Cnidarian-microbe interactions and the origin of innate immunity in metazoans

Annual Review of Microbiology

Volumn 67, Issue , 2013, Pages 499-518

  Bosch, Thomas C G ^a  

^a UNIVERSITY OF KIEL   (Germany)

Author keywords

Antimicrobial peptides; Evolution; Hologenome theory of evolution; Host microbe interactions; Hydra; Innate immunity; Metaorganism; Transcription factor FoxO

Indexed keywords

EPIDERMAL GROWTH FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; MYELOID DIFFERENTIATION FACTOR 88; PATTERN RECOGNITION RECEPTOR; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN S 100; PSORIASIN; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR FOXO;

ADAPTIVE IMMUNITY; ADULT STEM CELL; ALPHAPROTEOBACTERIA; ANTHOZOA; ANTIMICROBIAL ACTIVITY; ARTEMIA SALINA; ARTICLE; BACTERIAL COLONIZATION; BACTEROIDETES; BETAPROTEOBACTERIA; BIOCHEMICAL COMPOSITION; BRAIN DEVELOPMENT; CHLORELLA; CNIDARIA; CUBOZOA; DELTAPROTEOBACTERIA; DEVELOPMENTAL STAGE; EMBRYO DEVELOPMENT; ENVIRONMENTAL CHANGE; ENVIRONMENTAL FACTOR; ENVIRONMENTAL STRESS; EXOSKELETON; EXPRESSED SEQUENCE TAG; EXTRACELLULAR MATRIX; GAMMAPROTEOBACTERIA; GENETIC CONSERVATION; GENETIC VARIABILITY; GENOME SIZE; GERM LINE; HIGH THROUGHPUT SEQUENCING; HOMEOSTASIS; HOST PATHOGEN INTERACTION; HYDRA; HYDROZOA; IMMUNE RESPONSE; INNATE IMMUNITY; INTESTINE EPITHELIUM; JELLYFISH; LARVAL STAGE; MATHEMATICAL MODEL; MICROBIAL COLONIZATION; MICROBIAL COMMUNITY; MICROFLORA; MUSCLE CELL; NEMATOSTELLA; NONHUMAN; OLIGOMERIZATION; PHENOTYPE; PHYLOGENETIC TREE; PRIORITY JOURNAL; PROMOTER REGION; SENSORY NERVE; SPIROCHETE; STEM CELL; TRANSPOSON;

ANIMALS; BACTERIA; CNIDARIA; HUMANS; IMMUNITY, INNATE; MICROBIOTA; RECEPTORS, PATTERN RECOGNITION; SYMBIOSIS;

EID: 84884520631     PISSN: 00664227     EISSN: 15453251     Source Type: Book Series    
DOI: 10.1146/annurev-micro-092412-155626     Document Type: Article

References (108)

