Bacterial bioluminescence regulates expression of a host cryptochrome gene in the squid-vibrio symbiosis

mBio

Volumn 4, Issue 2, 2013, Pages

  Heath Heckman, Elizabeth A C ^a   Peyer, Suzanne M ^a   Whistler, Cheryl A ^b   Apicella, Michael A ^c   Goldman, William E ^d   McFall Ngai, Margaret J ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF NEW HAMPSHIRE   (United States)

^c UNIVERSITY OF IOWA   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

CRYPTOCHROME; LIPID A; PEPTIDOGLYCAN;

ANIMAL TISSUE; ARTICLE; BACTERIAL BIOLUMINESCENCE; BACTERIAL COLONIZATION; BIOLUMINESCENCE; CIRCADIAN RHYTHM; COLOR; CONTROLLED STUDY; CRY GENE; CRYPTOCHROME GENE; ESCRY1 GENE; ESCRY2 GENE; EUPRYMNA SCOLOPES; GENE EXPRESSION REGULATION; HEAD; LIGHT; NONHUMAN; PRIORITY JOURNAL; SQUID; SYMBIOSIS; TRANSCRIPTION REGULATION; VIBRIO FISCHERI; ALIIVIBRIO FISCHERI; ANIMAL; BIOSYNTHESIS; CEPHALOPOD; ENZYMOLOGY; GENETICS; LUMINESCENCE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; RADIATION EXPOSURE;

ALIIVIBRIO FISCHERI; ANIMALS; CRYPTOCHROMES; DECAPODIFORMES; GENE EXPRESSION REGULATION; LUMINESCENCE; SYMBIOSIS;

EID: 84880038226     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00167-13     Document Type: Article

References (64)

