Skip to main content
Log in

Chemoautotrophic, sulfur-oxidizing symbiotic bacteria on marine nematodes: Morphological and biochemical characterization

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The marine, free-living Stilbonematinae (Nematoda: Desmodorida) inhabit the oxygen sulfide chemocline in marine sands. They are characterized by an association with ectosymbiotic bacteria. According to their ultrastructure the bacteria are Gram-negative and form morphologically uniform coats that cover the entire body surface of the worms. They are arranged in host-genus or host-species specific patterns: cocci form multilayered sheaths, rods, and crescent- or filament-shaped bacteria form monolayers. The detection of enzymes associated with sulfur metabolism and of ribulose-1,5 bisphosphate carboxylase oxygenase, as well as elemental sulfur in the bacteria indicate a chemolithoautotrophic nature of the symbionts. Their reproductive patterns appear to optimize space utilization on the host surface: vertically standing rods divide by longitudinal fission, whereas other bacteria form non-septate filaments of up to 100 μm length.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Blome D, Riemann F (1987) A sediment agglutination on females of the free-living marine nematode Desmodora schulzi. Helgoländer Meeresunters 41:113–119.

    Google Scholar 

  2. Braunegg G, Sonnleitner B, Lafferty RM (1978) A rapid gas chromatographic method for the determination of poly-β-hydroxybutyric acid in microbial biomass. European J Appl Microbiol Biotechnol 6:29–37

    Google Scholar 

  3. Cavanaugh C (1985) Symbioses of chemoautotrophic bacteria and marine invertebrates from hydrothermal vents and reducing sediments. Biol Soc Wash Bull 6:373–388

    Google Scholar 

  4. Cavanaugh CM (1983) Symbiotic chemoautotrophic bacteria in marine invertebrates from sulphide-rich habitats. Nature 302:58–61

    Google Scholar 

  5. Cavanaugh CM, Gardiner SL, Jones ML, Jannasch HW, Waterbury JB (1981) Procaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: Possible chemoautotrophic symbionts. Science 213:340–342

    Google Scholar 

  6. Charles AM, Suzuki I (1965) Sulfite oxidase of a facultative autotroph, Thiobacillus novellus. Biochem Biophys Res Commun 19:686–690

    Google Scholar 

  7. Charles AM, Suzuki I (1966) Purification and properties of sulfite: Cytochrome c oxidoreductase from Thiobacillus novellus. Biochem Biophys Acta 128:522–534

    Google Scholar 

  8. Cobb NA (1920) One hundred new nemas. Contrib Sci Nematol 9:217–343

    Google Scholar 

  9. Conway N, McDowell Capuzzo J (1990) The use of biochemical indicators in the study of trophic interactions on animal-bacteria symbioses: Solemya velum, a case study. In: Barnes M, Gibson RN (eds) Trophic relationships in the marine environment. Proc. 24th Europ Mar Biol Symp Aberdeen University Press, Aberdeen, pp 553–564

    Google Scholar 

  10. Dando PR, Austen MC, Burke RA Jr, Kendall MA, Kennicutt MC II, Judd AG, Moore DC, O'Hara SCM, Schmaljohann R, Southward AJ (1991) Ecology of a North Sea pockmark with an active methane seep. Mar Ecol Progr Ser 70:49–63

    Google Scholar 

  11. Desbruyeres D, Gaill F, Laubier L, Prieur D, Rau GH (1983) Unusual nutrition of the “Pompeii worm” Alvinella pompejana (polychaetous annelid) from a hydrothermal vent environment: SEM, TEM, 13C and 15N evidence. Mar Biol 75:201–205

    Google Scholar 

  12. Dubochet J, McDowell AW, Menge B, Schmid EN, Lickfeld KG (1983) Electron microscopy of frozen-hydrated bacteria. J Bacteriol 155:381–390

    Google Scholar 

  13. Els HJ, Krecek RC (1990) Ultrastructure of filamentous microorganisms associated with Zebra cyathostomes. Microb Ecol 19:187–198

