Enigmatic dual symbiosis in the excretory organ of Nautilus macromphalus (Cephalopoda: Nautiloidea)

Proceedings of the Royal Society B: Biological Sciences

Volumn 274, Issue 1614, 2007, Pages 1143-1152

  Pernice, Mathieu ^a   Wetzel, Silke ^b   Gros, Olivier ^c   Boucher Rodoni, Renata ^a   Dubilier, Nicole ^b  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^b MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

^c UNIVERSITÉ DES ANTILLES ET DE LA GUYANE   (France)

Author keywords

16S rRNA; Bacteria; Cephalopods; Excretion; Nautilus; Symbiosis

Indexed keywords

RNA 16S;

ADAPTATION; ANCESTRY; BACTERIUM; CEPHALOPOD; ENDOSYMBIONT; EXCRETION; HYBRIDIZATION; METAZOAN; PHYLOGENY; RELATEDNESS; RNA; SYMBIOSIS; TRANSMISSION ELECTRON MICROSCOPY;

ACIDITY; ARTICLE; BACTERIAL METABOLISM; BETAPROTEOBACTERIA; CEPHALOPOD; EVOLUTION; EXOCRINE GLAND; FLUORESCENCE IN SITU HYBRIDIZATION; FORCE; LIVING FOSSIL; MORPHOLOGY; NAUTILUS; NAUTILUS MACROMPHALUS; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION; PHYLOGENY; PRIORITY JOURNAL; RNA SEQUENCE; SPIROCHETE; SYMBIONT; SYMBIOSIS; TRANSMISSION ELECTRON MICROSCOPY; ULTRAFILTRATION;

BACTERIA (MICROORGANISMS); CEPHALOPODA; COCCOIDEA; METAZOA; NAUTILOIDEA; NAUTILUS; NAUTILUS MACROMPHALUS; NITROSOMONADALES; PROTEOBACTERIA; SPIROCHAETA;

EID: 34447303497     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2006.0353     Document Type: Article

References (57)