1. Alegado RA, Brown LW, Cao S, Dermenjian RK, Zuzow R, et al. 2012. A bacterial sulfonolipid triggers multicellular development in the closest living relatives of animals. Elife 1:e00013
2. Augustin R, Anton-Erxleben F, Jungnickel S, Hemmrich G, Spudy B, et al. 2009. Activity of the novel peptide arminin against multiresistant human pathogens shows the considerable potential of phylogenetically ancient organisms as drug sources. Antimicrob. Agents Chemother. 53:5245-50
3. Augustin R, Fraune S, Bosch TCG. 2010. How Hydra senses and destroys microbes. Semin. Immunol. 22:54-58
4. Baliński A, Yuanlin S, Jerzy D. 2012. 470-million-year-old black corals from China. Naturwissenschaften 99(8):645-53
5. BarbeitosMS, Romano SL, LaskerHR. 2010. Repeated loss of coloniality and symbiosis in scleractinian corals. Proc. Natl. Acad. Sci. USA 107(26):11877-82
6. Baudisch A, Vaupel JW. 2012. Evolution. Getting to the root of aging. Science 338(6107):618-19
7. Baumgart DC, SandbornWJ. 2012. Crohn's disease. Lancet 380(9853):1590-605
8. Becker T, Loch G, Beyer M, Zinke I, Aschenbrenner AC, et al. 2010. FOXO-dependent regulation of innate immune homeostasis. Nature 463(7279):369-73
9. Bevins CL, Salzman NH. 2011. The potter's wheel: the host's role in sculpting its microbiota. Cell Mol. Life Sci. 68:3675-85
10. Boehm AM, Bosch TCG. 2012. Migration of multipotent interstitial stem cells in Hydra. Zoology 115(5):275-82
11. Boehm AM, Khalturin K, Anton-Erxleben F, Hemmrich G, Klostermeier UC, et al. 2012. FoxO is a critical regulator of stem cell maintenance in immortal Hydra. Proc. Natl. Acad. Sci. USA 109(48):19697-702
12. Bosch TCG. 2009. Hydra and the evolution of stem cells. BioEssays 31(4):478-86
13. Bosch TCG. 2012. Understanding complex host-microbe interactions in Hydra. Gut Microbes 3:345-51
14. Bosch TCG. 2012. What Hydra has to say about the role and origin of symbiotic interactions. Biol. Bull. 223:78-84
15. Bosch TCG, Anton-Erxleben F, Hemmrich G, Khalturin K. 2010. The Hydra polyp: nothing but an active stem cell community. Dev. Growth Differ. 52(1):15-25
16. Bosch TCG, Augustin R, Anton-Erxleben F, Fraune S, Hemmrich G, et al. 2009. Uncovering the evolutionary history of innate immunity: the simplemetazoan Hydra uses epithelial cells for host defence. Dev. Comp. Immunol. 33:559-69
17. Bosch TCG, David CN. 1984. Growth regulation in Hydra: relationship between epithelial cell cycle length and growth rate. Dev. Biol. 104:161-71
18. Bosch TCG, David CN. 1986. Male and female stem cells and sex reversal in Hydra polyps. Proc. Natl. Acad. Sci. USA 83:9478-82
19. Bosch TCG, McFall-Ngai MJ. 2011. Metaorganisms as the new frontier. Zoology 114:185-90
20. Bourne D, Iida Y, Uthicke S, Smith-Keune C. 2008. Changes in coral-associated microbial communities during a bleaching event. ISME J. 2:350-63
21. Broderick NA, Lemaitre B. 2012. Gut-associated microbes of Drosophila melanogaster. Gut Microbes 3(4):307-21
22. Capy P, Gasperi G, Biémont C, Bazin C. 2000. Stress and transposable elements: co-evolution or useful parasites? Heredity 85:101-6
23. Chapman JA, Kirkness EF, Simakov O, Hampson SE, Mitros T, et al. 2010. The dynamic genome of Hydra. Nature 464(7288):592-96
24. Collins AG, Cartwright P, McFaddenCS, Schierwater B. 2005. Phylogenetic context and basal metazoan model systems. Integr. Comp. Biol. 45(4):585-94
25. David CN. 2012. Interstitial stem cells in Hydra: multipotency and decision-making. Int. J. Dev. Biol. 56(6-8):489-97
26. Domazet-Lošo T, TautzD. 2008. An ancient evolutionary origin of genes associated with human genetic diseases. Mol. Biol. Evol. 25:2699-707
27. Fedoroff N. 2012. Transposable elements, epigenetics and genome evolution. Science 338:758-67
28. Flachsbart F, Caliebe A, Kleindorp R, Blanché H, von Eller-Eberstein H, et al. 2009. Association of FOXO3A variation with human longevity confirmed in German centenarians. Proc. Natl. Acad. Sci. USA 106(8):2700-5
29. Frank U, Leitz T, MüllerWA. 2001. The hydroid Hydractinia: a versatile, informative cnidarian representative. BioEssays 23:963-71