    Google Scholar 

  14. Farkas W, Macleod RW, Fridovich I, Handler P (1962) Sulfite cytochrome c reductase. Meth Enzymol 5:983–986

    Google Scholar 

  15. Felbeck H (1981) Chemoautotrophic potential of the hydrothermal vent tube worm, Riftia pachyptila Jones (Vestimentifera). Science 213:336–338

    Google Scholar 

  16. Felbeck H, Childress JJ, Somero GN (1981) Calvin-Benson cycle and sulphide oxidation enzymes in animals from sulphide-rich habitats. Nature 293:291–293

    Google Scholar 

  17. Felbeck H, Liebezeit G, Dawson R, Giere O (1983) CO2 fixation in tissues of marine oligochaetes (Phallodrilus leucodermatus and P. planus) containing symbiotic, chemoautotrophic bacteria. Mar Biol 75:187–191

    Google Scholar 

  18. Fenchel T, Finlay BJ (1989) Kentrophoros: a mouthless ciliate with a symbiotic kitchen garden. Ophelia 30:75–93

    Google Scholar 

  19. Fisher CR (1990) Chemoautotrophic and methanotrophic symbioses in marine invertebrates. Rev Aquat Sci 2:399–436

    Google Scholar 

  20. Foglesong MA, Walker DH, Puffer JS, Markovetz AJ (1975) Ultrastructural morphology of some prokaryotic microorganisms associated with the hindgut of cockroaches. J Bacteriol. 123:336–345

    Google Scholar 

  21. Fraser TW, Gilmour A (1986) Scanning electron microscopy preparation methods: Their influence on the morphology and fibril formation in Pseudomonas fragi (ATCC 4937). J Appl Bacteriol 60:527–533

    Google Scholar 

  22. Gaill F, Desbruyeres D, Prieur D (1987) Bacterial communities associated with Pompeii worms from the east Pacific rise hydrothemal vents. SEM, TEM observations. Microb Ecol 13:129–140

    Google Scholar 

  23. Gerlach SA (1956) Die Nematodenbesiedlung des tropischen Brandungsstrandes von Pernambuco. Brasilianische Meeresnematoden. II. Kieler Meeresforsch 12:202–218

    Google Scholar 

  24. Giere O (1981) The gutless marine oligochaete Phallodrilus leucodermatus. Structural studies on an aberrant tubificid associated with bacteria. Mar Ecol Progr Ser 5:353–357

    Google Scholar 

  25. Giere O, Wirsen CO, Schmidt J, Jannasch HW (1988) Contrasting effects of sulfide and thiosulfate on symbiotic CO2-assimilation of Phallodrilus leucodermatus (Annelida). Mar Biol 97:413–419

    Google Scholar 

  26. Hagström Å, Larsson U, Horstedt P, Normark S (1979) Frequency of dividing cells, and new approach to the determination of bacterial growth rates in aquatic environments. Appl Environ Microbiol 37:805–812

    Google Scholar 

  27. Hempfling WP, Trudinger PA (1967) Purification and some properties of sulfite oxidase from Thiobacillus neapolitanus. Archiv für Mikrobiologie 59:149–157

    Google Scholar 

  28. Inglis WG (1968) Interstitial nematodes from St. Vincent's Bay, New Caledonia. Editions Fondat, Singer-Polignac 2:29–74

    Google Scholar 

  29. Jensen P (1987) Feeding ecology of free-living aquatic nematodes. Mar Ecol Prog Ser 35:187–196

    Google Scholar 

  30. Jørgensen BB (1977) The sulfur cycle of a coastal marine sediment (Limfjorden, Denmark). Limnol Oceanogr 22:814–832

    Google Scholar 

  31. Lauren DR, Watkinson JH (1985) Elemental sulfur analysis using high-performance liquid chromatography on 10 μm rigid polymer particles. J Chromatogr 348:317–320