1. Altschul, S. F., Boguski, M. S., Gish, W. & Wootton, J. C. 1994 Issues in searching molecular sequence databases. Nat. Genet. 6, 119-129. (doi:10.1038/ng0294-119)
2. Amann, R. I., Krumholz, L. & Stahl, D. A. 1990 Fluorescent- oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J. Bacteriol. 172, 762-770.
3. Barbieri, E., Paster, B. J., Hughes, D., Zurek, L., Moser, D. P., Teske, A. & Sogin, M. L. 2001 Phylogenetic characterization of epibiotic bacteria in the accessory nidamental gland and egg of the squid Loligo pealei (Cephalopoda: Loliginidae). Environ. Microbiol. 3, 151-167. (doi:10.1046/j.1462-2920.2001.00172.x)
4. Behrens, S., Fuchs, B. M., Mueller, F. & Amann, R. 2003 Is the in situ accessibility of the 16S rRNA of Escherichia coli for Cy3-labeled oligonucleotide probes predicted by a three-dimensional structure model of the 30S ribosomal subunit? Appl. Environ. Microbiol. 69, 4935-4941. (doi:10. 1128/AEM.69.8.4935-4941.2003)
5. Boucher-Rodoni, R. 1989 Consommation d'oxygène et excrétion ammoniacale de Nautilus macromphalus. C.R. Acad. Sci. Paris 309, 173-179.
6. Boucher-Rodoni, R. & Mangold, K. 1994 Ammonia production in cephalopods: physiological and evolutionary aspects. Mar. Freshw. Behav. Physiol. 25, 53-60.
7. Boutilier, R. G., West, T. G., Pogson, G. H., Mesa, K. A., Wells, J. & Wells, M. J. 1996 Nautilus and the art of metabolic maintenance. Nature 382, 534-536. (doi:10. 1038/382534a0)
8. Braker, G., Fesefeldt, A. & Witzel, K. P. 1998 Development of PCR primer systems for amplification of nitrite reductase genes (nirK and nirS) to detect denitrifying bacteria in environmental samples. Appl. Environ. Microbiol. 64, 3769-3775.
9. Cabello, F. C., Sartakova, M. L. & Dobrikova, E. Y. 2001 Genetic manipulation of spirochetes-light at the end of the tunnel. Trends Microbiol. 9, 245-248. (doi:10.1016/S0966-842X(01)02046-7)
10. Cavanaugh, C. M., Gardiner, S. L., Jones, M. L., Jannasch, H. W. & Waterbury, J. B. 1981 Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science 213, 340-342. (doi:10.1126/science.213.4505.340)
11. Cochran, D. G. 1985 Nitrogen excretion in cockroaches. Annu. Rev. Entomol. 30, 29-49. (doi:10.1146/annurev.en. 30.010185.000333)
12. Cole, J. R., Chai, B., Farris, R. J., Wang, Q., Kulam, S. A., McGarrell, D. M., Garrity, G. M. & Tiedje, J. M. 2005 The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis. Nucleic Acids Res. 33, 294-296. (doi:10.1093/nar/gki038)
13. Davidson, S. K. & Stahl, D. A. 2006 Transmission of nephridial bacteria of the earthworm Eisenia fetida. Appl. Environ. Microbiol. 72, 769-775. (doi:10.1128/AEM.72.1. 769-775.2006)
14. De Beer, D., Schramm, A., Santegoeds, C. M. & Kühl, M. 1997 A nitrite microsensor for profiling environmental biofilms. Appl. Environ. Microbiol. 63, 9736-9777.
15. Denton, E. J. 1974 On buoyancy and the lives of modern and fossil cephalopods. Proc. R. Soc. B 185, 273-299. (doi:10.1098/rspb.1974. 0020)
16. Dubilier, N., Amann, R., Erseus, C., Muyzer, G., Park, S. Y., Giere, O. & Cavanaugh, C. M. 1999 Phylogenetic diversity of bacterial endosymbionts in the gutless marine oligochete Olavius loisae (Annelida). Mar. Ecol. Prog. Ser. 178, 271-280.
17. Dröge, S., Fröhlich, J., Radek, R. & König, H. 2006 Spirochaeta coccoides sp nov., a novel coccoid spirochete from the hindgut of the termite Neotermes castaneus. Appl. Environ. Microbiol. 72, 392-397. (doi:10.1128/AEM.721. 1.392-397.2006)
18. Felbeck, H., Childress, J. J. & Somero, G. N. 1981 Calvin-Benson enzymes in animals from suplhide-rich habitats. Nature 293, 291-293. (doi:10.1038/293291a0)
