Experimental manipulation of sponge/bacterial symbiont community composition with antibiotics: Sponge cell aggregates as a unique tool to study animal/microorganism symbiosis

FEMS Microbiology Ecology

Volumn 81, Issue 2, 2012, Pages 407-418

  Richardson, Crystal ^a,b   Hill, Malcolm ^a   Marks, Carolyn ^a,c   Runyen Janecky, Laura ^a   Hill, April ^a  

^a UNIVERSITY OF RICHMOND   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c HARVARD UNIVERSITY   (United States)

Author keywords

Antibiotics; Bacterial diversity; Host; Microbial ecology

Indexed keywords

ANTIINFECTIVE AGENT; BACTERIAL DNA; RNA 16S;

ANTIBIOTICS; BACTERIUM; COMMUNITY STRUCTURE; EXPERIMENTAL STUDY; GROWTH RATE; HOST-SYMBIONT INTERACTION; MICROBIAL COMMUNITY; SPONGE; SYMBIOSIS;

ANIMAL; ARTICLE; AXENIC CULTURE; BACTERIUM; BIODIVERSITY; CLASSIFICATION; DENATURING GRADIENT GEL ELECTROPHORESIS; DNA SEQUENCE; DRUG EFFECT; GENETICS; GROWTH, DEVELOPMENT AND AGING; METAGENOME; MICROBIOLOGY; PHYLOGENY; SPONGE (PORIFERA); SYMBIOSIS;

ANIMALS; ANTI-BACTERIAL AGENTS; AXENIC CULTURE; BACTERIA; BIODIVERSITY; DENATURING GRADIENT GEL ELECTROPHORESIS; DNA, BACTERIAL; METAGENOME; PHYLOGENY; PORIFERA; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

BACTERIA (MICROORGANISMS); CLATHRIA;

EID: 84863785265     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/j.1574-6941.2012.01365.x     Document Type: Article

References (90)

