A conserved chemical dialog of mutualism: Lessons from squid and vibrio

Microbes and Infection

Volumn 18, Issue 1, 2016, Pages 1-10

  Schwartzman, Julia A ^a   Ruby, Edward G ^b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF HAWAII   (United States)

Author keywords

Development; Innate immunity; MAMPs; Nutrition; Stress; Symbiosis

Indexed keywords

BIOLOGICAL RHYTHM; BIOLUMINESCENCE; CIRCADIAN RHYTHM; HOMEOSTASIS; MORPHOGENESIS; MUCUS; NONHUMAN; PRIORITY JOURNAL; SHORT SURVEY; SQUID; SYMBIONT; SYMBIOSIS; VIBRIO; ANIMAL; DECAPODIFORMES; INNATE IMMUNITY; MICROBIOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ANIMALS; DECAPODIFORMES; IMMUNITY, INNATE; STRESS, PHYSIOLOGICAL; SYMBIOSIS; VIBRIO;

EID: 84953835325     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2015.08.016     Document Type: Short Survey

References (84)

1. Altura M.A., Heath-Heckman E.A., Gillette A., Kremer N., Krachler A.M., Brennan C., et al. 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 2013, 15:2937-2950.
2. Altura M.A., Stabb E., Goldman W., Apicella M., McFall-Ngai M.J. Attenuation of host NO production by MAMPs potentiates development of the host in the squid-vibrio symbiosis. Cell Microbiol 2011, 13:527-537.
3. Bass J., Takahashi J.S. Circadian integration of metabolism and energetics. Science 2010, 330:1349-1354.
4. Boettcher K., Ruby E., McFall-Ngai M. Bioluminescence in the symbiotic squid Euprymna scolopes is controlled by a daily biological rhythm. J Comp Physiol 1996, 179:65-73.
5. Boettcher K.J., Ruby E.G. Depressed light emission by symbiotic Vibrio fischeri of the sepiolid squid Euprymna scolopes. J Bacteriol 1990, 172:3701-3706.
6. Boettcher K.J., Ruby E.G. Detection and quantification of Vibrio fischeri autoinducer from symbiotic squid light organs. J Bacteriol 1995, 177:1053-1058.
7. Brennan C.A., Hunt J.R., Kremer N., Krasity B.C., Apicella M.A., McFall-Ngai M.J., et al. A model symbiosis reveals a role for sheathed-flagellum rotation in the release of immunogenic lipopolysaccharide. eLife 2014, 3:e01579.
8. Chang P.V., Hao L., Offermanns S., Medzhitov R. The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc Natl Acad Sci U S A 2014, 111:2247-2252.
9. Chovatiya R., Medzhitov R. Stress, inflammation, and defense of homeostasis. Mol Cell 2014, 54:281-288.
10. Chun C.K., Troll J.V., Koroleva I., Brown B., Manzella L., Snir E., et al. Effects of colonization, luminescence, and autoinducer on host transcription during development of the squid-vibrio association. Proc Natl Acad Sci U S A 2008, 105:11323-11328.
11. Claes M.F., Dunlap P.V. Aposymbiotic culture of the sepiolid squid Euprymna scolopes: role of the symbiotic bacterium Vibrio fischeri in host animal growth, development, and light organ morphogenesis. J Exp Zool 2000, 286:280-296.
12. Costello E.K., Stagaman K., Dethlefsen L., Bohannan B.J., Relman D.A. The application of ecological theory toward an understanding of the human microbiome. Science 2012, 336:1255-1262.
13. Cox L.M., Yamanishi S., Sohn J., Alekseyenko A.V., Leung J.M., Cho I., et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell 2014, 158:705-721.
14. Cullen T., Schofield W., Barry N., Putnam E., Rundell E., Trent M., et al. Antimicrobial peptide resistance mediates resilience of prominent gut commensals during inflammation. Science 2015, 347:170-175.