19. Felsenstein, J. 2002 PHYLIP (Phylogeny Inference Package), 3.6a3 edn. Seattle, WA: Department of Genome Sciences, University of Washington.
20. Fracek, S. P. & Stolz, J. F. 1985 Spirochaeta bajacaliforniensis sp. from a microbial mat community at Laguna Figueroa, Baja California Norte, Mexico. Arch. Microbiol. 142, 317-325. (doi:10.1007/BF00491897)
21. Hillis, D. M. & Bull, J. J. 1993 An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst. Biol. 42, 182-192. (doi:10. 2307/2992540)
22. Holmes, A. J., Costello, A., Lidstrom, M. E. & Murrell, J. C. 1995 Evidence that particulate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiol. Lett. 132, 203-208. (doi:10. 1111/j.1574-6968.1995.tb07834.x)
23. Huber, T., Faulkner, G. & Hugenholtz, P. 2004 BELLEROPHON: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20, 2317-2319. (doi:10.1093/bioinformatics/bth226)
24. Kowalchuck, G. A. & Stephen, J. R. 2001 Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu. Rev. Microbiol. 55, 485-529. (doi:10.1146/annurev.micro. 55.1.485)
25. Lilbum, T. G., Kim, K. S., Ostrom, N. E., Byzek, K. R., Leadbetter, J. R. & Breznak, J. A. 2001 Nitrogen fixation by symbiotic and free-living spirochetes. Science 292, 2495-2498. (doi:10.1126/science.1060281)
26. Ludwig, W. 2004 ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363-1371. (doi:10.1093/nar/ gkh293)
27. Luyten, Y., Raymond, L., McMahon, G., Lechene, C. & Distel, D. 2006 Quantitative imaging of intracellular symbiotic N-fixation in the wood-boring bivalve Lyrodus pedicellatus (Bivalvia: Teredinidae). In 5th ISS Congress 2006 Proceedings, p. 45.
28. Magot, M., Fardeau, M. L., Arnauld, O., Lanau, C., Ollivier, B., Thomas, P. & Patel, B. K. C. 1997 Spirochaeta smaragdinae sp. nov, a new mesophilic strictly anaerobic spirochete from an oil field. FEMS Microbiol. Lett. 155, 185-191. (doi:10.1111/j.1574-6968.1997.tb13876.x)
29. Mangold, K., Bidder, A. M. & Boletsky, S. V. 1989 Appareils excréteurs et excrétion. In Traité de zoologie: Anatomie, Sytsématique, Biologie (ed. P. P. Grassé), pp. 437-457. Paris, France: Masson.
30. Martin, A. W. 1983 Excretion. In The Mollusca, part 2, physiology (ed. K. M. Wilbur), pp. 353-382. New York, NY: Academic press.
31. McFall-Ngai, M. J. 2002 Unseen forces: the influence of bacteria on animal development. Dev. Biol. 242, 1-14. (doi:10.1006/dbio.2001. 0522)
32. McFall-Ngai, M. J. & Ruby, E. G. 2000 Developmental biology in marine invertebrate symbioses. Curr. Opin. Microbiol. 3, 603-607. (doi:10.1016/S1369-5274(00) 00147-8)
33. Muyzer, G., Teske, A., Wirsen, C. O. & Jannasch, H. W. 1995 Phylogenetic relationships of Thiomicrospira species and their identification in deep sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch. Microbiol. 164, 165-172.
34. Norman, M. D. 2000 Cephalopods: a world guide. Frankfurt, Germany: IKAN publishing.
35. Pace, N. R. 1997 A molecular view of microbial diversity and the biosphere. Science 276, 734-740. (doi:10.1126/ science.276.5313.734)
36. Pearson, W. R. & Lipman, D. J. 1988 Improved tools for biological sequence comparison. Proc. Natl. Acad. Sci. USA 85, 2444-2448. (doi:10.1126/science.276.5313.734)
37. Pernice, M., Pichon, D., Domart-Coulon, I., Favet, J. & Boucher-Rodoni, R. 2007 Primary co-culture as a complementary approach to explore the diversity of bacterial associations in marine invertebrates: the example of Nautilus macromphalus (Cephalopoda:Nautiloidea). Mar. Biol. 150, 749-757. (doi:10.1007/s00227-006-0413-2)
38. Pernthaler, A., Pernthaler, J. & Amann, R. 2002 Fluorescence in situ hybridization and catalysed reporter deposition for the identification of marine bacteria. Appl. Environ. Microbiol. 68, 3094-3101. (doi:10.1128/AEM. 68.6.3094-3101.2002)