1. Keller M, Mazuch J, Abraham U, Eom GD, Herzog ED, Volk HD, Kramer A, Maier B. 2009. A circadian clock in macrophages controls inflammatory immune responses. Proc. Natl. Acad. Sci. U. S. A. 106: 21407-21412
2. Lee JE, Edery I. 2008. Circadian regulation in the ability of Drosophila to combat pathogenic infections. Curr. Biol. 18:195-199
3. Silver AC, Arjona A, Walker WE, Fikrig E. 2012. The circadian clock controls Toll-like receptor 9-mediated innate and adaptive immunity. Immunity 36:251-261
4. Wang W, Barnaby JY, Tada Y, Li H, Tör M, Caldelari D, Lee DU, Fu XD, Dong X. 2011. Timing of plant immune responses by a central circadian regulator. Nature 470:110-114
5. Hooper LV, Littman DR, Macpherson AJ. 2012. Interactions between the microbiota and the immune system. Science 336:1268-1273
6. Konturek PC, Brzozowski T, Konturek SJ. 2011. Gut clock: implication of circadian rhythms in the gastrointestinal tract. J. Physiol. Pharmacol. 62:139-150
7. Douris N, Kojima S, Pan X, Lerch-Gaggl AF, Duong SQ, Hussain MM, Green CB. 2011. Nocturnin regulates circadian trafficking of dietary lipid in intestinal enterocytes. Curr. Biol. 21:1347-1355
8. Froy O, Chapnik N. 2007. Circadian oscillation of innate immunity components in mouse small intestine. Mol. Immunol. 44:1954-1960
9. Hoogerwerf WA, Sinha M, Conesa A, Luxon BA, Shahinian VB, Cornélissen G, Halberg F, Bostwick J, Timm J, Cassone VM. 2008. Transcriptional profiling of mRNA expression in the mouse distal colon. Gastroenterology 135:2019-2029
10. Lamia KA, Papp SJ, Yu RT, Barish GD, Uhlenhaut NH, Jonker JW, Downes M, Evans RM. 2011. Cryptochromes mediate rhythmic repression of the glucocorticoid receptor. Nature 480:552-556
11. Tahira K, Ueno T, Fukuda N, Aoyama T, Tsunemi A, Matsumoto S, Nagura C, Matsumoto T, Soma M, Shimba S, Matsumoto Y. 2011. Obesity alters the expression profile of clock genes in peripheral blood mononuclear cells. Arch. Med. Sci. 7:933-940
12. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. 2006. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027-1031
13. Velagapudi VR, Hezaveh R, Reigstad CS, Gopalacharyulu P, Yetukuri L, Islam S, Felin J, Perkins R, Borén J, Oresic M, Bäckhed F. 2010. The gut microbiota modulates host energy and lipid metabolism in mice. J. Lipid Res. 51:1101-1112
14. Foster RG, Helfrich-Förster C. 2001. The regulation of circadian clocks by light in fruitflies and mice. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356:1779-1789
15. Reitzel AM, Behrendt L, Tarrant AM. 2010. Light entrained rhythmic gene expression in the sea anemone Nematostella vectensis: the evolution of the animal circadian clock. PLoS One 5:e12805.http://dx.doi.org/10.1371/journal.pone.0012805
16. Yuan Q, Metterville D, Briscoe AD, Reppert SM. 2007. Insect cryptochromes: gene duplication and loss define diverse ways to construct insect circadian clocks. Mol. Biol. Evol. 24:948-955
17. Oztürk N, Song SH, Ozgür S, Selby CP, Morrison L, Partch C, Zhong D, Sancar A. 2007. Structure and function of animal cryptochromes. Cold Spring Harb. Symp. Quant. Biol. 72:119-131
18. Zoltowski BD, Vaidya AT, Top D, Widom J, Young MW, Crane BR. 2011. Structure of full-length Drosophila cryptochrome. Nature 480: 396-399
19. Zhu H, Sauman I, Yuan Q, Casselman A, Emery-Le M, Emery P, Reppert SM. 2008. Cryptochromes define a novel circadian clock mechanism in monarch butterflies that may underlie sun compass navigation. PLoS Biol. 6:e4. http://dx.doi.org/10.1371/journal.pbio.0060004
20. Ikeno T, Katagiri C, Numata H, Goto SG. 2011. Causal involvement of mammalian-type cryptochrome in the circadian cuticle deposition rhythm in the bean bug Riptortus pedestris. Insect Mol. Biol. 20:409-415
21. Ikeno T, Numata H, Goto SG. 2008. Molecular characterization of the circadian clock genes in the bean bug, Riptortus pedestris, and their expression patterns under long-and short-day conditions. Gene 419:56-61