15. Davidson S.K., Koropatnick T.A., Kossmehl R., Sycuro L., McFall-Ngai M.J. NO means 'yes' in the squid-vibrio symbiosis: nitric oxide (NO) during the initial stages of a beneficial association. Cell Microbiol 2004, 6:1139-1151.
16. Doino J.A., McFall-Ngai M. A transient exposure to symbiosis-competent bacteria induces light organ morphogenesis in the host squid. Biol Bull 1995, 347-355.
17. Doino Lemus J., McFall-Ngai M.J. Alterations in the proteome of the Euprymna scolopes light organ in response to symbiotic Vibrio fischeri. Appl Environ Microbiol 2000, 66:4091-4097.
18. Dunn A.K. Vibrio fischeri metabolism: symbiosis and beyond. Adv Microb Physiol 2012, 61:37.
19. Dunn A.K., Karr E.A., Wang Y., Batton A.R., Ruby E.G., Stabb E.V. The alternative oxidase (AOX) gene in Vibrio fischeri is controlled by NsrR and upregulated in response to nitric oxide. Mol Microbiol 2010, 77:44-55.
20. Edgar R.S., Green E.W., Zhao Y., van Ooijen G., Olmedo M., Qin X., et al. Peroxiredoxins are conserved markers of circadian rhythms. Nature 2012, 485:459-464.
21. Erkosar B., Storelli G., Defaye A., Leulier F. Host-intestinal microbiota mutualism: 'learning on the fly'. Cell Host Microbe 2013, 13:8-14.
22. Fraune S., Bosch T.C. Long-term maintenance of species-specific bacterial microbiota in the basal metazoan Hydra. Proc Natl Acad Sci U S A 2007, 104:13146-13151.
23. Gilbert S.F. A holobiont birth narrative: the epigenetic transmission of the human microbiome. Front Genet 2014, 5:282.
24. Giles D.K., Hankins J.V., Guan Z., Trent M.S. Remodelling of the Vibrio cholerae membrane by incorporation of exogenous fatty acids from host and aquatic environments. Mol Microbiol 2011, 79:716-728.
25. Graf J., Ruby E.G. Host-derived amino acids support the proliferation of symbiotic bacteria. Proc Natl Acad Sci U S A 1998, 95:1818-1822.
26. Hashimoto C., Hudson K.L., Anderson K.V. The toll gene of Drosophila, required for dorsal-ventral embryonic polarity, appears to encode a transmembrane protein. Cell 1988, 52:269-279.
27. Hastings J., Balny C. The oxygenated bacterial luciferase-flavin intermediate. Reaction products via the light and dark pathways. J Biol Chem 1975, 250:7288-7293.
28. Heath-Heckman E.A., McFall-Ngai M.J. The occurrence of chitin in the hemocytes of invertebrates. Zoology 2011, 114:191-198.
29. Heath-Heckman E.A., Peyer S.M., Whistler C.A., Apicella M.A., Goldman W.E., McFall-Ngai M.J. Bacterial bioluminescence regulates expression of a host cryptochrome gene in the squid-vibrio symbiosis. mBio 2013, 4. e00167-13.
30. Heath-Heckman E.A., Gillette A.A., Augustin R., Gillette M.X., Goldman W.E., McFall-Ngai M.J. Shaping the microenvironment: evidence for the influence of a host galaxin on symbiont acquisition and maintenance in the squid-vibrio symbiosis. Environ Microbiol 2014, 16:3669-3682.
31. Hoyle N.P., O'Neill J.S. Oxidation-reduction cycles of peroxiredoxin proteins and non-transcriptional aspects of timekeeping. Biochemistry 2015, 54:184-193.
32. Janeway C.A. Approaching the Asymptote? Evolution and Revolution in Immunology. Cold Spring Harbor Symposia on Quantitative Biology 1989, 1-13. Cold Spring Harbor Laboratory Press.
