Epidermal ultrastructure and implications for sulfide tolerance in six species of deep-sea polychaetes

Invertebrate Biology

Volumn 122, Issue 4, 2003, Pages 334-346

  Menon, Jaishri ^a,b   Willsie, Julia K ^a   Tauscher, Andrew ^a   Arp, Alissa J ^a  

^a SAN FRANCISCO STATE UNIVERSITY   (United States)

^b WILLIAM PATERSON UNIVERSITY   (United States)

Author keywords

Annelida; Lamellibrachia; Riftia; Siboglinidae; Sulfide; Sulfide oxidizing bodies; Vestimentifera

Indexed keywords

ANIMALIA; ANNELIDA; DENDROBRANCHIATA; LAMELLIBRACHIA; LAMELLIBRACHIA LUYMESI; METHANOARICIA DENDROBRANCHIATA; OASISIA ALVINAE; PACHYPTILA; POGONOPHORA; POLYCHAETA; RIFTIA; RIFTIA PACHYPTILA; SEEPIOPHILA JONESI; SIBOGLINIDAE; TEVNIA; TEVNIA JERICHONANA; VESTIMENTIFERA;

EID: 0346328272     PISSN: 10778306     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1744-7410.2003.tb00098.x     Document Type: Article

References (54)

1. Arp AJ, Menon JG, & Julian D 1995. Multiple mechanisms for sulfide tolerance in Urechis caupo. Amer. Zool. 35: 132-144.
2. Bagarinao T & Vetter RD 1990. Oxidative detoxification of sulfide by mitochondria of the California killifish Fundulus parvipinnis and the speckled sanddab Citharicthys stigmaeus. J. Comp. Physiol. B160: 519-527.
3. Blake J 2000. A new genus and species of polychaete worm (family Orbiniidae) from methane seeps in the Gulf of Mexico, with a review of the systematics and phylogenetic interrelationships of the genera of Orbiniidae. Cah. Biol. Mar. 41: 435-449.
4. Cary C, Fry B, Felbeck H, & Vetter RD 1989. Multiple trophic resources for a chemoautotrophic community at a cold water brine seep at the base of the Florida Escarpment. Mar. Biol. 100: 411-418.
5. Childress JJ & Fisher CR 1992. The biology of hydrothermal vent animals: Physiology, biochemistry, and autotrophic symbioses. Oceanogr. Mar. Biol. Ann. Rev. 30: 337-441.
6. Corliss JB, Dymond J, Gordon LI, Edmond JM, Herzen RPV, Ballard RD, Green K, Williams D, Bainbridge A, Crane K, & van Andel TH 1979. Submarine thermal springs on the Galapagos Rift. Science 203: 1073-1083.
7. de Duve C & Wattiaux R 1966. Functions of lysosomes. Rev. Physiol. 28: 435-492.
8. Duffy JE & Tyler S 1984. Quantitative differences in mitochondrial ultrastructure of a thiobiotic and an oxybiotic turbellarian. Mar. Biol. 83: 95-102.
9. Ericsson JLE 1969. Mechanism of cellular autotroph. In: Lysosomes in Biology and Pathology, Vol. 2. Dingle JT & Fell HB eds., pp. 345. North Holland Publ., London.
10. Fischer E & Horvath I 1977. Cytochemical studies on the cuticle and epidermis of Tubifex tubifex Mull. with special regard to the localization of polysaccharides, heavy metals and the DAB reactivity. Histochemistry 54: 259-271.
11. Fisher CR 1990. Chemoautotrophic and methanotrophic symbioses in marine invertebrates. Rev. Aquat. Sci. 2: 399-436.
12. Freytag JK, Girguis P, Bergquist DC, Andras JP, Childress JJ, & Fisher CR 2001. Sulfide acquisition by roots of seep tubeworms sustains net chemoautotrophy. Proc. Nat. Acad. Sci. 98: 13408-13413.
13. Gardiner SL & Jones ML 1993. Vestimentifera. In: Microscopic Anatomy of Invertebrates, Vol. 12. Harrison FW & Rice ME, eds., pp. 484. Wiley-Liss, Inc., New York.
14. Gardiner SL, McMullin E, & Fisher CR 2001. Seepiophila jonesi, a new genus and species of vestimentiferan tube worm (Annelida: Pogonophora) from hydrocarbon seep communities in the Gulf of Mexico. Proc. Biol. Soc. Wash. 114: 694-707.
