The importance of microbes in animal development: Lessons from the squid-vibrio symbiosis

Annual Review of Microbiology

Volumn 68, Issue , 2014, Pages 177-194

  McFall Ngai, Margaret J ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Colonization; Euprymna scolopes; Holobiont; Horizontal transmission; Morphogenesis; Vibrio fischeri

Indexed keywords

ALIIVIBRIO FISCHERI; CIRCADIAN RHYTHM; DEVELOPMENTAL BIOLOGY; ECOLOGICAL NICHE; EMBRYO DEVELOPMENT; GASTROINTESTINAL TRACT; GENE CONTROL; MICROBIAL COMMUNITY; MICROORGANISM; MORPHOGENESIS; NONHUMAN; ORGAN; OSCILLATION; REVIEW; SQUID; SYMBIONT; SYMBIOSIS;

EID: 84907502395     PISSN: 00664227     EISSN: 15453251     Source Type: Book Series    
DOI: 10.1146/annurev-micro-091313-103654     Document Type: Review

References (99)

1. Adin DM, Engle JT, Goldman WE, McFall-Ngai MJ, Stabb EV. 2009. Mutations in ampG and lytic transglycosylase genes affect the net release of peptidoglycan monomers from Vibrio fischeri. J. Bacteriol. 191:2012-22
2. Altura MA,Heath-Heckman EA, Gillette A, Kremer N, Krachler AM, et al. 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. 15:2937-50
3. Altura MA, Stabb E, Goldman W, Apicella M, McFall-Ngai MJ. 2011. Attenuation of host NO production by MAMPs potentiates development of the host in the squid-vibrio symbiosis. Cell Microbiol. 13:527-37
4. Bass J, Takahashi JS. 2011. Circadian rhythms: redox redux. Nature 469:476-78
5. Boettcher KJ, Ruby EG, McFall-Ngai MJ. 1996. Bioluminescence in the symbiotic squid Euprymna scolopes is controlled by a daily biological rhythm. J. Comp. Physiol. 179:65-73
6. Bosch TC, McFall-Ngai MJ. 2011. Metaorganisms as the new frontier. Zoology (JENA) 114:185-90
7. Bosch TCG. 2013. Cnidarian-microbe interactions and the origin of innate immunity in metazoans. Annu. Rev. Microbiol. 67:499-518
8. Brennan CA, Mandel MJ, Gyllborg MC, Thomasgard KA, Ruby EG. 2013. Genetic determinants of swimming motility in the squid light-organ symbiont Vibrio fischeri. MicrobiologyOpen 2:576-94
9. Bright M, Bulgheresi S. 2010. A complex journey: transmission of microbial symbionts. Nat. Rev. Microbiol. 8:218-30
10. Bron R, Furness JB. 2009. Rhythm of digestion: keeping time in the gastrointestinal tract. Clin. Exp. Pharmacol. Physiol. 36:1041-48
11. Chun CK, Troll JV, Koroleva I, Brown B,Manzella L, et al. 2008. Effects of colonization, luminescence, and autoinducer on host transcription during development of the squid-vibrio association. Proc. Natl. Acad. Sci. USA 105:11323-28
12. Crookes WJ, Ding LL, Huang QL, Kimbell JR, Horwitz J, McFall-Ngai MJ. 2004. Reflectins: the unusual proteins of squid reflective tissues. Science 303:235-38
13. Davidson SK, Koropatnick TA, Kossmehl R, Sycuro L, McFall-Ngai MJ. 2004. NO means yes in the squid-vibrio symbiosis: nitric oxide (NO) during the initial stages of a beneficial association. Cell Microbiol. 6:1139-51
14. de Bary HA. 1879. Die Erscheinung der Symbiose. Strassburg, Fr.: K.J. Trubner
15. Deloney-Marino CR, Visick KL. 2012. Role for cheR of Vibrio fischeri in the Vibrio-squid symbiosis. Can. J. Microbiol. 58:29-38
16. Denton EJ, Herring PJ,Widder EA, Latz MF, Case JF. 1985. The roles of filters in the photophores of oceanic animals and their relation to vision in the oceanic environment. Proc. R. Soc. Lond. B 225:63-97