22. Ikeno T, Numata H, Goto SG. 2011. Photoperiodic response requires mammalian-type cryptochrome in the bean bug Riptortus pedestris. Biochem. Biophys. Res. Commun. 410:394-397
23. Merlin C, Beaver LE, Taylor OR, Wolfe SA, Reppert SM. 2013. Efficient targeted mutagenesis in the monarch butterfly using zinc-finger nucleases. Genome Res. 23:159-168
24. Müller WE, Wang X, Schröder HC, Korzhev M, Grebenjuk VA, Markl JS, Jochum KP, Pisignano D, Wiens M. 2010. A cryptochrome-based photosensory system in the siliceous sponge Suberites domuncula (Demospongiae). FEBS J. 277:1182-1201
25. Connor KM, Gracey AY. 2011. Circadian cycles are the dominant transcriptional rhythm in the intertidal mussel Mytilus californianus, Proc. Natl. Acad. Biol. U. S. A. 108:16110-16115
26. Wier AM, Nyholm SV, Mandel MJ, Massengo-Tiassé RP, Schaefer AL, Koroleva I, Splinter-BonDurant S, Brown B, Manzella L, Snir E, Almabrazi H, Scheetz TE, Bonaldo MDF, Casavant TL, Soares MB, Cronan JE, Reed JL, Ruby EG, McFall-Ngai MJ. 2010. Transcriptional patterns in both host and bacterium underlie a daily rhythm of anatomical and metabolic change in a beneficial symbiosis. Proc. Natl. Acad. Biol. U. S. A., 107:2259-2264
27. Jones BW, Nishiguchi MK. 2004. Counterillumination in the Hawaiian bobtail squid, Euprymna scolopes Berry (Mollusca: Cephalopoda). Mar. Biol. 144:1151-1155
28. 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. Biol. U. S. A. 106:9836-9841
29. 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. 182:4578-4586
30. Koropatnick TA, Engle JT, Apicella MA, Stabb EV, Goldman WE, McFall-Ngai MJ. 2004. Microbial factor-mediated development in a hostbacterial mutualism. Science 306:1186-1188
31. Chun CK, Troll JV, Koroleva I, Brown B, Manzella L, Snir E, Almabrazi H, Scheetz TE, Bonaldo MDF, Casavant TL, Soares MB, Ruby EG, McFall-Ngai MJ. 2008. Effects of colonization, luminescence, and autoinducer on host transcription during development of the squid-vibrio association. Proc. Natl. Acad. Sci. U. S. A. 105:11323-11328
32. 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. A 179:65-73
33. Chun CK, Scheetz TE, Bonaldo MDF, Brown B, Clemens A, Crookes-Goodson WJ, Crouch K, DeMartini T, Eyestone M, Goodson MS, Janssens B, Kimbell JL, Koropatnick TA, Kucaba T, Smith C, Stewart JJ, Tong D, Troll JV, Webster S, Winhall-Rice J, Yap C, Casavant TL, McFall-Ngai MJ, Soares MB. 2006. An annotated cDNA library of juvenile Euprymna scolopes with and without colonization by the symbiont Vibrio fischeri. BMC Genomics 7:154. http://dx.doi.org/10.1186/1471-2164-7-154
34. Chaves I, Pokorny R, Byrdin M, Hoang N, Ritz T, Brettel K, Essen LO, van der Horst GT, Batschauer A, Ahmad M. 2011. The cryptochromes: blue light photoreceptors in plants and animals. Annu. Rev. Plant Biol. 62:335-364
35. Sanada K, Harada Y, Sakai M, Todo T, Fukada Y. 2004. Serine phosphorylation of mCRY1 and mCRY2 by mitogen-activated protein kinase. Genes Cells 9:697-708
36. Graf J, Ruby EG. 1998. Host-derived amino acids support the proliferation of symbiotic bacteria. Proc. Natl. Acad. Sci. U. S. A. 95:1818-1822
37. Glossop NR, Hardin PE. 2002. Central and peripheral circadian oscillator mechanisms in flies and mammals. J. Cell Sci. 115:3369-3377
38. Fanjul-Moles ML, Escamilla-Chimal EG, Gloria-Osorio A, Hernández-Herrera G. 2004. The crayfish Procambarus clarkii CRY shows daily and circadian variation. J. Exp. Biol. 207:1453-1460
39. Whistler CA, Koropatnick TA, Pollack A, McFall-Ngai MJ, Ruby EG. 2007. The GacA global regulator of Vibrio fischeri is required for normal host tissue responses that limit subsequent bacterial colonization. Cell. Microbiol. 9:766-778
40. Levy O, Appelbaum L, Leggat W, Gothlif Y, Hayward DC, Miller DJ, Hoegh-Guldberg O. 2007. Light-responsive cryptochromes from a simple multicellular animal, the coral Acropora Millepora. Science 318:467-470