1. Adell T Müller WEG (2005) Expression pattern of the Brachyury and Tbx2 homologues from the sponge Suberites domuncula. Biol Cell 97: 641-650.
2. Amano S Hori I (1996) Transdifferentiation of larval flagellated cells to choanocytes in the metamorphosis of the demosponge Haliclona permollis. Biol Bull 190: 161-172.
3. Arillo A, Bavestrello G, Burlando B Sará M (1993) Metabolic integration between symbiotic cyanobacteria and sponges: a possible mechanism. Mar Biol 117: 159-162.
4. Blunt JW, Copp BR, Munro MH, Northcote PT Prinsep MR (2011) Marine natural products. Nat Prod Rep 28: 196-268.
5. Borojevic R Lévi C (1964) Etude au microscope électronique des cellules de l'éponge Ophlitaspongia serriata (Grant) au cours de la reorganization après dissociation. Z Zellforsch Mikrosk Anat 64: 708-725.
6. Buscema M, De Sutter D Van de Vyver G (1980) Ultrastructural study of differentiation processes during aggregation of purified sponge archaeocytes. Roux Arch Dev Biol 188: 45-53.
7. Curtis ASG (1962) Pattern and mechanism in the reaggregation of sponges. Nature 196: 245-248.
8. Custódio MR, Prokic I, Steffen R, Koziol C, Borojevic R, Brümmer F, Nickel M Müller WEG (1998) Primmorphs generated from dissociated cells from the sponge Suberites domuncula: a model system for studies of cell proliferation and cell death. Mech Ageing Dev 105: 45-59.
9. Custódio MR, Hajdu E Muricy G (2004) Cellular dynamics of in vitro allogeneic reactions of Hymeniacidon heliophila (Demospongiae: Halichondrida). Mar Biol 144: 999-1010.
10. Dattelbaum JD, Sieg D, Manieri CM, Thomson G Hill M (2010) Plasticity of acquired secondary metabolites in Clathria prolifera (Demospongia: Poecilosclerida): Putative photoprotective role of carotenoids in a temperate intertidal sponge. Open J Mar Biol 4: 87-95.
11. Enticknap JJ, Kelly M, Peraud O Hill RT (2006) Characterization of a culturable alphaproteobacterial symbiont common to many marine sponges and evidence for vertical transmission via sponge larvae. Appl Environ Microbiol 72: 3724-3732.
12. Ereskovsky AV, Gonobobleva E Vishnyakov A (2005) Morphological evidence for vertical transmission ofsymbiotic bacteria in the viviparous sponge Halisarca dujardini Johnston (Porifera, Demospongiae, Halisarcida). Mar Biol 146: 869-875.
13. Erwin PM, Olson JB Thacker RW (2011) Phylogenetic diversity, host-specificity and community profiling of sponge-associated bacteria in the northern Gulf of Mexico. PLoS ONE 6: e26806.
14. Fieseler L, Horn M, Wagner M Hentschel U (2004) Discovery of a novel candidate phylum 'Poribacteria' in marine sponges. Appl Environ Microbiol 70: 3724-3732.
15. Flemming H-C Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8: 623-633.
16. Funayama N (2010) The stem cell system in demosponges: insights into the origin of somatic stem cells. Dev Growth Differ 52: 1-14.
17. Gaino E, Zunino L, Burlando B Sarà M (1985) The locomotion of dissociated sponge cells: A cell-by-cell, time-lapse film analysis. Cell Motil 5: 463-473.
18. Galtsoff PS (1925a) Regeneration after dissociation (an experimental study on sponges). I. Behavior of dissociated cells of Microciona prolifera under normal and altered conditions. J Exp Zool 42: 183-221.
19. Galtsoff PS (1925b) Regeneration after dissociation (an experimental study on sponges). II. Histogenesis of Microciona prolifera, Verr. J Exp Zool 42: 223-255.
20. Gerce B, Schwartz T, Syldatk C Hausmann R (2011) Differences between bacterial communities associated with the surface or tissue of Mediterranean sponge species. Microb Ecol 61: 769-782.
21. Giberson RT Demaree RS (2001) Microwave: Techniques and Protocols. Humana Press, Totowa, NJ.
22. Girón JA, Ho AS Schoolnik GK (1993) Characterization of fimbriae produced by enteropathogenic Escherichia coli. J Bacteriol 175: 7391-7403.
23. Hentschel U, Hopke J, Horn M, Friedrich AB, Wagner M Hacker J (2002) Molecular evidence for a uniform microbial community in sponges from different oceans. Appl Environ Microbiol 68: 4431-4440.