17. Doino JA, McFall-Ngai MJ. 1995. A transient exposure to symbiosis competent bacteria induces light organ morphogenesis in the host squid. Biol. Bull. 189:347-55
18. Douglas AE. 1989. Mycetocyte symbiosis in insects. Biol. Rev. Camb. Philos. Soc. 64:409-34
19. Douglas AE. 2010. The Symbiotic Habit. Princeton, NJ: Princeton Univ. Press
20. Duperthuy M, Binesse J, Le Roux F, Romestand B, Caro A, et al. 2010. The major outer membrane protein OmpU of Vibrio splendidus contributes to host antimicrobial peptide resistance and is required for virulence in the oyster Crassostrea gigas. Environ. Microbiol. 12:951-63
21. Edgar RS, Green EW, Zhao Y, van Ooijen G, Olmedo M, et al. 2012. Peroxiredoxins are conserved markers of circadian rhythms. Nature 485:459-64
22. Engel P, Moran NA. 2013. The gut microbiota of insects-diversity in structure and function. FEMS Microbiol. Rev. 37:699-735
23. Fidopiastis PM, Rader BA, Gerling DG, Gutierrez NA, Watkins KH, et al. 2012. Characterization of a Vibrio fischeri aminopeptidase and evidence for its influence on an early stage of squid colonization. J. Bacteriol. 194:3995-4002
24. Flak TA, Heiss LN, Engle JT, Goldman WE. 2000. Synergistic epithelial responses to endotoxin and a naturally occurring muramyl peptide. Infect. Immun. 68:1235-42
25. Gilbert SF, Sapp J, Tauber AI. 2012. A symbiotic view of life: We have never been individuals. Q. Rev. Biol. 87:325-41
26. Gordon JI. 2012. Honor thy gut symbionts redux. Science 336:1251-53
27. Graf J, Dunlap PV, Ruby EG. 1994. Effect of transposon-induced motility mutations on colonization of the host light organ by Vibrio fischeri. J. Bacteriol. 176:6986-91
28. Graf J, Ruby EG. 1998. Host-derived amino acids support the proliferation of symbiotic bacteria. Proc. Natl. Acad. Sci. USA 95:1818-22
29. Grice EA, Segre JA. 2011. The skin microbiome. Nat. Rev. Microbiol. 9:244-53
30. Hadfield MG. 2011. Biofilms and marine invertebrate larvae: what bacteria produce that larvae use to choose settlement sites. Annu. Rev. Mar. Sci. 3:453-70
31. Hanlon RT,ClaesMF, Ashcraft SE, Dunlap PV. 1997. Laboratory culture of the sepiolid squid Euprymna scolopes: a model system for bacteria-animal symbiosis. Biol. Bull. 192:364-74
32. Heath-Heckman EA, Peyer SM, Whistler CA, Apicella MA, Goldman WE, McFall-Ngai MJ. 2013. Bacterial bioluminescence regulates expression of a host cryptochrome gene in the squid-vibrio symbiosis. mBio 4:e00167-13
33. Hooper LV, Littman DR, Macpherson AJ. 2012. Interactions between the microbiota and the immune system. Science 336:1268-73
34. Hungate RE. 1966. The Rumen and Its Microbes. New York: Academic
35. Jones BW, Nishiguchi MK. 2004. Counterillumination in the bobtail squid, Euprymna scolopes (Mollusca: Cephalopoda). Mar. Biol. 144:1151-55
36. Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC. 2007. How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat. Rev. Microbiol. 5:619-33
37. Kimbell JR, McFall-Ngai MJ. 2004. Symbiont-induced changes in host actin during the onset of a beneficial animal-bacterial association. Appl. Environ. Microbiol. 70:1434-41
38. Kleinert H, Schwarz PM, Forstermann U. 2003. Regulation of the expression of inducible nitric oxide synthase. Biol. Chem. 384:1343-64
39. Koch EJ, Miyashiro T, McFall-Ngai MJ, Ruby EG. 2013. Features governing symbiont persistence in the squid-vibrio association. Mol. Ecol. 23:1624-34