30. Franzenburg S, Fraune S, Altrock PM, Künzel S, Baines JF, et al. 2013. Bacterial colonization of Hydra hatchlings follows a robust temporal pattern. ISME J. 7:781-90
31. Franzenburg S, Fraune S, Künzel S, Baines JF, Domazet-Loso T, Bosch TCG. 2012. MyD88-deficient Hydra reveal an ancient function of TLR signaling in sensing bacterial colonizers. Proc. Natl. Acad. Sci. USA 109(47):19374-79
32. Fraune S, Abe Y, Bosch TCG. 2009. Disturbing epithelial homeostasis in the metazoan Hydra leads to drastic changes in associated microbiota. Environ. Microbiol. 11:2361-69
33. Fraune S, Augustin R, Anton-Erxleben F, Wittlieb J, Gelhaus C, et al. 2010. In an early branching metazoan, bacterial colonization of the embryo is controlled by maternal antimicrobial peptides. Proc. Natl. Acad. Sci. USA 107:18067-72
34. Fraune S, AugustinR, BoschTCG.2011. Embryo protection in contemporary immunology:why bacteria matter. Commun. Integr. 4:369-72
35. Fraune S, Bosch TCG. 2007. Long-term maintenance of species-specific bacterial microbiota in the basal metazoan Hydra. Proc. Natl. Acad. Sci. USA 104:13146-51
36. Fraune S, Bosch TCG. 2010. Why bacteria matter in animal development and evolution. BioEssays 32:571-80
37. Gilbert SF, Epel D. 2008. Ecological Developmental Biology. Sunderland, MA: Sinauer
38. Habetha M, Anton-Erxleben F, Neumann K, Bosch TCG. 2003. The Hydra viridis/Chlorella symbiosis. Growth and sexual differentiation in polyps without symbionts. Zoology 106(2):101-8
39. 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
40. Hemmrich G, Anokhin B, Zacharias H, Bosch TCG. 2007. Molecular phylogenetics in Hydra, a classical model in evolutionary developmental biology. Mol. Phylogenet. Evol. 44:281-90
41. Hemmrich G, Khalturin K, Boehm AM, Puchert M, Anton-Erxleben F, et al. 2012. Molecular signatures of the three stem cell lineages in Hydra and the emergence of stem cell function at the base of multicellularity. Mol. Biol. Evol. 29(11):3267-80
42. Hemmrich G, Miller DJ, Bosch TCG. 2007. The evolution of immunity: a low-life perspective. Trends Immunol. 28(10):449-54
43. Hughes DT, Sperandio V. 2008. Inter-kingdom signalling: communication between bacteria and their hosts. Nat. Rev. Microbiol. 6:111-20
44. Imler JL, Bulet P. 2005. Antimicrobial peptides in Drosophila: structures, activities and gene regulation. Chem. Immunol. Allergy 86:1-21
45. Jünger MA, Rintelen F, Stocker H, Wasserman JD, Végh M, et al. 2003. The Drosophila forkhead transcription factor FOXO mediates the reduction in cell number associated with reduced insulin signaling. J. Biol. 2(3):20
46. Keeling PJ, Palmer JD. 2008. Horizontal gene transfer in eukaryotic evolution. Nat. Rev. Genet. 9:605-18
47. Kenyon C. 2010. A pathway that links reproductive status to lifespan in Caenorhabditis elegans. Ann. N. Y. Acad. Sci. 1204:156-62
48. Khalturin K, Hemmrich G, Fraune S, Augustin R, Bosch TCG. 2009. More than just orphans: Are taxonomically restricted genes important in evolution? Trends Genet. 25(9):404-13
49. Knoll AH. 2003. Life on a Young Planet. Princeton, NJ: Princeton Univ. Press
50. Koren O, Rosenberg E. 2006. Bacteria associated with mucus and tissues of the coral Oculina patagonica in summer and winter. Appl. Environ. Microbiol. 72:5254-59
51. Kortschak RD, Samuel G, Saint R, Miller DJ. 2003. EST analysis of the cnidarian Acropora millepora reveals extensive gene loss and rapid sequence divergence in the model invertebrates. Curr. Biol. 13:2190-95
52. Kumar S, Ingle H, Prasad DV, Kumar H. 2013. Recognition of bacterial infection by innate immune sensors. Crit. Rev. Microbiol. 39:229-46
53. Lange C, Hemmrich G, Klostermeier UC, Löpez-Quintero JA, Miller DJ, et al. 2011. Defining the origins of the NOD-like receptor system at the base of animal evolution. Mol. Biol. Evol. 28:1687-702
54. Lee JH, Cho KS, Lee J, Yoo J, Lee J, Chung J. 2001. Diptericin-like protein: an immune response gene regulated by the anti-bacterial gene induction pathway in Drosophila. Gene 271(2):233-38