39. Pichon, D., Gaia, V., Norman, M. D. & Boucher-Rodoni, R. 2005 Phylogenetic diversity of epibiotic bacteria in the accessory nidamental glands of squids (Cephalopoda: Loliginidae and Idiosepiidae). Mar. Biol. 147, 1323-1332. (doi:10.1007/s00227-005-0014-5)
40. Prescott, L., Harley, J. & Klein, D. (eds) 2003 Microbiologie 5ème édn. Bruxelles, Belgium: De Boeck Université.
41. Purkhold, U., Pommerening-Roser, A., Juretschko, S., Schmid, M. C., Koops, H. P. & Wagner, M. 2000 Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Appl. Environ. Microbiol. 66, 5368-5382. (doi:10.1128/ AEM.66.12.5368-5382.2000)
42. Ritalahti, K. M. & Loffler, F. E. 2004 Characterisation of novel free-living pleomorphic spirochetes (FLiPS), abstr. 539. In 10th Int. Symp. Microbiol. Ecol. Int. Soc. Microbiol. Ecol., Geneva, Switzerland.
43. Rotthauwe, J. H., Witzel, K. P. & Liesack, W. 1997 The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl. Environ. Microbiol. 63, 4704-4712.
44. Sasaki, T., Kawamura, M. & Ishikawa, H. 1996 Nitrogen recycling in the brown planthopper, Nilaparvata lugens: involvement of yeast-like endosymbionts in uric acid metabolism. J. Insect Physiol. 42, 125-129. (doi:10.1016/ 0022-1910(95)00086-0)
45. Scala, D. J. & Kerkhof, L. J. 1998 Nitrous oxide reductase (nosZ) gene-specific PCR primers for detection of denitrifiers and three nosZ genes from marine sediments. FEMS Microbiol. Lett. 162, 61-68. (doi:10.1111/j.1574-6968.1998.tb12979.x)
46. Schipp, R. & Martin, A. W. 1987 The excretory system of Nautilus. In Nautilus the biology and Paleobiology of a living fossil (eds W. B. Saunders & N. H. Landman), pp. 281-304. New York, NY: Plenum Press.
47. Schipp, R., Martin, A. W., Liebermann, H. & Magnier, Y. 1985 Cytomorphology and function of pericardial appendages of Nautilus (Cephalopoda, Tetrabranchiata). Zoomorphology 105, 16-29. (doi:10.1007/BF00312069)
48. Schipp, R., Chung, Y. S. & Arnold, J. M. 1990 Symbiotic bacteria in the coelom of Nautilus (Cephalopoda, Tetrabranchiata). J. Ceph. Biol. 1, 59-74.
49. Schramm, A., Davidson, S. K., Dodsworth, J. A., Drake, H. L., Stahl, D. A. & Dubilier, N. 2003 Acidovorax-like symbionts in the nephridia of earthworms. Environ. Microbiol. 5, 804-809. (doi:10.1046/j.1462- 2920.2003.00474.x)
50. 2 and temperature on oxygen uptake in Nautilus pompilius. J. Comp. Physiol. 170, 231-236.
51. Strous, M., Fuerst, J. A., Kramer, E. H., Logemann, S., Muyzer, G., van de Pas-Schoonen, K. T., Webb, R., Kuenen, J. G. & Jetten, M. S. 1999 Missing lithotroph identified as new planctomycete. Nature 400, 446-449. (doi:10.1038/22749)
52. Tayasu, I., Sugimoto, A., Wada, E. & Abe, T. 1994 Xylophagous termites depending on atmospheric nitrogen. Naturwissenschaften 81, 229-231. (doi:10.1007/BF0113 8550)
53. Teske, A., Alm, E., Regan, J. M., Toze, S., Rittmann, B. E. & Stahl, D. A. 1994 Evolutionary relationships among ammonia- and nitrite-oxidizing bacteria. J. Bacteriol. 176, 6623-6630.
54. van Borm, S., Buschinger, A., Boomsma, J. J. & Billen, J. 2002 Tetraponera ants have gut symbionts related to nitrogen-fixing root-nodule bacteria. Proc. R. Soc. B 269, 2023-2027. (doi:10.1098/rspb.2002.2101)
55. Wallner, G., Amann, R. & Beisker, W. 1993 Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry 14, 136-143. (doi:10.1002/ cyto.990140205)
56. Woyke, T. et al. 2006 Symbiosis insights through metagenomic analysis of a microbial consortium. Nature 443, 950-955. (doi:10.1038/nature05192)
57. Zhou, J., Bruns, M. A. & Tiedje, M. 1996 DNA recovery from soils of diverse composition. Appl. Environ. Microbiol. 62, 316-322.