Bacterial Influences on Animal Origins

Cold Spring Harbor Perspectives in Biology

Volumn 6, Issue 11, 2014, Pages

  Alegado, Rosanna A ^a   King, Nicole ^b  

^a UNIVERSITY OF HAWAII   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; BACTERIA (MICROORGANISMS);

ANIMAL; BACTERIUM; CELL ADHESION; CHOANOFLAGELLATE; EUKARYOTE; EVOLUTION; GENETICS; METABOLISM; PHAGOCYTOSIS; PHYLOGENY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; BACTERIA; BIOLOGICAL EVOLUTION; CELL ADHESION; CHOANOFLAGELLATA; EUKARYOTA; PHAGOCYTOSIS; PHYLOGENY; SIGNAL TRANSDUCTION;

EID: 84908430749     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a016162     Document Type: Article

References (180)

1. Abedin M, King N. 2008. The premetazoan ancestry of cadherins. Science 319: 946-948.
2. Adamska M, Matus DQ, Adamski M, Green K, Rokhsar DS, Martindale MQ, Degnan BM. 2007. The evolutionary origin of hedgehog proteins. Curr Biol 17: R836-R837.
3. Alegado RA, Brown LW, Cao S, Dermenjian RK, Zuzow R, Fairclough SR, Clardy J, King N. 2012. A bacterial sulfonolipid triggers multicellular development in the closest living relatives of animals. eLife 1: e00013.
4. Alegado RA, Grabenstatter JD, Zuzow R, Morris A, Huang SY, Summons RE, King N. 2013. Algoriphagus machipongonensis sp. nov., co-isolated with a colonial choanoflagellate. Int J Syst Evol Microbiol 63: 163-168.
5. Allwood AC, Walter MR, Burch IW, Kamber BS. 2007. 3.43 billion-year-old stromatolite reef from the Pilbara Craton ofWestern Australia: Ecosystem-scale insights to early life on Earth. Precamb Res 158: 198-227.
6. Awramik SM. 1971. Precambrian columnar stromatolite diversity: Reflection of metazoan appearance. Science 174: 825-827.
7. Bapteste E, Moreira D, Philippe H. 2003. Rampant horizontal gene transfer and phospho-donor change in the evolution of the phosphofructokinase. Gene 318: 185-191.
8. Baronio M, Lattanzio VMT, Vaisman N, Oren A, Corcelli A. 2010. The acylhalocapnines of halophilic bacteria: Structural details of unusual sulfonate sphingoids. J Lipid Res 51: 1878-1885.
9. Bates JM, Mittge E, Kuhlman J, Baden KN, Cheesman SE, Guillemin K. 2006. Distinct signals from the microbiota promote different aspects of zebrafish gut differentiation. Dev Biol 297: 374-386.
10. Batrakov SG, Nikitin DI, Sheichenko VI, Ruzhitsky AO. 1998. A novel sulfonic-acid analogue of ceramide is the major extractable lipid of the gram-negative marine bacterium Cyclobacterium marinus WH. Biochim Biophys Acta 1391: 79-91.
11. Batrakov SG, Sheichenko VI, Nikitin DI. 1999. A novel glycosphingolipid from gram-negative aquatic bacteria. Biochim Biophys Acta 1440: 163-175.
12. Baumann P. 2005. Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu Rev Microbiol 59: 155-189.
13. Bertrand JF, Woollacott RM. 2003. G protein-linked receptors and induction of metamorphosis in Bugula stolonifera (Bryozoa). Invert Biol 122: 380-385.
14. Beutler B. 2004. Innate immunity: An overview. Mol Immunol 40: 845-859.
15. Bierne H, Hamon M, Cossart P. 2012. Epigenetics and bacterial infections. Cold Spring Harb Perspect Med 2: a010272.
16. Bonner J. 1998. The origins of multicellularity. Integr Biol 1: 27-36.
17. Bottjer DJ. 2005. Geobiology and the fossil record: Eukaryotes, microbes, and their interactions. Palaeogeography, Palaeoclimatology, Palaeoecology 219: 5-21.
18. Brusca RC, Brusca GJ. 2002. Invertebrates. Sinauer, Sunderland, MA. Budd GE, Jensen S. 2000. A critical reappraisal of the fossil record of the bilaterian phyla. Biol Rev Camb Philos Soc 75: 253-295.