33. Koch E.J., Miyashiro T.I., McFall-Ngai M.J., Ruby E.G. Features governing symbiont persistence in the squid-vibrio association. Mol Ecol 2013, 23:1624-1634.
34. Koropatnick T., Goodson M.S., Heath-Heckman E.A., McFall-Ngai M. Identifying the cellular mechanisms of symbiont-induced epithelial morphogenesis in the squid-vibrio association. Biol Bull 2014, 226:56-68.
35. Koropatnick T.A., Engle J.T., Apicella M.A., Stabb E.V., Goldman W.E., McFall-Ngai M.J. Microbial factor-mediated development in a host-bacterial mutualism. Science 2004, 306:1186-1188.
36. Koropatnick T.A., Kimbell J.R., McFall-Ngai M.J. Responses of host hemocytes during the initiation of the squid-vibrio symbiosis. Biol Bull 2007, 212:29-39.
37. Kremer N., Philipp E.E., Carpentier M.-C., Brennan C.A., Kraemer L., Altura M.A., et al. Initial symbiont contact orchestrates host-organ-wide transcriptional changes that prime tissue colonization. Cell Host Microbe 2013, 14:183-194.
38. Kremer N., Schwartzman J., Augustin R., Zhou L., Ruby E.G., Hourdez S., et al. The dual nature of haemocyanin in the establishment and persistence of the squid-vibrio symbiosis. Proc Biol Sci 2014, 281.
39. Lamarcq L.H., McFall-Ngai M.J. Induction of a gradual, reversible morphogenesis of its host's epithelial brush border by Vibrio fischeri. Infect Immun 1998, 66:777-785.
40. Lee K.H., Ruby E.G. Effect of the squid host on the abundance and distribution of symbiotic Vibrio fischeri in nature. Appl Environ Microbiol 1994, 60:1565-1571.
41. Mandel M.J., Schaefer A.L., Brennan C.A., Heath-Heckman E.A., DeLoney-Marino C.R., McFall-Ngai M.J., et al. Squid-derived chitin oligosaccharides are a chemotactic signal during colonization by Vibrio fischeri. Appl Environ Microbiol 2012, 78:4620-4626.
42. Mandel M.J., Wollenberg M.S., Stabb E.V., Visick K.L., Ruby E.G. A single regulatory gene is sufficient to alter bacterial host range. Nature 2009, 458:215-218.
43. McFall-Ngai M., Hadfield M.G., Bosch T.C., Carey H.V., Domazet-Lošo T., Douglas A.E., et al. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci U S A 2013, 110:3229-3236.
44. McFall-Ngai M., Heath-Heckman E.A., Gillette A.A., Peyer S.M., Harvie E.A. The secret languages of coevolved symbioses: Insights from the Euprymna scolopes-Vibrio fischeri symbiosis. Semin Immunol 2012, 24:3-8.
45. McFall-Ngai M., Nyholm S.V., Castillo M.G. The role of the immune system in the initiation and persistence of the Euprymna scolopes-Vibrio fischeri symbiosis. Semin Immunol, Elsevier 2010, 48-53.
46. McFall-Ngai M.J. The importance of microbes in animal development: lessons from the squid-vibrio symbiosis. Annu Rev Microbiol 2014, 68.
47. Miyashiro T., Klein W., Oehlert D., Cao X., Schwartzman J., Ruby E.G. The N-acetyl-d-glucosamine repressor NagC of Vibrio fischeri facilitates colonization of Euprymna scolopes. Mol Microbiol 2011, 82:894-903.
48. Miyashiro T., Ruby E.G. Shedding light on bioluminescence regulation in Vibrio fischeri. Mol Microbiol 2012, 84:795-806.
49. Mowat A.M., Agace W.W. Regional specialization within the intestinal immune system. Nat Rev Immunol 2014, 10:667-685.
50. Mukherji A., Kobiita A., Ye T., Chambon P. Homeostasis in intestinal epithelium is orchestrated by the circadian clock and microbiota cues transduced by TLRs. Cell 2013, 153:812-827.