55. Leitz T, Wagner T. 1993. The marine bacterium Alteromonas espejiana induces metamorphosis of the hydroid Hydractinia echinata. Mar. Biol. 115:173-78
56. Li Y, Wang WJ, Cao H, Lu J, Wu C, et al. 2009. Genetic association of FOXO1A and FOXO3A with longevity trait in Han Chinese populations. Hum. Mol. Genet. 18(24):4897-904
57. Lin L, Hron JD, Peng SL. 2004. Regulation of NF-βB, Th activation, and autoinflammation by the forkhead transcription factor Foxo3a. Immunity 21(2):203-23
58. Littlefield CL. 1984. The interstitial cells control the sexual phenotype of heterosexual chimeras of Hydra. Dev. Biol. 102(2):426-32
59. Littlefield CL, Finkemeier C, Bode HR. 1991. Spermatogenesis in Hydra oligactis. II. How temperature controls the reciprocity of sexual and asexual reproduction. Dev. Biol. 146(2):292-300
60. Martin VJ, Littlefield CL, Archer WE, Bode HR. 1997. Embryogenesis in Hydra. Biol. Bull. 192(3):345-63
61. MartíNez DE. 1998. Mortality patterns suggest lack of senescence in Hydra. Exp. Gerontol. 33(3):217-25
62. McClintock B. 1984. The significance of responses of the genome to challenge. Science 226:792-801
63. McFall-Ngai M. 2007. Adaptive immunity: care for the community. Nature 445(7124):153
64. McFall-Ngai M, Hadfield MG, Bosch TC, Carey HV, Domazet-Lošo T, et al. 2013. Animals in a bacterial world: a new imperative for the life sciences. Proc. Natl. Acad. Sci. USA 110:3229-36
65. Meyer JE, Harder J, Sipos B, Maune S, Kl öppel G, et al. 2008. Psoriasin (S100A7) is a principal antimicrobial peptide of the human tongue. Mucosal Immunol. 1(3):239-43
66. Miller DJ, Ball EE. 2008. Cryptic complexity captured: The Nematostella genome reveals its secrets. Trends Genet. 24(1):1-4
67. Miller DJ, Ball EE, TechnauU. 2005. Cnidarians and ancestral genetic complexity in the animal kingdom. Trends Genet. 21:536-39
68. Miller DJ, Hemmrich G, Ball EE, HaywardDC, Khalturin K, et al. 2007. The innate immune repertoire in Cnidaria-ancestral complexity and stochastic gene loss. Genome Biol. 8(4):R59
69. Miyamoto K, Araki KY, Naka K, Arai F, Takubo K, et al. 2007. Foxo3a is essential for maintenance of the hematopoietic stem cell pool. Cell Stem Cell 1(1):101-12
70. Muscatine L, Lenhoff HM. 1963. Symbiosis: on the role of algae symbiotic with Hydra. Science 142:956-58
71. Nebel A, Bosch TCG. 2012. Evolution of human longevity: lessons from Hydra. Aging 4(11):730-31
72. Nichols SA, DayelMJ, King N. 2009. Genomic, phylogenetic, and cell biological insights into metazoan origins. In Animal Evolution:Genes, Genomes, Fossils and Trees, ed.MJTelford, DTJLittlewood, pp. 24-32. Oxford: Oxford Univ. Press
73. Nyholm SV, Graf J. 2012. Knowing your friends: Invertebrate innate immunity fosters beneficial bacterial symbioses. Nat. Rev. Microbiol. 10(12):815-27
74. O'Brien TL. 1982. Inhibition of vacuolar membrane fusion by intracellular symbiotic algae in Hydra viridis (Florida strain). J. Exp. Zool. 223(3):211-18
75. Ochman H, WorobeyM, Kuo CH, Ndjango JB, PeetersM, et al. 2010. Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol. 8(11):e1000546
76. O'Hara AM, Shanahan F. 2006. The gut flora as a forgotten organ. EMBO Rep. 7:688-93
77. Ovchinnikova TV, Balandin SV, Aleshina GM, Tagaev AA, Leonova YF, et al. 2006. Aurelin, a novel antimicrobial peptide from jellyfish Aurelia aurita with structural features of defensins and channelblocking toxins. Biochem. Biophys. Res. Commun. 348(2):514-23
78. Paik JH, Ding Z, Narurkar R, Ramkissoon S, Muller F, et al. 2009. FoxOs cooperatively regulate diverse pathways governing neural stem cell homeostasis. Cell Stem Cell 5(5):540-53
79. Pantos O, Cooney RP, Le Tissier MD, Barer MR, O'Donnell AG, et al. 2003. The bacterial ecology of a plague-like disease affecting the Caribbean coral Montastrea annularis. Environ. Microbiol. 5:370-82
80. Piskurek O, Jackson DJ. 2012. Transposable elements: from DNA parasites to architects of metazoan evolution. Genes 3:409-22
81. Pradeu T. 2011. A mixed self: the role of symbiosis in development. Biol. Theory 6:80-88