19. Buss LW. 1987. The evolution of individiuality. Princeton University Press, Princeton, NJ.
20. Butterfield NJ. 2000. Bangiomorpha pubescens n. gen., n. sp.: Implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology 26: 386-404.
21. Byrum CA, Martindale MQ. 2004. Gastrulation in the Cnidaria and Ctenophora. In Gastrulation from cells to embryos. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 33-50.
22. Canfield DE, Poulton SW, Narbonne GM. 2007. Late-neoproterozoic deep-ocean oxygenation and the rise of animal life. Science 315: 92-95.
23. Canfield DE, Poulton SW, Knoll AH, Narbonne GM, Ross G, Goldberg T, Strauss H. 2008. Ferruginous conditions dominated later neoproterozoic deep-water chemistry. Science 321: 949-952.
24. Canfield DE, Ngombi-Pemba L, Hammarlund EU, Bengtson S, Chaussidon M, Gauthier-Lafaye F, Meunier A, Riboulleau A, Rollion-Bard C, Rouxel O, et al. 2013. Oxygen dynamics in the aftermath of the Great Oxidation of Earth’s atmosphere. Proc Natl Acad Sci 110: 16736-16741.
25. Carlson JG, Handel MA. 1988. Intercellular bridges and factors determining their patterns in the grasshopper testis. J Morphol 196: 173-185.
26. Carr M, Leadbeater BSC, Hassan R, Nelson M, Baldauf SL. 2008. Molecular phylogeny of choanoflagellates, the sister group to Metazoa. Proc Natl Acad Sci 105: 16641-16646.
27. Cavalier-Smith T. 2009. Predation and eukaryote cell origins: Acoevolutionary perspective. Int J Biochem Cell Biol 41: 307-322.
28. Cox CJ, Foster PG, Hirt RP, Harris SR, Embley TM. 2008. The archaebacterial origin of eukaryotes. Proc Natl Acad Sci 105: 20356-20361.
29. Dayel MJ, Alegado RA, Fairclough SR, Levin TC, Nichols SA, McDonald K, King N. 2011. Cell differentiation and morphogenesis in the colony-forming choanoflagellate Salpingoeca rosetta. Dev Biol 357: 73-82.
30. Degnan BM, Leys SP, Larroux C. 2005. Sponge development and antiquity of animal pattern formation. Integr Comp Biol 45: 335-341.
31. deMendoza A, Suga H, Ruiz-Trillo I. 2010. Evolution of the MAGUK protein gene family in premetazoan lineages. BMC Evol Biol 10: 93.
32. Dobretsov S, Qian P-Y. 2006. Facilitation and inhibition of larval attachment of the bryozoan Bugula neritina in association with mono-species and multi-species biofilms. J Exp Marine Biol Ecol 333: 263-274.
33. Doolittle WF. 1998. You are what you eat: A gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet 14: 307-311.
34. Dornbos SQ, Bottjer DJ, Chen J-Y. 2004. Evidence for seafloor microbial mats and associated metazoan lifestyles in Lower Cambrian phosphorites of Southwest China. LETHAIA 37: 127-138.
35. Douzery EJP, Snell EA, Bapteste E, Delsuc F, Philippe H. 2004. The timing of eukaryotic evolution: Does a relaxed molecular clock reconcile proteins and fossils? Proc Natl Acad Sci 101: 15386-15391.
36. Drijber R, McGill W. 1994. Sulfonolipid content of cytophaga and flexibacter species isolated from soil and cultured under different nutrient and temperature regimes. Can J Microbiol 40: 132-139.
37. El Albani A, Bengtson S, Canfield DE, Bekker A, Macchiarelli R, Mazurier A, Hammarlund EU, Boulvais P, Dupuy J-J, Fontaine C, et al. 2010. Large colonial organisms with coordinated growth in oxygenated environments 2.1 Gyr ago. Nature 466: 100-104.
38. Embley TM, Martin W. 2006. Eukaryotic evolution, changes and challenges. Nat Cell Biol 440: 623-630.
39. Erwin DH. 1993. The origin of metazoan development: A palaeobiological perspective. Biol J Linnean Soc 50: 255-274.
40. Erwin DH, Laflamme M, Tweedt SM, Sperling EA, Pisani D, Peterson KJ. 2011. The Cambrian conundrum: Early divergence and later ecological success in the early history of animals. Science 334: 1091-1097.