51. Naik S., Bouladoux N., Linehan J.L., Han S.-J., Harrison O.J., Wilhelm C., et al. Commensal-dendritic-cell interaction specifies a unique protective skin immune signature. Nature 2015, 520:104-108.
52. Nyholm S.V., Deplancke B., Gaskins H.R., Apicella M.A., McFall-Ngai M.J. 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 2002, 68:5113-5122.
53. Nyholm S.V., Graf J. Knowing your friends: invertebrate innate immunity fosters beneficial bacterial symbioses. Nat Rev Microbiol 2012, 10:815-827.
54. Nyholm S.V., McFall-Ngai M.J. 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 1998, 195:89-97.
55. Nyholm S.V., McFall-Ngai M.J. Dominance of Vibrio fischeri in secreted mucus outside the light organ of Euprymna scolopes: the first site of symbiont specificity. Appl Environ Microbiol 2003, 69:3932-3937.
56. Nyholm S.V., McFall-Ngai M.J. The winnowing: establishing the squid-vibrio symbiosis. Nat Rev Microbiol 2004, 2:632-642.
57. Nyholm S.V., Stewart J.J., Ruby E.G., McFall-Ngai M.J. Recognition between symbiotic Vibrio fischeri and the haemocytes of Euprymna scolopes. Environ Microbiol 2009, 11:483-493.
58. Pan M., Schwartzman J.A., Dunn A.K., Lu Z., Ruby E.G. A single host-derived glycan impacts key regulatory nodes of symbiont metabolism in a coevolved mutualism. mBio 2015, 6:e00811-e00815.
59. Peyer S.M., Pankey M.S., Oakley T.H., McFall-Ngai M.J. Eye-specification genes in the bacterial light organ of the bobtail squid Euprymna scolopes, and their expression in response to symbiont cues. Mech Dev 2014, 131:111-126.
60. Pride A.C., Herrera C.M., Guan Z., Giles D.K., Trent M.S. The outer surface lipoprotein VolA mediates utilization of exogenous lipids by Vibrio cholerae. mBio 2013, 4:e00305-e00313.
61. Provenzano D., Klose K.E. Altered expression of the ToxR-regulated porins OmpU and OmpT diminishes Vibrio cholerae bile resistance, virulence factor expression, and intestinal colonization. Proc Natl Acad Sci U S A 2000, 97:10220-10224.
62. Rader B.A., Kremer N., Apicella M.A., Goldman W.E., McFall-Ngai M.J. Modulation of symbiont lipid A signaling by host alkaline phosphatases in the squid-vibrio symbiosis. mBio 2012, 3. e00093-12.
63. Rader B.A., Nyholm S.V. Host/microbe interactions revealed through "omics" in the symbiosis between the Hawaiian bobtail squid Euprymna scolopes and the bioluminescent bacterium Vibrio fischeri. Biol Bull 2012, 223:103-111.
64. Ruby E.G., Asato L.M. Growth and flagellation of Vibrio fischeri during initiation of the sepiolid squid light organ symbiosis. Arch Microbiol 1993, 159:160-167.
65. Saito H.E., Harp J.R., Fozo E.M. Incorporation of exogenous fatty acids protects Enterococcus faecalis from membrane-damaging agents. Appl Environ Microbiol 2014, 80:6527-6538.
66. Schleicher T.R., Nyholm S.V. Characterizing the host and symbiont proteomes in the association between the bobtail squid, Euprymna scolopes, and the bacterium, Vibrio fischeri. PLoS One 2011, 6:e25649.
67. Schleicher T.R., VerBerkmoes N.C., Shah M., Nyholm S.V. Colonization state influences the hemocyte proteome in a beneficial squid-vibrio symbiosis. Mol Cell Proteom 2014, 13:2673-2686.