15. Ghadially FN 1988. Ultrastructural Pathology of the Cell and Matrix, 2nd edition. Butterworths, London. 176 pp.
16. Giere O, Rhode B, & Dubilier N 1988. Structural peculiarities of the body wall of Tubificoides benedii (Oligochaeta) and possible relations to its life in sulphidic sediments. Zoomorphology 108: 29-39.
17. Green CR 1981. A clarification of the two types of invertebrate pleated septate junction. Tissue Cell 13: 173-188.
18. Grieshaber MK & Volkel S 1998. Animal adaptations for tolerance and exploitation of poisonous sulfide. Ann. Rev. Physiol. 60: 33-53.
19. Hekinian R, Fevier M, Bischoff JL, Picot P, & Shanks WC 1980. Sulfide deposits from the East Pacific Rise near 21° N. Science 207: 1443-1444.
20. Holland ND & Nealson KH 1978. The fine structure of the echinoderm cuticle and the subcuticular bacteria of echinoderms. Acta Zool. 59: 169-185.
21. Hourdez S & Jouin-Toulmond C 1998. Functional anatomy of the respiratory system of Branchipolynoe species (Polychaeta, Polynoidae), commensal with Bathymodiolus species (Bivalvia, Mytilidae) from deep-sea hydrothermal vents. Zoomorphology 118: 225-233.
22. Hourdez S, Frederick LA, Schernecke A, & Fisher CR 2001. Functional respiratory anatomy of a deep-sea orbiniid polychaete from the Brine Pool NR-1 in the Gulf of Mexico. Invertebr. Biol. 120: 29-40.
23. Hourdez S, Weber RE, Green BN, Kenney JM, & Fisher CR 2002. Respiratory adaptations in a deep-sea orbiniid polychaete from Gulf of Mexico Brine Pool NR-1: Metabolic rates and hemoglobin structure/function relationships. J. Exp. Biol. 205: 1669-1681.
24. Hruban Z, Spargo B, Swift H, Wissler RW, & Kleinfeld RG 1963. Focal cytoplasmic degradation. Am. J. Pathol. 42: 657-683.
25. Jones ML 1981. Riftia pachyptila, new genus, new species, the vestimentiferan tubeworm from the Galapagos Rift geothermal vents. Proc. Biol. Soc. Wash. 93: 1295-1313.
26. _ 1985. On the Vestimentifera, new phylum: six new species, and other taxa, from hydrothermal vents and elsewhere. Bull. Biol. Soc. Wash. 6: 117-158.
27. Jouin C & Gaill F 1990. Gills of hydrothermal vent annelids: Structure, ultrastructure, and functional implications in two alvinellid species. Prog. Oceanog. 24: 59-69.
28. Jouin-Toulmond C, Augustin D, Desbruyères D, & Toulmond A 1996. The gas transfer system in alvinellids (Annelida Polychaeta, Terebellida). Anatomy and ultrastructure of the anterior circulatory system and characterization of a coelomic, intracellular, haemoglobin. Cah. Biol. Mar. 37: 135-151.
29. Julian D & Arp AJ 1992. Sulfide permeability in the marine invertebrate Urechis caupo. J. Comp. Physiol. B162: 59-67.
30. Julian D, Passman WE, & Arp AJ 1996. Water lung and body wall contributions to respiration in an echiuran worm. Respir. Physiol. 106: 187-198.
31. Julian D, Gaill F, Wood E, Arp AJ, & Fisher CR 1999. Roots as a site of hydrogen sulfide uptake in the hydrocarbon seep vestimentiferan Lamellibrachia cf. luymesi J. Exp. Biol. 202: 2245-2257.
32. Juniper SK & Martineu P 1995. Alvinellids and sulfides at hydrothermal vents of the eastern Pacific: A review. Amer. Zool. 35: 174-185.
33. Liberge M, Gros O, & Frenkiel L 2001. Lysosomes and sulfide-oxidizing bodies in the bacteriocytes of Lucina pectinata, a cytochemical and microanalysis approach. Mar. Biol. 139: 401-409.