41. Fairclough SR, Dayel MJ, King N. 2010.Multicellular development in a choanoflagellate. Curr Biol 20: R875-R876.
42. Fairclough SR, Chen Z, Kramer E, Zeng Q, Young S, Robertson HM, Begovic E, Richter DJ, Russ C, Westbrook MJ, et al. 2013. Premetazoan genome evolution and the regulation of cell differentiation in the choanoflagellate Salpingoeca rosetta. Genome Biol 14: R15.
43. Falk P, Roth KA, Gordon JI. 1994. Lectins are sensitive tools for defining the differentiation programs of mouse gut epithelial cell lineages. Am J Physiol 266: G987-G1003.
44. Falk PG, Hooper LV, Midtvedt T, Gordon JI. 1998. Creating and maintaining the gastrointestinal ecosystem:What we know and need to know from gnotobiology. Microbiol Mol Biol Rev 62: 1157-1170.
45. Fjerdingstad EJ. 1961. The ultrastructure of choanocyte collars in Spongilla lacustris (L.). Z Zellforschung 53: 645-657.
46. Foe VE, Alberts BM. 1983. Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J Cell Sci 61: 31-70.
47. Fraune S, Bosch TCG. 2010.Why bacteria matter in animal development and evolution. Bioessays 32: 571-580.
48. Fujiwara N, Porcelli SA, Naka T, Yano I, Maeda S, Kuwata H, Akira S, Uematsu S, Takii T, Ogura H, et al. 2013. Bacterial sphingophospholipids containing non-hydroxy fatty acid activate murine macrophages via Toll-like receptor 4 and stimulate bacterial clearance. Biochim Biophys Acta 1831: 1177-1184.
49. Gaidos E, Dubuc T, Dunford M, McAndrew P, Padilla-Gamino J, Studer B, Weersing K, Stanley S. 2007. The Precambrian emergence of animal life: A geobiological perspective. Geobiology 5: 351-373.
50. Garrett P. 1970. Phanerozoic stromatolites: Noncompetitive ecologic restriction by grazing and burrowing animals. Science 169: 171-173.
51. Gilbert SF, Sapp J, Tauber AI. 2012. A symbiotic view of life: We have never been individuals. Q Rev Biol 87: 325-341.
52. Godchaux W, Leadbetter ER. 1984. Sulfonolipids of gliding bacteria. Structure of the N-acylaminosulfonates. J Biol Chem 259: 2982-2990.
53. Goldberg WM, Taylor GT. 1989a. Cellular structure and ultrastructure of the black coral Antipathes aperta: 1. Organization of the tentacular epidermis and nervous system. J Morphol 202: 239-253.
54. Goldberg WM, Taylor GT. 1989b. Cellular structure and ultrastructure of the black coral Antipathes aperta: 2. The gastrodermis and its collar cells. J Morphol 202: 255-269.
55. Gonobobleva E, Maldonado M. 2009. Choanocyte ultrastructure in Halisarca dujardini (Demospongiae, Halisarcida). J Morphol 270: 615-627.
56. Greenbaum MP, Ma L, Matzuk MM. 2007. Conversion of midbodies into germ cell intercellular bridges. Dev Biol 305: 389-396.
57. Grosberg RK, Strathmann RR. 2007. The evolution of multicellularity: A minor major transition? Annu Rev Ecol Evol Syst 38: 621-654.
58. Grotzinger JP, Knoll AH. 1999. Stromatolites in Precambrian carbonates: Evolutionary mileposts or environmental dipsticks? Annu Rev Earth Planet Sci 27: 313-358.
59. Hadfield MG. 2011. Biofilms and marine invertebrate larvae: What bacteria produce that larvae use to choose settlement sites. Ann Rev Mar Sci 3: 453-470.
60. Haeckel E. 1872. Die Kalkschwamme [The calcareous sponges]. Georg Reimer, Berlin.
61. Haeckel E. 1874.Memoirs: The Gastraea-theory, the phylogenetic classification of the animal kingdom and the homology of the germ-lamellae. J Cell Sci s2-s14: 223-247.
62. Hannun YA, Obeid LM. 2008. Principles of bioactive lipid signalling: Lessons from sphingolipids. Nat Rev Mol Cell Biol 9: 139-150.
63. Hedges SB, Blair JE, Venturi ML, Shoe JL. 2004. A molecular timescale of eukaryote evolution and the rise of complex multicellular life. BMC Evol Biol 4: 2.