68. Schuster B.M., Perry L.A., Cooper V.S., Whistler C.A. Breaking the language barrier: experimental evolution of non-native Vibrio fischeri in squid tailors luminescence to the host. Symbiosis 2010, 51:85-96.
69. Schwartzman J.A., Koch E., Heath-Heckman E.A., Zhou L., Kremer N., McFall-Ngai M.J., et al. The chemistry of negotiation: rhythmic, glycan-driven acidification in a symbiotic conversation. Proc Natl Acad Sci U S A 2015, 112:566-571.
70. Septer A.N., Wang Y., Ruby E.G., Stabb E.V., Dunn A.K. The haem-uptake gene cluster in Vibrio fischeri is regulated by Fur and contributes to symbiotic colonization. Environ Microbiol 2011, 13:2855-2864.
71. Singley C. Euprymna scolopes. Cephalopod Life Cycles: Species Accounts 1983, vol. 1:69.
72. Small A.L., McFall-Ngai M.J. Halide peroxidase in tissues that interact with bacteria in the host squid Euprymna scolopes. J Cell Biochem 1999, 72:445-457.
73. Studer S.V., Schwartzman J.A., Ho J.S., Geske G.D., Blackwell H.E., Ruby E.G. Non-native acylated homoserine lactones reveal that LuxIR quorum sensing promotes symbiont stability. Environ Microbiol 2013, 16:2623-2634.
74. Sycuro L.K., Ruby E.G., McFall-Ngai M. Confocal microscopy of the light organ crypts in juvenile Euprymna scolopes reveals their morphological complexity and dynamic function in symbiosis. J Morphol 2006, 267:555-568.
75. Troll J.V., Bent E.H., Pacquette N., Wier A.M., Goldman W.E., Silverman N., et al. Taming the symbiont for coexistence: a host PGRP neutralizes a bacterial symbiont toxin. Environ Microbiol 2010, 12:2190-2203.
76. Visick K.L. An intricate network of regulators controls biofilm formation and colonization by Vibrio fischeri. Mol Microbiol 2009, 74:782-789.
77. Visick K.L., Foster J., Doino J., McFall-Ngai M., Ruby E.G. Vibrio fischeri lux genes play an important role in colonization and development of the host light organ. J Bacteriol 2000, 182:4578-4586.
78. Visick K.L., Ruby E.G. 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 1998, 180:2087-2092.
79. Wang Y., Dufour Y.S., Carlson H.K., Donohue T.J., Marletta M.A., Ruby E.G. H-NOX-mediated nitric oxide sensing modulates symbiotic colonization by Vibrio fischeri. Proc Natl Acad Sci U S A 2010, 107:8375-8380.
80. Wang Y., Dunn A.K., Wilneff J., McFall-Ngai M.J., Spiro S., Ruby E.G. Vibrio fischeri flavohaemoglobin protects against nitric oxide during initiation of the squid-vibrio symbiosis. Mol Microbiol 2010, 78:903-915.
81. Weis V.M., Small A.L., McFall-Ngai M.J. A peroxidase related to the mammalian antimicrobial protein myeloperoxidase in the Euprymna-Vibrio mutualism. Proc Natl Acad Sci U S A 1996, 93:13683-13688.
82. Wier A.M., Nyholm S.V., Mandel M.J., Massengo-Tiassé P.R., Schaefer A.L., Koroleva I., et al. Transcriptional patterns in both host and bacterium underlie a daily rhythm of anatomical and metabolic change in a beneficial symbiosis. Proc Natl Acad Sci U S A 2010, 107:2259-2264.
83. Wollenberg M.S., Ruby E.G. Phylogeny and fitness of Vibrio fischeri from the light organs of Euprymna scolopes in two Oahu, Hawaii populations. ISME 2012, 6:352-362.
84. Yip E.S., Geszvain K., DeLoney-Marino C.R., Visick K.L. The symbiosis regulator RscS controls the syp gene locus, biofilm formation and symbiotic aggregation by Vibrio fischeri. Mol Microbiol 2006, 62:1586-1600.