24. Hill MS (1996) Symbiotic zooxanthellae enhance boring and growth rates of the tropical sponge Anthosigmella varians forma varians. Mar Biol 125: 649-654.
25. Hill RT (2004) Microbes from marine sponges: a treasure trove of biodiversity for natural products discovery. Microbial Diversity and Bioprospecting (Bull AT ed). 177-190. American Society of Microbiology, Washington, DC.
26. Hill M, Hill A, Lopez N Harriott O (2006) Sponge-Specific Bacterial Symbionts in the Caribbean Sponge, Chondrilla nucula (Demospongiae, Chondrosida). Mar Biol 148: 1221-1230.
27. Hochmuth T, Niederkrüger H, Gernert C, Siegl A, Taudien S, Platzer M, Crews P, Hentschel U Piel J (2010) Linking chemical and microbial diversity in marine sponges: possible role for Poribacteria as producers of methyl-branched fatty acids. ChemBioChem 11: 2572-2578.
28. Hoffmann F, Larsen O, Thiel V, Rapp H, Pape T Michaelis W (2005) An anaerobic world in sponges. J Geomicrobiol 22: 1-10.
29. Holmes B Blanch H (2007) Possible taxonomic trends in the success of primary aggregate format formation in marine sponge cell cultures. Mar Biotechnol 10: 99-109.
30. Humphreys T (1963) Chemical dissolution and in vitro reconstruction of sponge cell adhesions. I. Isolation and functional demonstration of the components involved. Dev Biol 8: 27-47.
31. Humphreys T, Humphreys S Moscona A (1960) A procedure for obtaining completely dissociated sponge cells. Biol Bull 119: 284.
32. Huxley JS (1912) Some phenomena of regeneration in Sycon; with a note on the structure of its collar-cells. Philos Trans R Soc B 202: 165-189.
33. Johnson JR (1991) Virulence factors in Escherichia coli urinary tract infection. Clin Microbiol Rev 4: 80-128.
34. Kaesler I, Graeber I, Borchert MS, Pape T, Dieckmann R, von Döhren H, Nielsen P, Lurz R, Michaelis W Szewzyk U (2008) Spongiispira norvegica gen. nov., sp. nov., a marine bacterium isolated from the boreal sponge Isops phlegraei. Int J Syst Evol Microbiol 58: 1815-1820.
35. Kaye HR (1991) Sexual reproduction in four Caribbean commercial sponges II. Oogenesis and transfer of bacterial symbionts. Invertebr Reprod Dev 19: 13-24.
36. Kaye HR Reiswig HM (1985) Histocompatibility responses in Verongia species (Demospongiae): Implications of immunological studies. Biol Bull 168: 183-188.
37. Lafi FF, Fuerst JA, Fieseler L Hentschel U (2009) Widespread distribution of poribacteria in Demospongiae. Appl Environ Microbiol 75: 5695-5699.
38. Lee OO, Wang Y, Yang J, Lafi FF, Al-Suwailem A Qian P-Y (2010) Pyrosequencing reveals highly diverse and species-specific microbial communities in sponges from the Red Sea. ISME J 5: 650-654.
39. Lemoine N, Buell N, Hill A Hill M (2007) Assessing the utility of sponge microbial symbiont communities as models to study global climate change: a case study with Halichondria bowerbanki. Porifera Research: Biodiversity, Innovation, and Sustainability (Custódio MR, Lôbo-Hajdu G, Hajdu E Muricy G eds) 419-425. Museu Nacional, Rio de Janeiro, Brazil.
40. Le Pennec G, Perovic S, Ammar MS, Grebenjuk VA, Steffen R, Brümmer F Müller WEG (2003) Cultivation of primmorphs from the marine sponge Suberites domuncula: morphogenetic potential of silicon and iron. J Biotechnol 100: 93-108.
41. Li ZY Liu Y (2006) Marine sponge Craniella austrialiensis-associated bacterial diversity revelation based on 16S rDNA library and biologically active Actinomycetes screening, phylogenetic analysis. Lett Appl Microbiol 43: 410-416.
42. Loewenstein WR (1967) On the genesis of cellular communication. Dev Biol 15: 503-520.
43. MacLennan A (1974) The chemical bases of taxon-specific cellular reaggregation and 'self-not-self' recognition in sponges. Arch Biol 85: 53-90.
44. MacLennan A Dodd R (1967) Promoting activity of extracellular materials on sponge cell reaggregation. J Embryol Exp Morphol 17: 473-480.