64. Hibberd DJ. 1975. Observations on the ultrastructure of the choanoflagellate Codosiga botrytis (Ehr.) Saville-Kent with special reference to the flagellar apparatus. J Cell Sci 17: 191-219.
65. Hoffman P, Kaufman A, Halverson G, Schrag D. 1998. A neoproterozoic snowball earth. Science 281: 1342-1346.
66. Hughes DT, Sperandio V. 2008. Inter-kingdom signalling: Communication between bacteria and their hosts. Nat Rev Micro 6: 111-120.
67. James-Clark H. 1868. On the spongiae ciliatae as infusoria flagellata; or observations on the structure, animality, and relationship of Leucosolenia botryoides, Bowerbank. Memoirs Boston Soc Hist 1: 133-142, 188-215, 250-264.
68. Kaiser D. 2001. Building a multicellular organism. Annu Rev Genet 35: 103-123.
69. Karpov SA, Coupe SJ. 1998. A revision of choanoflagellate genera Kentrosiga Schiller, 1953 and Desmarella Kent, 1880. Acta Protozool 37: 23-27.
70. Karpov SA, Leadbeater BSC. 1997. Cell and nuclear division in a freshwater choanoflagellate, Monosiga ovata Kent. Eur J Protistol 33: 323-334.
71. Karpov SA, Leadbeater BSC. 1998. Cytoskeleton structure and composition in choanoflagellates. J Eukaryot Microbiol 45: 361-367.
72. Kasting JF, Siefert JL. 2002. Life and the evolution of earth’s atmosphere. Science 296: 1066-1068.
73. Kawasaki S, Moriguchi R, Sekiya K, Nakai T, Ono E, Kume K, Kawahara K. 1994. The cell envelope structure of the lipopolysaccharide-lacking gram-negative bacterium Sphingomonas paucimobilis. J Bacteriol 176: 284-290.
74. Keeling PJ. 2014. The impact of history on our perception of evolutionary events: Endosymbiosis and the origin of eukaryotic complexity. Cold Spring Harb Perspect Biol 6: a016196.
75. King N. 2004. The unicellular ancestry of animal development. Dev Cell 7: 313-325.
76. King N, Hittinger CT, Carroll SB. 2003. Evolution of key cell signaling and adhesion protein families predates animal origins. Science 301: 361-363.
77. King N, Westbrook MJ, Young SL, Kuo A, Abedin M, Chapman J, Fairclough S, Hellsten U, Isogai Y, Letunic I, et al. 2008. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451: 783-788.
78. Knoll AH. 2003. The geological consequences of evolution. Geobiology 1: 3-14.
79. Knoll AH. 2011. The multiple origins of complex multicellularity. Annu Rev Earth Planet Sci 39: 217-239.
80. Knoll AH, Carroll SB. 1999. Early animal evolution: Emerging views from comparative biology and geology. Science 284: 2129-2137.
81. Kojima Y. 1992. Ultrastructure of goat testes: Intercellular bridge between germ cells. J Vet Med Sci 54: 213-219.
82. Koonin EV, Yutin N. 2014. The dispersed archaeal eukaryome and the complex archaeal ancestor of eukaryotes. Cold Spring Harb Perspect Biol 6: a016188.
83. Kunsman JE, Caldwell DR. 1974. Comparison of the sphingolipid content of rumen Bacteroides species. Appl Microbiol 28: 1088-1089.
84. Lang BF, O’Kelly C, Nerad T, Gray MW, Burger G. 2002. The closest unicellular relatives of animals. Curr Biol 12: 1773-1778.
85. Lapage G. 1925. Notes on the choanoflagellate, Codosiga botrytis, Ehrbg. Q J Microsc Sci 69: 471-508.
86. Lev M. 1979. Sphingolipid biosynthesis and vitamin K metabolism in Bacteroides melaninogenicus. Am J Clin Nutr 32: 179-186.
87. Levin TC, King N. 2013. Evidence for sex and recombination in the choanoflagellate Salpingoeca rosetta. Curr Biol 23: 2176-2180.
88. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R, et al. 2008. Evolution of mammals and their gut microbes. Science 320: 1647-1651.
89. Leys SP. 2006. Embryogenesis in the glass sponge Oopsacas minuta: Formation of syncytia by fusion of blastomeres. Integr Comp Biol 46: 104-117.
