Possible Roles of Sulfur-Containing Amino Acids in a Chemoautotrophic Bacterium-Mollusc Symbiosis

Biological Bulletin

Volumn 205, Issue 3, 2003, Pages 331-338

  Joyner, Joanna L ^a,b   Peyer, Suzanne M ^a   Lee, Raymond W ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b 223 Bartram Hall ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BACTERIUM; MOLLUSC; SULFUR; SYMBIOSIS;

ANIMALIA; BACTERIA (MICROORGANISMS); BIVALVIA; EUKARYOTA; GEUKENSIA DEMISSA; INVERTEBRATA; LIMATULA; MOLLUSCA; PROKARYOTA; SOLEMYA VELUM; YOLDIA LIMATULA;

EID: 0346333371     PISSN: 00063185     EISSN: None     Source Type: Journal    
DOI: 10.2307/1543296     Document Type: Article

References (63)

1. Alberic, P., and J. Boulegue. 1990. Unusual amino compounds in the tissues of Calyptogena phaseoliformis (Japan Trench): possible link to symbiosis. Prog. Oceanogr. 24: 89-101.
2. Allen, J. A., and M. R. Garrett. 1971. Taurine in marine invertebrates. Adv. Mar. Biol. 9: 205-253.
3. Allen, J. A., and M. R. Garrett. 1972. Studies on taurine in the euryhaline bivalve Mya arenaria. Comp. Biochem. Physiol. 41A: 307-317.
4. Allen, K., and J. Awapara. 1960. Metabolism of sulfur amino acids in Mytilus edulis and Rangia cuneata. Biol. Bull. 118: 173-182.
5. 2 driven by sulphide and thiosulphate oxidation in the bacterial symbiont-containing clam Solemya reidi. J. Exp. Biol. 133: 1-31.
6. Bender, D. A. 1975. Amino Acid Metabolism. John Wiley & Sons, New York.
7. Bishop, S. H., L. L. Ellis, and J. M. Burcham. 1983. Amino acid metabolism in molluscs. Pp. 243-327 in The Mollusca: Metabolic Biochemistry and Molecular Biomechanics, P. W. Hochachka, ed. Academic Press, New York.
8. Burnap, R. L., and R. K. Trench. 1989. The biogenesis of the cyanellae of Cyanophora paradoxa. II. Pulse-labeling of cyanellar polypeptides in the presence of transcriptional and translational inhibitors. Proc. R. Soc. Lond. B 238: 73-87.
9. Carrico, R. J., W. E. Blumberg, and J. Peisach. 1978. The reversible binding of oxygen to sulfhemoglobin. J. Biol. Chem. 253: 7212-7215.
10. Cavallini, D., B. Mondovi, and C. de Marco. 1963. Hypotaurine and thiotaurine. Biochem. Prep. 10: 72-75.
11. Cavallini, D., R. Scandurra, S. Dupré, G. Federici, L. Santoro, G. Ricci, and D. Barra. 1976. Alternative pathways of taurine biosynthesis. Pp. 59-66 in Taurine, R. J. Huxtable and A. Barbeau, eds. Raven Press, New York.
12. Cavanaugh, C. M. 1983. Symbiotic chemoautotrophic bacteria in marine invertebrates from sulphide-rich habitats. Nature 302: 58-61.
13. Cavanaugh, C. M. 1994. Microbial symbiosis: patterns of diversity in the marine environment. Am. Zool. 34: 79-89.
14. Chien, C.-C., E. R. Leadbetter, and W. Godchaux, III. 1999. Rhodoccus spp. utilize taurine (2-aminoethanesulfonate) as sole source of carbon, energy, nitrogen, and sulfur for aerobic respiratory growth. FEMS Microbiol. Lett. 176: 333-337.
15. Conway, N. M., and J. E. McDowell Capuzzo. 1992. High taurine levels in the Solemya velum symbiosis. Comp. Biochem. Physiol. 102B: 175-185.
16. Conway, N. M., B. L. Howes, J. E. McDowell Capuzzo, R. D. Turner, and C. M. Cavanaugh. 1992. Characterization and site description of Solemya borealis (Bivalvia: Solemyidae), another bivalve-bacteria symbiosis. Mar. Biol. 112: 601-613.
17. Cook, A. M., H. Laue, and F. Junker. 1999. Microbial desulfonation. FEMS Microbiol. Rev. 22: 399-419.
18. Denis, W., and L. Reed. 1927. The action of blood on sulfides. J. Biol. Chem. 72: 385-394.
19. Doeller, J. E., D. W. Kraus, J. M. Colacino, and J. B. Wittenberg. 1988. Gill hemoglobin may deliver sulfide to bacterial symbionts of Solemya velum (Bivalvia, Mollusca). Biol. Bull. 175: 388-396.