82. Putnam NH, Srivastava M, Hellsten U, Dirks B, Chapman J, et al. 2007. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317:86-94
83. Renault VM, Rafalski VA, Morgan AA, Salih DA, Brett JO, et al. 2009. FoxO3 regulates neural stem cell homeostasis. Cell Stem Cell 5(5):527-39
84. Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E. 2006. The coral probiotic hypothesis. Environ. Microbiol. 8:2068-73
85. Ritchie KB, Smith WG. 1995. Carbon-source utilization of coral-associated marine heterotrophs. J. Mar. Biotechnol. 3:107-9
86. Rohwer F, Seguritan V, Azam F, Knowlton N. 2002. Diversity and distribution of coral-associated bacteria. Mar. Ecol. Prog. Ser. 243:1-10
87. Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I. 2007. The role of microorganisms in coral health, disease and evolution. Nat. Rev. Microbiol. 5:355-62
88. RosenbergE, SharonG, Zilber-Rosenberg I. 2009.Thehologenome theory of evolution containsLamarckian aspects within a Darwinian framework. Environ. Microbiol. 11(12):2959-62
89. Rosenstiel P, Philipp EE, Schreiber S, Bosch TCG. 2009. Evolution and function of innate immune receptors-insights from marine invertebrates. J. Innate Immun. 1:291-300
90. Salih DA, Brunet A. 2008. FoxO transcription factors in the maintenance of cellular homeostasis during aging. Curr. Opin. Cell Biol. 20(2):126-36
91. Salzman NH, Hung K, Haribhai D, Chu H, Karlsson-Sjoberg J, et al. 2010. Enteric defensins are essential regulators of intestinal microbial ecology. Nat. Immunol. 11:76-83
92. Shenkarev ZO, Panteleev PV, Balandin SV, Gizatullina AK, Altukhov DA, et al. 2012. Recombinant expression and solution structure of antimicrobial peptide aurelin from jellyfish Aurelia aurita. Biochem. Biophys. Res. Commun. 429(1-2):63-69
93. ShinzatoC, Shoguchi E, KawashimaT, HamadaM, HisataK, et al. 2011. Using the Acropora digitifera genome to understand coral responses to environmental change. Nature 476(7360):320-23
94. Snoeks L, Weber CR, Wasland K, Turner JR, Vainder C, et al. 2009. Tumor suppressor FOXO3 participates in the regulation of intestinal inflammation. Lab. Invest. 89(9):1053-62
95. Steele RE, David CN, Technau U. 2011. A genomic view of 500 million years of cnidarian evolution. Trends Genet. 27(1):7-13
96. Stolarski J, Kitahara MV, Miller DJ, Cairns SD, Mazur M, Meibom A. 2011. The ancient evolutionary origins of Scleractinia revealed by azooxanthellate corals. BMC Evol. Biol. 11:316
97. Takeuchi O, Akira S. 2010. Pattern recognition receptors and inflammation. Cell 140(6):805-20
98. Tardent P, Holstein T. 1982. Morphology and morphodynamics of the stenotele nematocyst of Hydra attenuata Pall (Hydrozoa, Cnidaria). Cell Tissue Res. 224(2):269-90
99. Technau U, Rudd S, Maxwell P. 2005. Maintenance of ancestral complexity and non-metazoan genes in two basal cnidarians. Trends Genet. 21:633-39
100. Thorington G, Margulis L. 1981. Hydra viridis: transfer of metabolites between Hydra and symbiotic algae. Biol. Bull. 160:175-88
101. Tothova Z, Gilliland DG. 2007. FoxO transcription factors and stem cell homeostasis: insights from the hematopoietic system. Cell Stem Cell 1(2):140-52
102. Travis J. 2009. On the origin of the immune system. Science 324(5927):580-82
103. WaltherM, Ulrich R, KroiherM, Berking S. 1996. Metamorphosis and pattern formation in Hydractinia echinata, a colonial hydroid. Int. J. Dev. Biol. 40:313-22
104. Wehkamp J, Salzman NH, Porter E, Nuding S, Weichenthal M, Petras RE. 2005. Reduced Paneth cell α-defensins in ileal Crohn's disease. Proc. Natl. Acad. Sci. USA 102:18129-34
105. Wittlieb J, Khalturin K, Lohmann JU, Anton-Erxleben F, Bosch TCG. 2006. Transgenic Hydra allow in vivo tracking of individual stem cells during morphogenesis. Proc. Natl. Acad. Sci. USA 103(16):6208-11
106. Zacharias H, Anokhin B, Khalturin K, Bosch TCG. 2004. Genome sizes and chromosomes in the basal metazoan Hydra. Zoology 107(3):219-27
107. ZhangX, Yalcin S, LeeDF, YehTY, Lee SM, et al. 2011.FOXO1is an essential regulator of pluripotency in human embryonic stem cells. Nat. Cell Biol. 13(9):1092-99
108. 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