313: 1126-1130.
11. Chun, C.K., Scheetz, T.E., Bonaldo Mde, F., Brown, B., Clemens, A., Crookes-Goodson, W.J., etal. (2006) An annotated cDNA library of juvenile Euprymna scolopes with and without colonization by the symbiont Vibrio fischeri. BMC Genomics 7: 154.
12. Chun, C.K., Troll, J.V., Koroleva, I., Brown, B., Manzella, L., Snir, E., etal. (2008) Effects of colonization, luminescence, and autoinducer on host transcription during development of the squid-vibrio association. Proc Natl Acad Sci USA 105: 11323-11328.
13. Collins, A.J., LaBarre, B.A., Won, B.S., Shah, M.V., Heng, S., Choudhury, M.H., etal. (2012) Diversity and partitioning of bacterial populations within the accessory nidamental gland of the squid Euprymna scolopes. Appl Environ Microbiol 78: 4200-4208.
14. Davidson, S.K., Koropatnick, T.A., Kossmehl, R., Sycuro, L., and McFall-Ngai, M.J. (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.
15. Davy, S.K., Allemand, D., and Weis, V.M. (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol Rev 76: 229-261.
16. Doino, J.A., and McFall-Ngai, M.J. (1995) A transient exposure to symbiosis-competent bacteria induces light organ morphogenesis in the host squid. Biol Bull 189: 347-355.
17. Dunlap, P.V. (1985) Osmotic control of luminescence and growth in Photobacterium leiognathi from ponyfish light organs. Arch Microbiol 141: 44-50.
18. Dunn, A.K., Millikan, D.S., Adin, D.M., Bose, J.L., and Stabb, E.V. (2006) New rfp- and pES213-derived tools for analyzing symbiotic Vibrio fischeri reveal patterns of infection and lux expression in situ. Appl Environ Microbiol 72: 802-810.
19. Edgar, R.C. (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.
20. Epand, R.M., and Epand, R.F. (2011) Bacterial membrane lipids in the action of antimicrobial agents. J Pept Sci 17: 298-305.
21. Fedders, H., and Leippe, M. (2008) A reverse search for antimicrobial peptides in Ciona intestinalis: identification of a gene family expressed in hemocytes and evaluation of activity. Dev Comp Immunol 32: 286-298.
22. Foster, J.S., Apicella, M.A., and McFall-Ngai, M.J. (2000) Vibrio fischeri lipopolysaccharide induces developmental apoptosis, but not complete morphogenesis, of the Euprymna scolopes symbiotic light organ. Dev Biol 226: 242-254.
23. Franzenburg, S., Walter, J., Kunzel, S., Wang, J., Baines, J.F., Bosch, T.C., etal. (2013) Distinct antimicrobial peptide expression determines host species-specific bacterial associations. Proc Natl Acad Sci USA 110: E3730-E3738.
24. Fraune, S., Augustin, R., Anton-Erxleben, F., Wittlieb, J., Gelhaus, C., Klimovich, V.B., etal. (2010) In an early branching metazoan, bacterial colonization of the embryo is controlled by maternal antimicrobial peptides. Proc Natl Acad Sci USA 107: 18067-18072.
25. Fuhrman, J.A. (2009) Microbial community structure and its functional implications. Nature 459: 193-199.
26. Fukuda, I., Ooki, S., Fujita, T., Murayama, E., Nagasawa, H., Isa, Y., etal. (2003) Molecular cloning of a cDNA encoding a soluble protein in the coral exoskeleton. Biochem Biophys Res Commun 304: 11-17.
27. Gallo, R.L., and Hooper, L.V. (2012) Epithelial antimicrobial defence of the skin and intestine. Nat Rev Immunol 12: 503-516.
28. Gontang, E.A., Fenical, W., and Jensen, P.R. (2007) Phylogenetic diversity of gram-positive bacteria cultured from marine sediments. Appl Environ Microbiol 73: 3272-3282.