90. Leys SP, Degnan BM. 2002. Embryogenesis and metamorphosis in a haplosclerid demosponge: Gastrulation and transdifferentiation of larval ciliated cells to choanocytes. Invert Biol 121: 171-189.
91. Leys SP, Eerkes-Medrano D. 2005. Gastrulation in calcareous sponges: In search of Haeckel’s Gastraea. Integr Comp Biol 45: 342-351.
92. Leys SP, Ereskovsky AV. 2006. Embryogenesis and larval differentiation in sponges. Can J Zool 84: 262-287.
93. Leys SP, Nichols SA, Adams EDM. 2009. Epithelia and integration in sponges. Integr Comp Biol 49: 167-177.
94. Li W, Young SL, King N, Miller WT. 2008. Signaling properties of a non-metazoan Src kinase and the evolutionary history of Src negative regulation. J Biol Chem 283: 15491-15501.
95. Liu Y, Steenkamp ET, Brinkmann H, Forget L, Philippe H, Lang BF. 2009. Phylogenomic analyses predict sistergroup relationship of nucleariids and fungi and paraphyly of zygomycetes with significant support. BMC Evol Biol 9: 272.
96. Love GD, Grosjean E, Stalvies C, Fike DA, Grotzinger JP, Bradley AS, Kelly AE, Bhatia M, Meredith W, Snape CE, et al. 2009. Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature 457: 718-721.
97. Lyons KM. 1973. Collar cells in planula and adult tentacle ectoderm of the solitary coral Balanophyllia regia (Anthozoa Eupsammiidae). Z Zellforsch Mikrosk Anat 145: 57-74.
98. Maldonado M, Bergquist PR. 2002. Phylum Porifera. In Atlas of marine invertebrate larvae (ed. Young CM, Sewell MA, Rice ME), pp. 21-50. Academic, San Diego.
99. Maloof AC, Rose CV, Beach R, Samuels BM, Calmet CC, Erwin DH, Poirier GR, Yao N, Simons FJ. 2010. Possible animal-body fossils in pre-Marinoan limestones from South Australia. Nat Geosci 3: 653-659.
100. Manning G, Young SL, Miller WT, Zhai Y. 2008. The protist, Monosiga brevicollis, has a tyrosine kinase signaling network more elaborate and diverse than found in any known metazoan. Proc Natl Acad Sci 105: 9674-9679.
101. Margulis L. 1996. Archaeal-eubacterial mergers in the origin of Eukarya: Phylogenetic classification of life. Proc Natl Acad Sci 93: 1071-1076.
102. Marron AO, Alston MJ, Heavens D, Akam M, Caccamo M, Holland PWH, Walker G. 2013. A family of diatom-like silicon transporters in the siliceous loricate choanoflagellates. Proc Biol Sci 280: 20122543.
103. Martinez A, Lopez J, Villaro AC, Sesma P. 1991. Choanocytelike cells in the digestive system of the starfish Marthasterias glacialis (Echinodermata). J Morphol 208: 215-225.
104. Matsuo Y, Imagawa H, Nishizawa M, Shizuri Y. 2005. Isolation of an algal morphogenesis inducer from a marine bacterium. Science 307: 1598.
105. Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. 2005. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122: 107-118.
106. McFall-Ngai M. 1999. Consequences of evolving with bacterial symbionts: Insights from the squid-vibrio associations. Annu Rev Ecol Syst 30: 235-256.
107. McFall-Ngai M., Ruby EG. 2000. Developmental biology in marine invertebrate symbioses. Curr Opin Microbiol 3: 603-607.
108. McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Loso T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF, et al. 2013. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci 110: 3229-3236.
109. Medina M, Collins AG, Taylor JW, Valentine JW, Lipps JH, Amaral-Zettler L, Sogin ML. 2003. Phylogeny of Opisthokonta and the evolution of multicellularity and complexity in Fungi and Metazoa. Int J Astrobiol 2: 203-211.
110. Mikhailov KV, Konstantinova AV, Nikitin MA, Troshin PV, Rusin LY, Lyubetsky VA, Panchin YV, Mylnikov AP, Moroz LL, Kumar S, et al. 2009. The origin of Metazoa: A transition from temporal to spatial cell differentiation. Bioessays 31: 758-768.
111. Milanesi C. 1971. Choanocytes in endostyle of Botryllus-Schlosseri (Pallas) Ascidiacea Stolidobranchiata. J Submicrosc Cytol 3: 359-363.