45. Moscona AA (1963) Studies on cell aggregation: demonstration of materials with a selective cell-binding activity. P Natl Acad Sci USA 49: 742-747.
46. Moscona AA (1968) Cell aggregation: properties of specific cell-ligands and their role in the formation of multicellular systems. Dev Biol 18: 250-277.
47. Müller WEG (1982) Cell membranes in sponges. Int Rev Cytol 77: 129-181.
48. Müller WEG Müller IM (2003) Origin of the metazoan immune system: identification of the molecules and their functions in sponges. Integr Comp Biol 43: 281-292.
49. Müller WEG, Korzhev M, Le Pennec G, Müller IM Schröder HC (2003) Origin of metazoan stem cell system in sponges: first approach to establish the model (Suberites domuncula). Biomol Eng 20: 369-379.
50. Müller WEG, Thakur NL, Ushijima H, Thakur AN, Krasko A, Le Pennec G, Indap MM, Perović-Ottstadt S, Schröder HC, Lang G Bringmann G (2004) Matrix-mediated canal formation in primmorphs from the sponge Suberites domuncula involves the expression of a CD36 receptor-ligand system. J Cell Sci 117: 2579-2590.
51. Pamp SJ, Gjermansen M Toker-Nielsen T (2007) The biofilm matrix: a sticky framework. The Biofilm Mode of Life: Mechanisms and Adaptations (Kjelleberg S Givskov M eds). 37-69. Horizon Bioscience, Norwich, UK.
52. Piel J (2004) Metabolites from symbiotic bacteria. Nat Prod Rep 21: 519-538.
53. Pozzolini M, Sturla L, Cerrano C, Bavestrello G, Camardella L, Parodi AM, Raheli F, Benfatti U, Müller WEG Giovine M (2005) Molecular cloning of silicatein gene from the sponge Petrosia fciformis (Porifera, demospongia) and development of primmorphs as a model for biosilification. Mar Biotechnol 6: 594-603.
54. Radwan M, Hanora A, Zan J, Mohamed NM, Abo-Elmatty DM, Abou-El-Ela SH Hill RT (2010) Bacterial community analyses of two Red Sea sponges. Mar Biotechnol 12: 350-360.
55. Regoli F, Cerrano C, Chierici E, Chiantore MC Bavestrello G (2004) Seasonal variability of prooxidant pressure and antioxidant adaptation to symbiosis in the Mediterranean demosponge Petrosia ficiformis. Mar Ecol Prog Ser 275: 129-137.
56. Schlappy M-L, Schöttner SI, Lavik G, Kuypers MM, de Beer D Hoffmann F (2010) Evidence of nitrification and denitrification in high and low microbial abundance sponges. Mar Biol 157: 593-602.
57. Schmitt S, Weisz J, Lindquist N Hentschel U (2007) Vertical transmission of a phylogenetically complex microbial consortium in the viviparous sponge Ircinia felix. Appl Environ Microbiol 73: 2067-2078.
58. Schmitt S, Angelmeier H, Schiller R, Lindquist N Hentschel U (2008) Molecular microbial diversity survey of sponge reproductive stages and mechanistic insights into vertical transmission of microbial symbionts. Appl Environ Microbiol 74: 7694-7708.
59. Schmitt S, Tsai P, Bell J et al. (2011a) Assessing the complex sponge microbiota: core, variable, and species-specific bacterial communities in marine sponges. ISME J 6: 564-576.
60. Schmitt S, Deines P, Behnam F, Wagner M Taylor MW (2011b) Chloroflexi bacteria are more diverse, abundant, and similar in high than in low microbial abundance sponges. FEMS Microbiol Ecol 78: 497-510.
61. Sfanos K, Harmody D, Dang P, Ledger A, Pomponi S, McCarthy P Lopez J (2005) A molecular systematic survey of cultured microbial associates of deep-water marine invertebrates. Syst Appl Microbiol 28: 242-264.
62. Sharp KH, Eam B, Faulkner DJ Haygood MG (2007) Vertical transmission of diverse microbes in the tropical sponge Corticium sp. Appl Environ Microbiol 73: 622-629.
63. Sipkema D, van Wielink R, van Lammeren AAM, Tramper J, Osinga R Wijffels RH (2003) Primmorphs from seven marine sponges: formation and structure. J Biotechnol 100: 127-139.
64. Spiegel M (1954) The role of specific surface antigens in cell adhesion. Part I. The reaggregation of sponge cells. Biol Bull 107: 130-148.