40. Koropatnick T, Goodson MS, Heath-Heckman EAC, McFall-Ngai M. 2014. Identifying the cellular mechanisms of symbiont-induced epithelial morphogenesis in the squid-vibrio association. Biol. Bull. 226:56-68
41. Koropatnick TA, Engle JT, Apicella MA, Stabb EV, Goldman WE, McFall-Ngai MJ. 2004. Microbial factor-mediated development in a host-bacterial mutualism. Science 306:1186-88
42. Kostic AD, Howitt MR, Garrett WS. 2013. Exploring host-microbiota interactions in animal models and humans. Genes Dev. 27:701-18
43. Kremer N, Philipp EE, Carpentier MC, Brennan CA, Kraemer L, et al. 2013. Initial symbiont contact orchestrates host-organ-wide transcriptional changes that prime tissue colonization. Cell Host Microbe 14:183-94
44. Lamarcq LH, McFall-Ngai MJ. 1998. Induction of a gradual, reversible morphogenesis of its hosts epithelial brush border by Vibrio fischeri. Infect. Immun. 66:777-85
45. Lathrop SK, Bloom SM, Rao SM, Nutsch K, Lio CW, et al. 2011. Peripheral education of the immune system by colonic commensal microbiota. Nature 478:250-54
46. Lee K, Ruby EG. 1995. Symbiotic role of the viable but nonculturable state of Vibrio fischeri in Hawaiian coastal seawater. Appl. Environ. Microbiol. 61:278-83
47. Liu CX, Yin QQ, Zhou HC, Wu YL, Pu JX, et al. 2012. Adenanthin targets peroxiredoxin I and II to induce differentiation of leukemic cells. Nat. Chem. Biol. 8:486-93
48. Mandel MJ, Schaefer AL, Brennan CA, Heath-Heckman EA, Deloney-Marino CR, et al. 2012. Squidderived chitin oligosaccharides are a chemotactic signal during colonization by Vibrio fischeri. Appl. Environ. Microbiol. 78:4620-26
49. Mandel MJ,WollenbergMS, Stabb EV, Visick KL, Ruby EG. 2009. A single regulatory gene is sufficient to alter bacterial host range. Nature 458:215-18
50. Matamoros S, Gras-Leguen C, Le Vacon F, Potel G, de La Cochetiere M-F. 2013. Development of intestinal microbiota in infants and its impact on health. Trends Microbiol. 21:167-73
51. Mathur J, Davis BM, Waldor MK. 2007. Antimicrobial peptides activate the Vibrio cholerae σE regulon through an OmpU-dependent signalling pathway. Mol. Microbiol. 63:848-58
52. McFall-Ngai M, Hadfield MG, Bosch TC, Carey HV, Domazet-Loso T, et al. 2013. Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl. Acad. Sci. USA 110:3229-36
53. McFall-Ngai M, Heath-Heckman EA, Gillette AA, Peyer SM, Harvie EA. 2012. The secret languages of coevolved symbioses: insights from the Euprymna scolopes-Vibrio fischeri symbiosis. Semin. Immunol. 24:3-8
54. McFall-Ngai M, Montgomery MK. 1990. The anatomy and morphology of the adult bacterial light organ of Euprymna scolopes (Cephalopoda: Sepiolidae). Biol. Bull. 179:332-39
55. McFall-Ngai M, Nyholm SV, Castillo MG. 2010. The role of the immune system in the initiation and persistence of the Euprymna scolopes-Vibrio fischeri symbiosis. Semin. Immunol. 22:48-53
56. McFall-Ngai MJ. 2002. Unseen forces: the influence of bacteria on animal development. Dev. Biol. 242:1-14
57. Milligan-Myhre K, Charette JR, Phennicie RT, Stephens WZ, Rawls JF, et al. 2011. Study of hostmicrobe interactions in zebrafish. Methods Cell Biol. 105:87-116
58. MontgomeryMK, McFall-Ngai M. 1994. Bacterial symbionts induce host organ morphogenesis during early postembryonic development of the squid Euprymna scolopes. Development 120:1719-29