41. Merlin C, Gegear RJ, Reppert SM. 2009. Antennal circadian clocks coordinate sun compass orientation in migratory monarch butterflies. Science 325:1700-1704
42. Gegear RJ, Foley LE, Casselman A, Reppert SM. 2010. Animal cryptochromes mediate magnetoreception by an unconventional photochemical mechanism. Nature 463:804-807
43. Song SH, Oztürk N, Denaro TR, Arat NO, Kao YT, Zhu H, Zhong D, Reppert SM, Sancar A. 2007. Formation and function of flavin anion radical in cryptochrome 1 blue-light photoreceptor of monarch butterfly. J. Biol. Chem. 282:17608-17612
44. Hughes ME, DiTacchio L, Hayes KR, Vollmers C, Pulivarthy S, Baggs JE, Panda S, Hogenesch JB. 2009. Harmonics of circadian gene transcription in mammals. PLoS Genet. 5:e1000442. http://dx.doi.org/10.1371/journal.pgen.1000442
45. Narasimamurthy R, Hatori M, Nayak SK, Liu F, Panda S, Verma IM. 2012. Circadian clock protein cryptochrome regulates the expression of proinflammatory cytokines. Proc. Natl. Acad. Sci. U. S. A. 109: 12662-12667
46. Damiola F, Le Minh N, Preitner N, Kornmann B, Fleury-Olela F, Schibler U. 2000. Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev. 14:2950-2961
47. Johnson BC. 1992. Nutrient intake as a time signal for circadian rhythm. J. Nutr. 122:1753-1759
48. Wen L, Ley RE, Volchkov PY, Stranges PB, Avanesyan L, Stonebraker AC, Hu C, Wong FS, Szot GL, Bluestone JA, Gordon JI, Chervonsky AV. 2008. Innate immunity and intestinal microbiota in the development of type 1 diabetes. Nature 455:1109-1113
49. Manco M, Putignani L, Bottazzo GF. 2010. Gut microbiota, lipopolysaccharides, and innate immunity in the pathogenesis of obesity and cardiovascular risk. Endocr. Rev. 31:817-844
50. Holzer P, Reichmann F, Farzi A. 2012. Neuropeptide Y, Peptide YY and pancreatic polypeptide in the gut-brain axis. Neuropeptides 46:261-274
51. Gonzalez A, Stombaugh J, Lozupone C, Turnbaugh PJ, Gordon JI, Knight R. 2011. The mind-body-microbial continuum. Dialogues Clin. Neurosci. 13:55-62
52. Tremaroli V, Bäckhed F. 2012. Functional interactions between the gut microbiota and host metabolism. Nature 489:242-249
53. Montgomery MK, McFall-Ngai MJ. 1993. Embryonic development of the light organ of the sepiloid squid Euprymna scolopes Berry. Biol. Bull. 184:296-308
54. Boettcher KJ, Ruby EG. 1990. Depressed light emission by symbiotic Vibrio fischeri of the sepiolid squid Euprymna scolopes. J. Bacteriol. 172: 3701-3706
55. Bose JL, Rosenberg CS, Stabb EV. 2008. Effects of luxCDABEG induction in Vibrio fischeri: enhancement of symbiotic colonization and conditional attenuation of growth in culture. Arch. Microbiol. 190:169-183
56. Hastings JW, Riley WH, Massa J. 1965. The purification, properties, and chemiluminescent quantum yield of bacterial luciferase. J. Biol. Chem. 240:1473-1481
57. Foster JS, Apicella MA, McFall-Ngai MJ. 2000. Vibrio fischeri lipopolysaccharide induces developmental apoptosis, but not complete morphogenesis, of the Euprymna scolopes symbiotic light organ. Dev. Biol. 226: 242-254
58. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410
59. Edgar RC. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113. http://dx.doi.org/10.1186/1471-2105-5-113
60. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm toestimate large phylogenies by maximum likelihood. Syst. Biol. 52: 696-704
61. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT. 2009. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55:611-622
62. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.http://dx.doi.org/10.1093/nar/29.9.e45
63. Troll JV, Bent EH, Pacquette N, Wier AM, Goldman WE, Silverman N, McFall-Ngai MJ. 2010. Taming the symbiont for coexistence: a host PGRP neutralizes a bacterial symbiont toxin. Environ. Microbiol. 12: 2190-2203
64. Troll JV, Adin DM, Wier AM, Paquette N, Silverman N, Goldman WE, Stadermann FJ, Stabb EV, McFall-Ngai MJ. 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.