34. Menon JG & Arp AJ 1992. Morphological adaptations of the respiratory hindgut of a marine echiuran worm. J. Morph. 214: 131-138.
35. _ 1993. The integument of the marine echiuran worm Urechis caupo. Biol. Bull. 185: 440-454.
36. _ 1998. Ultrastructural evidence of detoxification in the alimentary canal of Urechis caupo. Invertebr. Biol. 117(4): 307-317.
37. National Research Council, Division of Medical science, subcommittee on Hydrogen sulfide 1979. Hydrogen sulfide. University Press, Baltimore. 183 pp.
38. Nelson DC & Fisher CR 1995. Chemoautotrophic and methanotrophic endosymbiotic bacteria at deep sea vents and seeps. In: The Microbiology of Deep-sea Hydrothermal Vents. Karl D, ed., pp. 125-167. CRC Press, Inc., New York.
39. Oeschger R & Schmaljohann R 1988. Association of various epibacteria with Halicryptus spinulosus (Priapulida). Mar. Ecol. Prog. Ser. 48: 285-293.
40. Ord MJ & RA Smith 1982. Correlation of mitochondrial form and function in vivo: Microinjection of substrates and nucleotides. Cell Tissue Res. 227: 129-137.
41. Powell MA & Somero GN 1985. Sulfide oxidation occurs in the animal tissue of the gutless clam, Solemya reidi. Biol. Bull. 169: 164-181.
42. _ 1986. Adaptations to sulfide by hydrothermal vent animals: Sites and mechanisms of detoxification and metabolism. Biol. Bull. 171: 274-290.
43. Powell EN, Crenshaw MA, & Rieger RM 1979. Adaptations to sulfide in the meiofauna of the sulfide system. I. 35-S sulfide accumulation and the presence of a sulfide detoxification system. J. Exp. Mar. Biol. Ecol. 37: 57-79.
44. _ 1980. Adaptations to sulfide in sulfide system meiofauna. End products of sulfide detoxification in three turbellarians and a gastrotrich. Mar. Ecol. Prog. Ser. 2: 169-177.
45. Scott KM & Fisher CR 1995. Physiological ecology of sulfide metabolism in hydrothermal vent and cold seep vesicomyid clams and vestimentiferan tube worms. Amer. Zool. 35: 102-111.
46. Sharkey SM, Wilson BM, Moorehead R, & Singh G 1993. Mitochondrial alteration in photodynamic therapy-resistant cells. Cancer Research 53: 4994-4999.
47. Smith EB, Scott KM, Nix ER, Korte C, & Fisher CR 2000. Growth and condition of seep mussels (Bathymodiolus childressi) at a Gulf of Mexico Brine Pool. Ecology 81: 2392-2403.
48. Somero GN, Childress JJ, & Anderson AE 1989. Transport, metabolism, and detoxification of hydrogen sulfide in animals from sulfide-rich environments. Rev. Aquat. Sci. 1: 591-614.
49. Southward EC 1982. Bacterial symbionts in pogonophora. J. Mar. Biol. 62: 889-906.
50. Storch V & Gaill F 1986. Ultrastructural observations of feeding appendages and gills of Alvinella pompejana (Annelida, Polychaeta). Helgol. Meeresunters. 40: 309-319.
51. van der Land J & Norrevang A 1975. The systematic position of Lamellibrachia (Annelida, Vestimentifera). Z. Zool. Syst. Evolutionsforsch. 13: 88-101.
52. Vismann B 1991. Sulfide tolerance: Physiological mechanisms and ecological implications. Ophelia 34(1): 1-27.
53. Volkel S & Grieshaber MK 1996. Mitochondrial sulfide oxidation in Arenicola marina - evidence for alternative electron pathways. Eur. J. Biochem. 235 (1-2): 231-237.
54. Welsch U, Storch V, & Richards S 1984. Epidermal cells. In: Biology of the Integument 1. Invertebrates. Bereiter-Hahn J, Matoltsy AG, & Richards KS, eds., pp. 269-296. Springer-Verlag, New York.