20. Douglas, A. E., L. B. Minto, and T. L. Wilkinson. 2001. Quantifying nutrient production by the microbial symbionts in an aphid. J. Exp. Biol. 204: 349-358.
21. Felbeck, H. 1983. Sulfide oxidation and carbon fixation by the gutless clam Solemya reidi: an animal-bacteria symbiosis. J. Comp. Physiol. 152B: 3-11.
22. 2 fixation in the hydrothermal vent tube worm Riftia pachyptila (Jones). Physiol. Zool. 58: 272-281.
23. Felbeck, H., J. J. Childress, and G. N. Somero. 1981. Calvin-Benson cycle and sulphide oxidation enzymes in animals from sulphide-rich habitats. Nature 293: 291-293.
24. Fenchel, T. M., and R. J. Riedl. 1970. The sulfide system: a new biotic community underneath the oxidized layer of marine sand bottoms. Mar. Biol. 7: 255-268.
25. Frey, R. W. 1968. The Lebensspuren of some common marine invertebrates near Beaufort, North Carolina. I. Pelecypod burrows. J. Paleontol. 42: 570-574.
26. Huxtable, R. J. 1992. Physiological actions of taurine. Physiol. Rev. 72: 101-163.
27. Jacobsen, J. G., and L. H. Smith, Jr. 1968. Biochemistry and physiology of taurine and taurine derivatives. Physiol. Rev. 48: 424-511.
28. Julian, D., and A. J. Arp. 1992. Sulfide permeability in the marine invertebrate Urechis caupo. J. Comp. Physiol. 162B: 59-67.
29. King, J. E., and J. P. Quinn. 1997. The utilization of organosulphonates by soil and freshwater bacteria. Lett. Appl. Microbiol. 24: 474-478.
30. 552 in gills of Solemya reidi (Mollusca). Biol. Bull. 182: 435-443.
31. Kredich, N. M. 1996. Biosynthesis of cysteine. Pp. 514-527 in Escherichia coli and Salmonella: Cellular and Molecular Biology, F. C. Neidhardt, ed. ASM Press, Washington, D.C.
32. Krueger, D. M. 1996. Ecology and evolution of Solemya spp., marine bivalves living in symbiosis with chemoautotrophic bacteria. Ph.D. dissertation. Harvard University, Cambridge, MA.
33. Lee, P. L. Y., and R. H. Slocum. 1988. A high-resolution method for amino acid analysis of physiological fluids containing mixed disulfides. Clin. Chem. 34: 719-723.
34. Lee, R. W., and J. J. Childress. 1994. Assimilation of inorganic nitrogen by marine invertebrates and their chemoautotrophic and methanotrophic symbionts. Appl. Environ. Microbiol. 60: 1852-1858.
35. Lee, R. W., E. V. Thuesen, and J. J. Childress. 1992. Ammonium and free amino acids as nitrogen sources for the chemoautotrophic symbiosis Solemya reidi Bernard (Bivalvia: Protobranchia). J. Exp. Mar. Biol. Ecol. 158: 75-91.
36. Lee, R. W., J. J. Childress, and N. T. Desaulniers. 1997. The effects of exposure to ammonia on ammonia and taurine pools of the symbiotic clam Solemya reidi. J. Exp. Biol. 200: 2797-2805.
37. Lee, R. W., J. J. Robinson, and C. M. Cavanaugh. 1999. Pathways of inorganic nitrogen assimilation in chemoautotrophic bacteria-marine invertebrate symbioses: expression of host and symbiont glutamine synthetase. J. Exp. Biol. 202: 289-300.
38. Lovatt Evans, C. 1967. The toxicity of hydrogen sulphide and other sulphides. Q. J. Exp. Physiol. 52: 231-248.
39. Nicholls, P. 1975. The effect of sulphide on cytochrome aa3: isoteric and allosteric shifts of the reduced alpha-peak. Biochim. Biophys. Acta 396: 24-35.
40. Pierce, S. K. 1982. Invertebrate cell volume control mechanisms: a coordinated use of intracellular amino acids and inorganic ions as osmotic solute. Biol. Bull. 163: 405-419.
41. Powell, M. A., and A. J. Arp. 1989. Hydrogen sulfide oxidation by abundant nonhemoglobin heme compounds in marine invertebrates from sulfide-rich habitats. J. Exp. Zool. 249: 121-132.
42. Powell, M. A., and G. N. Somero. 1985. Sulfide oxidation occurs in the animal tissue of the gutless clam, Solemya reidi. Biol. Bull. 169: 164-181.