112. Minamino M, Sakaguchi I, Naka T, Ikeda N, Kato Y, Tomiyasu I, Yano I, Kobayashi K. 2003. Bacterial ceramides and sphingophospholipids induce apoptosis of human leukaemic cells. Microbiology 149: 2071-2081.
113. Miyagawa E, Azuma R, Suto T, Yano I. 1979. Occurrence of free ceramides in Bacteroides fragilis NCTC 9343. J Biochem 86: 311-320.
114. Mojzsis SJ, Arrhenius G, McKeegan KD, Harrison TM, Nutman AP, Friend CR. 1996. Evidence for life on Earth before 3,800 million years ago. Nature 384: 55-59.
115. Montgomery MK, McFall-Ngai MJ. 1994. Bacterial symbionts induce host organ morphogenesis during early postembryonic development of the squid Euprymna scolopes. Development 120: 1719-1729.
116. Moran NA. 2007. Symbiosis as an adaptive process and source of phenotypic complexity. Proc Natl Acad Sci 104: 8627-8633.
117. Naka T, Fujiwara N, Yabuuchi E, Doe M, Kobayashi K, Kato Y, Yano I. 2000. A novel sphingoglycolipid containing galacturonic acid and 2-hydroxy fatty acid in cellular lipids of Sphingomonas yanoikuyae. J Bacteriol 182: 2660-2663.
118. Narbonne GM. 2005. The Ediacara biota: Neoproterozoic origin of animals and their ecosystems. Annu Rev Earth Planet Sci 33: 421-442.
119. Nedelcu AM, Miles IH, Fagir AM, Karol K. 2008. Adaptive eukaryote-to-eukaryote lateral gene transfer: Stress-related genes of algal origin in the closest unicellular relatives of animals. J Evol Biol 21: 1852-1860.
120. Nerrevang A, Wingstrand KG. 1970. On the occurrence and structure of choanocyte-like cells in some echinoderms. Acta Zoologica 51: 249-270.
121. Newman DK, Banfield JF. 2002. Geomicrobiology: How molecular-scale interactions underpin biogeochemical systems. Science 296: 1071-1077.
122. Nichols FC. 1998. Novel ceramides recovered from Porphyromonas gingivalis: Relationship to adult periodontitis. J Lipid Res 39: 2360-2372.
123. Nichols SA, Dirks W, Pearse JS, King N. 2006. Early evolution of animal cell signaling and adhesion genes. Proc Natl Acad Sci 103: 12451-12456.
124. Nichols SA, Dayel M, King N. 2009. Genomic, phylogenetic, and cell biological insights into metazoan origins. In Animal Evolution: Genomes, Fossils, and Trees (ed. Telford MJ, Littlewood DTJ), pp. 24-32. Oxford University Press, Oxford.
125. Nichols SA, Roberts BW, Richter DJ, Fairclough SR, King N. 2012. Origin of metazoan cadherin diversity and the antiquity of the classical cadherin/b-catenin complex. Proc Natl Acad Sci 109: 13046-13051.
126. Nielsen C. 2008. Six major steps in animal evolution: Are we derived sponge larvae? Evol Dev 10: 241-257.
127. Norrevang A. 1964. Choanocytes in the skin of Harrimania kupfferi (Enteropneusta). Nature 204: 398-399.
128. Nursall JR. 1959. Oxygen as a prerequisite to the origin of the Metazoa. Nature 183: 1170-1172.
129. Olsen I, Jantzen E. 2001. Sphingolipids in bacteria and fungi. Anaerobe 7: 103-112.
130. Ong S, Tan C. 2010. Germline cyst formation and incomplete cytokinesis during Drosophila melanogaster oogenesis. Dev Biol 337: 84-98.
131. Orme B, Otto SR, Blake JR. 2001. Enhanced efficiency of feeding and mixing due to chaotic flow patterns around choanoflagellates. IMA J Math Appl Med Biol 18: 293-325.
132. Paps J, Medina-Chacón LA, Marshall W, Suga H, Ruiz-Trillo I. 2013. Molecular phylogeny of unikonts: New insights into the position of apusomonads and ancyromonads and the internal relationships of opisthokonts. Protist 164: 2-12.
133. Parfrey LW, Lahr DJG, Knoll AH, Katz LA. 2011. Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc Natl Acad Sci 108: 13624-13629.