29. Graf, J., and Ruby, E.G. (1998) Host-derived amino acids support the proliferation of symbiotic bacteria. Proc Natl Acad Sci USA 95: 1818-1822.
30. Heath-Heckman, E.A.C., Peyer, S.M., Whistler, C.A., Apicella, M.A., Goldman, W.E., and McFall-Ngai, M.J. (2013) Bacterial bioluminescence regulates expression of a host cryptochrome gene in the squid-Vibrio symbiosis. mBio 4: e00167-13.
31. Koropatnick, T.A., Engle, J.T., Apicella, M.A., Stabb, E.V., Goldman, W.E., and McFall-Ngai, M.J. (2004) Microbial factor-mediated development in a host-bacterial mutualism. Science 306: 1186-1188.
32. Krediet, C.J., Ritchie, K.B., Paul, V.J., and Teplitski, M. (2013) Coral-associated micro-organisms and their roles in promoting coral health and thwarting diseases. Proc Biol Sci 280: 20122328.
33. Kremer, N., Philipp, E.E., Carpentier, M.C., Brennan, C.A., Kraemer, L., Altura, M.A., etal. (2013) Initial symbiont contact orchestrates host-organ-wide transcriptional changes that prime tissue colonization. Cell Host Microbe 14: 183-194.
34. Lamarcq, L.H., and McFall-Ngai, M.J. (1998) Induction of a gradual, reversible morphogenesis of its host's epithelial brush border by Vibrio fischeri. Infect Immun 66: 777-785.
35. Login, F.H., Balmand, S., Vallier, A., Vincent-Monegat, C., Vigneron, A., Weiss-Gayet, M., etal. (2011) Antimicrobial peptides keep insect endosymbionts under control. Science 334: 362-365.
36. Lundgren, P., Vera, J.C., Peplow, L., Manel, S., and van Oppen, M.J. (2013) Genotype - environment correlations in corals from the Great Barrier Reef. BMC Genet 14: 9.
37. McFall-Ngai, M., Nyholm, S.V., and Castillo, M.G. (2010) The role of the immune system in the initiation and persistence of the Euprymna scolopes-Vibrio fischeri symbiosis. Semin Immunol 22: 48-53.
38. McFall-Ngai, M., Heath-Heckman, E.A., Gillette, A.A., Peyer, S.M., and Harvie, E.A. (2012) The secret languages of coevolved symbioses: insights from the Euprymna scolopes-Vibrio fischeri symbiosis. Semin Immunol 24: 3-8.
39. Needham, D.M., Chow, C.E., Cram, J.A., Sachdeva, R., Parada, A., and Fuhrman, J.A. (2013) Short-term observations of marine bacterial and viral communities: patterns, connections and resilience. ISME J 7: 1274-1285.
40. Nyholm, S.V., and McFall-Ngai, M.J. (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.
41. Nyholm, S.V., and McFall-Ngai, M.J. (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.
42. Nyholm, S.V., and McFall-Ngai, M.J. (2004) The winnowing: establishing the squid-vibrio symbiosis. Nat Rev Microbiol 2: 632-642.
43. Nyholm, S.V., Stabb, E.V., Ruby, E.G., and McFall-Ngai, M.J. (2000) Establishment of an animal-bacterial association: recruiting symbiotic vibrios from the environment. Proc Natl Acad Sci USA 97: 10231-10235.
44. Nyholm, S.V., Deplancke, B., Gaskins, H.R., Apicella, M.A., and McFall-Ngai, M.J. (2002) Roles of Vibrio fischeri and nonsymbiotic bacteria in the dynamics of mucus secretion during symbiont colonization of the Euprymna scolopes light organ. Appl Environ Microbiol 68: 5113-5122.
45. de Oliveira, L.S., Gregoracci, G.B., Silva, G.G., Salgado, L.T., Filho, G.A., Alves-Ferreira, M., etal. (2012) Transcriptomic analysis of the red seaweed Laurencia dendroidea (Florideophyceae, Rhodophyta) and its microbiome. BMC Genomics 13: 487.
46. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
47. Redmond, J.W., Batley, M., Djordjevic, M.A., Innes, R.W., Kuempel, P.L., and Rolfe, B.G. (1986) Flavones induce expression of nodulation genes in rhizobium. Nature 323: 632-635.
48. Reyes-Bermudez, A., Lin, Z., Hayward, D.C., Miller, D.J., and Ball, E.E. (2009) Differential expression of three galaxin-related genes during settlement and metamorphosis in the scleractinian coral Acropora millepora. BMC Evol Biol 9: 178.
49. Ruby, E.G., and Asato, L.M. (1993) Growth and flagellation of Vibrio fischeri during initiation of the sepiolid squid light organ symbiosis. Arch Microbiol 159: 160-167.
50. Salzman, N.H., Hung, K., Haribhai, D., Chu, H., Karlsson-Sjoberg, J., Amir, E., etal. (2010) Enteric defensins are essential regulators of intestinal microbial ecology. Nat Immunol 11: 76-83.
51. Sanchez, S., Hourdez, S., and Lallier, F.H. (2007) Identification of proteins involved in the functioning of Riftia pachyptila symbiosis by Subtractive Suppression Hybridization. BMC Genomics 8: 337.
52. Schwarz, J.A., Mitchelmore, C.L., Jones, R., O'Dea, A., and Seymour, S. (2012) Exposure to copper induces oxidative and stress responses and DNA damage in the coral Montastraea franksi. Comp Biochem Physiol C Toxicol Pharmacol 157: 272-279.
53. Shnit-Orland, M., Sivan, A., and Kushmaro, A. (2012) Antibacterial activity of Pseudoalteromonas in the coral holobiont. Microb Ecol 64: 851-859.
54. Stabb, E., and Visick, K. (2013) Vibrio fisheri: Squid Symbiosis. In The Prokaryotes. Rosenberg, E., DeLong, E., Lory, S., Stackebrandt, E., and Thompson, F. (eds). Berlin Heidelberg, Germany: Springer-Verlag, pp. 497-532.
55. Troll, J.V., Adin, D.M., Wier, A.M., Paquette, N., Silverman, N., Goldman, W.E., etal. (2009) Peptidoglycan induces loss of a nuclear peptidoglycan recognition protein during host tissue development in a beneficial animal-bacterial symbiosis. Cell Microbiol 11: 1114-1127.
56. Troll, J.V., Bent, E.H., Pacquette, N., Wier, A.M., Goldman, W.E., Silverman, N., etal. (2010) Taming the symbiont for coexistence: a host PGRP neutralizes a bacterial symbiont toxin. Environ Microbiol 12: 2190-2203.
57. Vaishnava, S., Yamamoto, M., Severson, K.M., Ruhn, K.A., Yu, X., Koren, O., etal. (2011) The antibacterial lectin RegIIIγ promotes the spatial segregation of microbiota and host in the intestine. Science 334: 255-258.
58. Visick, K.G., and Ruby, E.G. (1996) Construction and symbiotic competence of a luxA-deletion mutant of Vibrio fischeri. Gene 175: 89-94.
59. Wang, Y., Dunn, A.K., Wilneff, J., McFall-Ngai, M.J., Spiro, S., and Ruby, E.G. (2010) Vibrio fischeri flavohaemoglobin protects against nitric oxide during initiation of the squid-Vibrio symbiosis. Mol Microbiol 78: 903-915.
60. Watanabe, T., Fukuda, I., China, K., and Isa, Y. (2003) Molecular analyses of protein components of the organic matrix in the exoskeleton of two scleractinian coral species. Comp Biochem Physiol B Biochem Mol Biol 136: 767-774.
61. Wier, A.M., Nyholm, S.V., Mandel, M.J., Massengo-Tiasse, R.P., Schaefer, A.L., Koroleva, I., etal. (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 107: 2259-2264.
62. Wollenberg, M.S., and Ruby, E.G. (2012) Phylogeny and fitness of Vibrio fischeri from the light organs of Euprymna scolopes in two Oahu, Hawaii populations. ISME J 6: 352-362.