59. Montgomery MK, McFall-Ngai MJ. 1992. The muscle-derived lens of a squid bioluminescent organ is biochemically convergent with the ocular lens: evidence for recruitment of aldehyde dehydrogenase as a predominant structural protein. J. Biol. Chem. 267:20999-1003
60. Montgomery MK, McFall-Ngai MJ. 1993. Embryonic development of the light organ of the sepiolid squid Euprymna scolopes Berry. Biol. Bull. 184:296-308
61. Morris AR, Visick KL. 2013. Inhibition of SypG-induced biofilms and host colonization by the negative regulator SypE in Vibrio fischeri. PLoS ONE 8:e60076
62. Mukherji A, Kobiita A, Ye T, Chambon P. 2013. Homeostasis in intestinal epithelium is orchestrated by the circadian clock and microbiota cues transduced by TLRs. Cell 153:812-27
63. Norsworthy AN, Visick KL. 2013. Gimme shelter: how Vibrio fischeri successfully navigates an animals multiple environments. Front. Microbiol. 4:356
64. Nyholm SV,Deplancke B,Gaskins HR, Apicella MA,McFall-Ngai MJ. 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. 68:5113-22
65. Nyholm SV, McFall-Ngai MJ. 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
66. Nyholm SV, Stabb EV, Ruby EG, McFall-Ngai MJ. 2000. Establishment of an animal-bacterial association: recruiting symbiotic vibrios from the environment. Proc. Natl. Acad. Sci. USA 97:10231-35
67. Nyholm SV, Stewart JJ, Ruby EG,McFall-Ngai MJ. 2009. Recognition between symbiotic Vibrio fischeri and the haemocytes of Euprymna scolopes. Environ. Microbiol. 11:483-93
68. OldroydGE, Downie JA. 2008. Coordinating nodulemorphogenesiswith rhizobial infection in legumes. Annu. Rev. Plant Biol. 59:519-46
69. Ozturk N, Song SH, Ozgur S, Selby CP, Morrison L, et al. 2007. Structure and function of animal cryptochromes. Cold Spring Harb. Symp. Quant. Biol. 72:119-31
70. Parfrey LW, Knight R. 2012. Spatial and temporal variability of the human microbiota. Clin. Microbiol. Infection 18(Suppl. 4):8-11
71. Peyer SM, Pankey MS, Oakley TH, McFall-Ngai MJ. 2013. Eye-specification genes in the bacterial light organ of the bobtail squid Euprymna scolopes, and their expression in response to symbiont cues. Mech. Dev. 131:111-26
72. Pirofski LA, Casadevall A. 2008. The damage-response framework of microbial pathogenesis and infectious diseases. Adv. Exp. Med. Biol. 635:135-46
73. Reid DE, Ferguson BJ, Hayashi S, Lin YH, Gresshoff PM. 2011. Molecular mechanisms controlling legume autoregulation of nodulation. Ann. Bot. 108:789-95
74. Round JL, Lee SM, Li J, Tran G, Jabri B, et al. 2011. The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 332:974-77
75. Ruby EG. 2008. Symbiotic conversations are revealed under genetic interrogation. Nat. Rev. Microbiol. 6:752-62
76. Ruby EG, Asato LM. 1993. Growth and flagellation of Vibrio fischeri during initiation of the sepiolid squid light organ symbiosis. Arch. Microbiol. 159:160-67
77. Sage PT, Carman CV. 2009. Settings and mechanisms for trans-cellular diapedesis. Front. Biosci. 14:5066-83
78. Sawa S, Lochner M, Satoh-Takayama N, Dulauroy S, Berard M, et al. 2011. RORt+ innate lymphoid cells regulate intestinal homeostasis by integrating negative signals from the symbiotic microbiota. Nat. Immunol. 12:320-26
79. Schleicher TR, Nyholm SV. 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
80. Schmidt MA. 2010. LEEways: tales of EPEC, ATEC and EHEC. Cell Microbiol. 12:1544-52