134. Peterson KJ. 2004. Estimating metazoan divergence times with a molecular clock. Proc Natl Acad Sci 101: 6536-6541.
135. Pettitt ME, Orme B, Blake JR, Leadbeater B. 2002. The hydrodynamics of filter feeding in choanoflagellates. Eur J Protistol 38: 313-332.
136. Philippe H, Snell EA, Bapteste E, Lopez P, Holland PWH, Casane D. 2004. Phylogenomics of eukaryotes: Impact of missing data on large alignments. Mol Biol Evol 21: 1740-1752.
137. Pincus D, Letunic I, Bork P, Lim WA. 2008. Evolution of the phospho-tyrosine signaling machinery in premetazoan lineages. Proc Natl Acad Sci 105: 9680-9684.
138. Pires-daSilva A, Sommer R. 2003. The evolution of signalling pathways in animal development. Nat Rev Genet 4: 39-49.
139. Putnam NH, Srivastava M, Hellsten U, Dirks B, Chapman J, Salamov A, Terry A, Shapiro H, Lindquist E, Kapitonov VV, et al. 2007. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317: 86-94.
140. Richter DJ, King N. 2013. The genomic and cellular foundations of animal origins. Annu Rev Genet 47: 509-537.
141. Rivera MC, Lake JA. 2004. The ring of life provides evidence for a genome fusion origin of eukaryotes. Nature 431: 152-155.
142. Rokas A. 2008. The origins of multicellularity and the early history of the genetic toolkit for animal development. Annu Rev Genet 42: 235-251.
143. Rokas A, King N, Finnerty J, Carroll SB. 2003. Conflicting phylogenetic signals at the base of the metazoan tree. Evol Dev 5: 346-359.
144. Roper M, Dayel MJ, Pepper RE, Koehl MAR. 2013. Cooperatively generated stresslet flows supply fresh fluid to multicellular choanoflagellate colonies. Phys Rev Lett 110: 228104.
145. Rosing M. 1999. 13C-Depleted carbon microparticles in.3700-Ma sea-floor sedimentary rocks fromwest greenland. Science 283: 674-676.
146. Ruiz-Trillo I, Inagaki Y, Davis LA, Sperstad S, Landfald B, Roger AJ. 2004. Capsaspora owczarzaki is an independent opisthokont lineage. Curr Biol 14: R946-R947.
147. Ruiz-Trillo I, Lane CE, Archibald JM, Roger AJ. 2006. Insights into the evolutionary origin and genome architecture of the unicellular opisthokonts Capsaspora owczarzaki and Sphaeroforma arctica. J Eukaryot Microbiol 53: 379-384.
148. Ruiz-Trillo I, Roger AJ, Burger G, Gray MW, Lang BF. 2008. A phylogenomic investigation into the origin of metazoa. Mol Biol Evol 25: 664-672.
149. Sagan L. 1967. On the origin of mitosing cells. J Theor Biol 14: 225-274.
150. Schaefer AL, Hanzelka BL, Eberhard A, Greenberg EP. 1996. Quorum sensing in Vibrio fischeri: Probing autoinducer-LuxR interactions with autoinducer analogs. J Bacteriol 178: 2897-2901.
151. Sebé-Pedró s A, Roger AJ, Lang FB, King N, Ruiz-Trillo I. 2010. Ancient origin of the integrin-mediated adhesion and signaling machinery. Proc Natl Acad Sci 107: 10142-10147.
152. Sebé-Pedró s A, Burkhardt P, Sánchez-Pons N, Fairclough SR, Lang BF, King N, Ruiz-Trillo I. 2013. Insights into the origin of metazoan filopodia and microvilli. Mol Biol Evol 30: 2013-2023.
153. Shalchian-Tabrizi K, Minge MA, Espelund M, Orr R, Ruden T, Jakobsen KS, Cavalier-Smith T. 2008. Multigene phylogeny of choanozoa and the origin of animals. PLoS ONE 3: e2098.
154. Shen Y, Zhang T, Hoffman PF. 2008. On the coevolution of Ediacaran oceans and animals. Proc Natl Acad Sci 105: 7376-7381.
155. Singla V, Reiter JF. 2006. The primary cilium as the cell’s antenna: Signaling at a sensory organelle. Science 313: 629-633.
156. Srivastava M, Begovic E, Chapman J, Putnam NH, Hellsten U, Kawashima T, Kuo A, Mitros T, Salamov A, Carpenter ML, et al. 2008. The Trichoplax genome and the nature of placozoans. Nature 454: 955-960.
157. Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier MEA, Mitros T, Richards GS, Conaco C, Dacre M, Hellsten U, et al. 2010. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466: 720-726.
158. Stanley SM. 1973. An ecological theory for the sudden origin of multicellular life in the late precambrian. ProcNatl Acad Sci 70: 1486-1489.
159. Steenkamp ET, Wright J, Baldauf SL. 2006. The protistan origins of animals and fungi. Mol Biol Evol 23: 93-106.
160. Steiner S, Conti SF, Lester RL. 1973. Occurrence of phosphonosphingolipids in Bdellovibrio bacteriovorus strain UKi2. J Bacteriol 116: 1199-1211.
161. Suga H, Chen Z, deMendoza A, Sebé-Pedró s A, Brown MW, Kramer E, Carr M, Kerner P, Vervoort M, Sánchez-Pons N, et al. 2013. The Capsaspora genome reveals a complex unicellular prehistory of animals. Nat Commun 4: 2325.
162. Sun G, Huang J. 2011. Horizontally acquired DAP pathway as a unit of self-regulation. J Evol Biol 24: 587-595.
163. Sun G, Yang Z, Ishwar A, Huang J. 2010. Algal genes in the closest relatives of animals. Mol Biol Evol 27: 2879-2889.
164. Szathmáry E, Smith JM. 1995. The major evolutionary transitions. Nature 374: 227-232.
165. Torruella G, Suga H, Riutort M, Peretó J, Ruiz-Trillo I. 2009. The evolutionary history of lysine biosynthesis pathways within eukaryotes. J Mol Evol 69: 240-248.
166. Towe KM. 1970. Oxygen-collagen priority and the early metazoan fossil record. Proc Natl Acad Sci 65: 781.
167. Tucker RP, Beckmann J, Leachman NT, Schöler J, Chiquet-Ehrismann R. 2012. Phylogenetic analysis of the teneurins: Conserved features and premetazoan ancestry. Mol Biol Evol 29: 1019-1029.
168. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP, et al. 2009. Acore gut microbiome in obese and lean twins. Nature 457: 480-484.
169. Tyler S. 2003. Epithelium—The primary building block for metazoan complexity. Integr Comp Biol 43: 55-63.
170. Walker CW. 1979. Ultrastructure of the somatic portion of the gonads in asteroids, with emphasis on flagellated-collar cells and nutrient transport. J Morphol 162: 127-161.
171. Walter MR, Heys GR. 1985. Links between the rise of the metazoa and the decline of stromatolites. Precamb Res 29: 149-174.
172. Walter MR, Buick R, Dunlop J. 1980. Stromatolites 3,400-3,500 myr old from the North-Pole Area, Western Australia. Nature 284: 443-445.
173. Webster NS, Smith LD, Heyward AJ, Watts JEM, Webb RI, Blackall LL, Negri AP. 2004. Metamorphosis of a scleractinian coral in response to microbial biofilms. Appl Environ Microbiol 70: 1213-1221.
174. Weis WI, Taylor ME, Drickamer K. 1998. The C-type lectin superfamily in the immune system. Immunol Rev 163: 19-34.
175. Wieczorek SK, Todd CD. 1997. Inhibition and facilitation of bryozoan and ascidian settlement by natural multispecies biofilms: Effects of film age and the roles of active and passive larval attachment. Marine Biol 128: 463-473.
176. Woollacott RM, Hadfield MG. 1996. Induction of metamorphosis in larvae of a sponge. Invert Biol 115: 257-262.
177. Yano I, Tomiyasu I, Yabuuchi E. 1982. Long chain base composition of strains of three species of Sphingobacterium gen. nov. FEMS Microbiol Lett 15: 303-307.
178. Young SL, Diolaiti D, Conacci-Sorrell M, Ruiz-Trillo I, Eisenman RN, King N. 2011. Premetazoan ancestry of the Myc-Max network. Mol Biol Evol 28: 2961-2971.
179. Yue J, Sun G, Hu X, Huang J. 2013. The scale and evolutionary significance of horizontal gene transfer in the choanoflagellateMonosiga brevicollis. BMC Genomics 14: 729.
180. Ziegler TA, Forward RB. 2007. Larval release behaviors in the Caribbean spiny lobster, Panulirus argus: Role of peptide pheromones. J Chem Ecol 33: 1795-1805.