43. Powell, M. A., and G. N. Somero. 1986. Hydrogen sulfide oxidation is coupled to oxidative phosphorylation in mitochondria of Solemya reidi. Science 233: 563-566.
44. Pranal, V., A. Fiala-Médioni, and J.-C. Colomines. 1995. Amino acid and related compound composition in two symbiotic mytilid species from hydrothermal vents. Mar. Ecol. Prog. Ser. 119: 155-166.
45. Pruski, A. M. 2001. Carrier of reduced sulfur is a possible role for thiotaurine in symbiotic species from hydrothermal vents with thiotrophic symbionts. Hydrobiologia 461: 9-13.
46. Pruski, A. M., A. Fiala-Médioni, and J.-C. Colomines. 1997. High amounts of sulphur-amino acids in three symbiotic mytilid bivalves from deep benthic communities. C. R. Acad. Sci. Paris. 320: 791-796.
47. Pruski, A. M., A. Fiala-Médioni, R. Prodon, and J.-C. Colomines. 2000. Thiotaurine is a biomarker of sulfide-based symbiosis in deep-sea bivalves. Limnol. Oceanogr. 45: 1860-1867.
48. 12C: further evidence of nonphotosynthetic food sources. Science 213: 338-339.
49. Rees, T. A. V. 1987. The green hydra symbiosis and ammonium. I. The role of the host in ammonium assimilation and its possible regulatory significance. Proc. R. Soc. Lond. B. 229: 299-314.
50. Reichenbecher, W., and J. C. Murrell. 1999. Linear alkanesulfonates as carbon and energy sources for gram-positive and gram-negative bacteria. Arch. Microbiol. 171: 430-438.
51. Reitzer, L. J. 1996. Ammonia assimilation and the biosynthesis of glutamine, glutamate, aspartate, asparagine, L-alanine, and D-alanine. Pp. 391-407 in Escherichia coli and Salmonella: Cellular and Molecular Biology, F. C. Neidhardt, ed. ASM Press, Washington, D.C.
52. Rice, M. A., and G. C. Stephens. 1988. Influx, net flux and transepithelial flux of amino acids in the hardshell clam Mercenaria mercenaria (Linne): influence of salinity. Comp. Biochem. Physiol. 89A: 631-636.
53. Ruby, E. G., C. O. Wirsen, and H. W. Jannasch. 1981. Chemolithotrophic sulfur-oxidizing bacteria from the Galápagos Rift hydrothermal vents. Appl. Environ. Microbiol. 42: 317-324.
54. Seitz, A. P., E. R. Leadbetter, and W. Godehaux, III. 1993. Utilization of sulfonates as sole sulfur sources by soil bacteria including Comamonas acidovorans. Arch. Microbiol. 159: 440-444.
55. Smiley, D. W., and B. J. Wilkinson. 1983. Survey of taurine uptake and metabolism in Staphylococcus aureus. J. Gen. Microbiol. 129: 2421-2428.
56. 12C ratios in tissues of Pogonopltora indicate unusual nutrition and metabolism. Nature 293: 616-620.
57. Stapley, E. O., and R. L. Starkey. 1970. Decomposition of cysteic acid and taurine by soil micro-organisms. J. Gen. Microbiol. 63: 77-84.
58. Stauffer, G. V. 1996. Biosynthesis of serine, glycine, and one-carbon units. Pp. 506-513 in Escherichia coli and Salmonella: Cellular and Molecular Biology, F. C. Neidhardt, ed. ASM Press, Washington, D.C.
59. Svenson, A. 1980. A rapid and sensitive spectrophotometric method for determination of hydrogen sulfide with 2,2′-dipyridyl disulfide. Anal. Biochem. 107: 51-55.
60. Wang, J. T., and A. E. Douglas. 1999. Essential amino acid synthesis and nitrogen recycling in an alga-invertebrate symbiosis. Mar. Biol. 135: 219-222.
61. Willason, S. W., and K. S. Johnson. 1986. A rapid, highly sensitive technique for the determination of ammonia in seawater. Mar. Biol. 91: 285-290.
62. Yancey, P. H., M. E. Clark, S. C. Hand, R. D. Bowlus, and G. N. Somero. 1982. Living with water stress: evolution of osmolyte systems. Science 217: 1214-1222.
63. Yin, M., H. R. Palmer, A. L. Fyfe-Johnson, J. J. Bedford, R. A. J. Smith, and P. H. Yancey. 2000. Hypotaurine, N-methyltaurine, taurine, and glycine betaine as dominant osmolytes of vestimentiferan tubeworms from hydrothermal vents and cold seeps. Physiol. Biochem. Zool. 73: 629-637.