81. Shapiro BJ, Friedman J, Cordero OX, Preheim SP, Timberlake SC, et al. 2012. Population genomics of early events in the ecological differentiation of bacteria. Science 336:48-51
82. Shikuma NJ, Pilhofer M, Weiss GL, Hadfield MG, Jensen GJ, Newman DK. 2014. Marine tubeworm metamorphosis induced by arrays of bacterial phage tail-like structures. Science 343:529-33
83. Stabb EV, Visick KL. 2013. Vibrio fischeri: a bioluminescent light-organ symbiont of the bobtail squid Euprymna scolopes. In The Prokaryotes, ed. E Rosenberg, EF DeLong, E Stackebrandt, S Lory, F Thompson, pp. 497-532. Berlin: Springer-Verlag
84. Stangherlin A, Reddy AB. 2013. Regulation of circadian clocks by redox homeostasis. J. Biol. Chem. 288:26505-11
85. Sycuro LK, Ruby EG, McFall-Ngai M. 2006. Confocal microscopy of the light organ crypts in juvenile Euprymna scolopes reveals their morphological complexity and dynamic function in symbiosis. J. Morphol. 267:555-68
86. Tong D, Rozas NS, Oakley TH, Mitchell J, Colley NJ, McFall-Ngai MJ. 2009. Evidence for light perception in a bioluminescent organ. Proc. Natl. Acad. Sci. USA 106:9836-41
87. Troll JV, Adin DM, Wier AM, Paquette N, Silverman N, et al. 2009. Peptidoglycan induces loss of a nuclear peptidoglycan recognition protein during host tissue development in a beneficial animal-bacterial symbiosis. Cell Microbiol. 11:1114-27
88. Vaishnava S, Yamamoto M, Severson KM, Ruhn KA, Yu X, et al. 2011. The antibacterial lectin RegIIIγ promotes the spatial segregation of microbiota and host in the intestine. Science 334:255-58
89. Vedam V, Haynes JG, Kannenberg EL, Carlson RW, Sherrier DJ. 2004. A Rhizobium leguminosarum lipopolysaccharide lipid-A mutant induces nitrogen-fixing nodules with delayed and defective bacteroid formation. Mol. Plant-Microbe Interact. 17:283-91
90. Visick KL. 2009. An intricate network of regulators controls biofilm formation and colonization by Vibrio fischeri. Mol. Microbiol. 74:782-89
91. Visick KL, Foster J,Doino J, McFall-Ngai M, Ruby EG. 2000. Vibrio fischeri lux genes play an important role in colonization and development of the host light organ. J. Bacteriol. 182:4578-86
92. Wang Y, Dunn AK,Wilneff J,McFall-Ngai MJ, Spiro S, Ruby EG. 2010. Vibrio fischeri flavohaemoglobin protects against nitric oxide during initiation of the squid-Vibrio symbiosis. Mol. Microbiol. 78:903-15
93. Wang Y, Ruby EG. 2011. The roles of NO in microbial symbioses. Cell Microbiol. 13:518-26
94. Wier AM, Nyholm SV, Mandel MJ, Massengo-Tiasse RP, Schaefer AL, 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 107:2259-64
95. WollenbergMS, Preheim SP, Polz MF, Ruby EG. 2012. Polyphyly of non-bioluminescent Vibrio fischeri sharing a lux-locus deletion. Environ. Microbiol. 14:655-68
96. Wollenberg MS, Ruby EG. 2009. Population structure of Vibrio fischeri within the light organs of Euprymna scolopes squid from two Oahu (Hawaii) populations. Appl. Environ. Microbiol. 75:193-202
97. Yip ES, Geszvain K, DeLoney-Marino CR, Visick KL. 2006. The symbiosis regulator RscS controls the syp gene locus, biofilm formation and symbiotic aggregation by Vibrio fischeri. Mol. Microbiol. 62:1586-600
98. Young RE, Roper CF. 1976. Bioluminescent countershading in midwater animals: evidence from living squid. Science 191:1046-48
99. Zilber-Rosenberg I, Rosenberg E. 2008. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol. Rev. 32:723-35