65. Steger D, Ettinger-Epstein P, Whalan S, Hentschel U, de Nys R Wagner M (2008) Diversity and mode of transmission of ammonia-oxidizing archaea in marine sponges. Environ Microbiol 10: 1087-1094.
66. Sun L, Song Y, Qu Y, Yu X Zhang W (2007) Purification and in vitro cultivation of archaeocytes (stem cells) of the marine sponge Hymeniacidon perleve (Demospongiae). Cell Tissue Res 328: 223-237.
67. Taylor MW, Schupp PJ, de Nys R, Kjelleberg S Steinberg PD (2005) Biogeography of bacteria associated with the sponge Cymbastella concentrica. Environ Microbiol 7: 419-433.
68. Taylor MW, Hill RT, Piel J, Thacker RW Hentschel U (2007a) Soaking it up: the complex lives of marine sponges and their microbial associates. ISME J 1: 187-190.
69. Taylor MW, Radax R, Steger D Wagner M (2007b) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71: 295-347.
70. Thacker RW (2005) Impacts of shading on sponge-cyanobacteria symbioses: a comparison between host-specific and generalist associations. Integr Comp Biol 45: 369-376.
71. Thomas T, Rusch D, DeMaere MZ, Yung PY, Lewis M, Halpern A, Heidelberg KB, Egan S, Steinberg PD Kjelleberg S (2010) Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis. ISME J 4: 1557-1567.
72. To Isaacs L, Kan J, Nguyen L, Videau P, Anderson MA, Wright TL Hill RT (2009) Comparison of the bacterial communities of wild and captive sponge Clathria prolifera from the Chesapeake Bay. Mar Biotechnol 11: 758-770.
73. Usher KM, Kuo J, Fromont J Sutton DC (2001) Vertical transmission of cyanobacterial symbionts in the marine sponge Chondrilla australiensis (Demospongiae). Hydrobiologia 461: 15-23.
74. Usher KM, Sutton DC, Toze S, Kuo J Fromont J (2005) Inter-generational transmission of microbial symbionts in the marine sponge Chondrilla australiensis (Demospongiae). Mar Freshw Res 56: 125-131.
75. Valisano L, Bavestrello G, Giovine M Cerrano C (2006) Primmorphs formation dynamics: a screening among Mediterranean sponges. Mar Biol 149: 1037-1046.
76. Valisano L, Bavestrello G, Giovine M, Arillo A Cerrano C (2007) Effect of iron and dissolved silica on primmorphs of Petrosia ficiformis (Poiret, 1789). Chem Ecol 23: 233-241.
77. Van de Vyver G Buscema M (1981) Capacités morphogènes des cellules d'éponges dissociées. Annls Soc R Zool Belg 111: 9-19.
78. Vogel G (2008) The inner lives of sponges. Science 320: 1028-1030.
79. Wang Q, Garrity GM, Tiedje JM Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261-5267.
80. Webster NS, Cobb RE Negri AP (2008) Temperature thresholds for bacterial symbiosis with a sponge. ISME J 2: 830-842.
81. Webster NS, Taylor MW, Behnam F, Luecker S, Rattei T, Whalan S, Horn M Wagner M (2010) Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ Microbiol 12: 2070-2082.
82. Weisz JB, Lindquist N Martens CS (2008) Do associated microbial abundances impact marine demosponge pumping rates and tissue densities? Oecologia 155: 367-376.
83. Weisz J, Massaro A, Ramsby B Hill M (2010) Zooxanthellar symbionts shape host sponge trophic status through translocation of carbon. Biol Bull 219: 189-197.
84. Wilkinson CR (1979) Nutrient translocation from symbiotic cyanobacteria to coral reef sponges. Biologie des Spongiaires (Levi C Boury-Esnault N eds). 373-380. Coli. Int. C.N.R.S., Paris.
85. Wilson HV (1907a) A new method by which sponges may be artificially reared. Science 25: 912-915.
86. Wilson HV (1907b) On some phenomena of coalescence and regeneration in sponges. J Exp Zool 5: 245-258.
87. Wilson HV (1911) Development of sponges from dissociated tissue cells. Bull US Bur Fish 30: 1-30.
88. Wilson HV Penney JT (1930) The regeneration of sponges (Microciona) from dissociated cells. J Exp Zool 56: 73-147.
89. Wolfson JS Hooper DC (1985) The fluoroquinolones: structures, mechanisms of action and resistance, and spectra of activity in vitro. Antimicrob Agents Chemother 28: 581-586.
90. Zar JH (2009) Biostatistical Analysis, 5th edn. Pearson Education, Upper Saddle River, NJ.