    Google Scholar 

  32. Lawrey NH, Jam V, Jensen TE (1981) Identification of the sulfur inclusion bodies in Beggiatoa alba by energy dispersive X-ray microanalysis. Curr Microbiol 6:71–74

    Google Scholar 

  33. Nebelsick M, Novak R, Ott JA (1992) A new glandular sensory organ in Catanema sp. (Nematoda, Stilbonematinae). Zoomorphology, 112:17–26

    Google Scholar 

  34. Nelson DC, Castenholz RW (1981) Use of reduced sulfur compounds by Beggiatoa sp. J Bacteriol 147:140–154

    Google Scholar 

  35. Oeschger R, Schmaljohann R (1988) Association of various types of epibacteria with Halicryptus spinulosus (Priapulida). Mar Ecol Prog Ser 48:285–293

    Google Scholar 

  36. Ott J, Rieger G, Rieger R, Enderes F (1982) New mouthless interstitial worms from the sulfide system: Symbiosis with prokaryotes. P.S.Z.N. I: Mar Ecol 3:313–333

    Google Scholar 

  37. Ott JA, Novak R (1989) Living at an interface: Meiofauna at the oxygen/sulide boundary of marine sediments. In: Ryland JS, Tyler PA (eds) Reproduction, genetics and distribution of marine organisms. Olsen & Olsen, Fredensbourg, Denmark, pp 415–421

    Google Scholar 

  38. Ott JA, Novak R, Schiemer F, Hentschel U, Nebelsick M, Polz M (1991) Tackling the sulfide gradient: A novel strategy involving marine nematodes and chemoautotrophic ectosymbionts. P.S.Z.N. I. Mar Ecol 12:261–279

    Google Scholar 

  39. Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948

    Google Scholar 

  40. Powell EN, Crenshaw M, Rieger RM (1979) Adaptions to sulfide in the meiofauna of the sulfide system. I. 35S-sulfide accumulation and the presence of a sulfide detoxification system. J Exp Mar Biol Ecol 37:57–76

    Google Scholar 

  41. Schiemer F, Novak R, Ott J (1990) Metabolic studies on thiobiotic free-living nematodes and their symbiotic microorganisms. Mar Biol 106:129–137

    Google Scholar 

  42. Schmidt TM, Ariell B, Cohen Y, Padan E, Strohl WR (1987) Sulfur metabolism in Beggiatoa alba. J Bacteriol 169:5466–5472

    Google Scholar 

  43. Shivley JM, Ball F, Brown DH, Saunders RE (1973) Functional organelles in prokaryotes: Polyhedral inclusions (carboxysomes) of Thiobacillus neapolitanus. Science 182:584–586

    Google Scholar 

  44. Southward AJ, Southward EC, Dando PR, Barrett RL, Ling L (1986) Chemoautotrophic funcion of bacterial symbionts in small pogonophora J Mar Biol Assoc UK 66:415–437

    Google Scholar 

  45. Steinbüchel A, Schlegel HG (1991) Physiology and molecular genetics of poly (β-hydroxy-alcanoic acid) synthesis in Alcaligenes eutrophus. Mol Microbiol 5:535–542

    Google Scholar 

  46. Swift H, Leser GP (1989) Cytochemical studies on Prochlorophytes: Localization of DNA and ribulose 1,5-bisphosphate carboxylase-oxygenase. J Phycol 25:751–761

    Google Scholar 

  47. Vetter RD (1985) Elemental sulfur in the gills of three species of clams containing chemoautotrophic symbiotic bacteria: A possible inorganic energy storage compound. Mar Biol 88:33–42

    Google Scholar 

  48. Wieser W (1959) Eine ungewöhnliche Assoziation zwischen Blaualgen und freilebenden marinen Nematoden. Österr Bot Z 106:81–87

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Polz, M.F., Felbeck, H., Novak, R. et al. Chemoautotrophic, sulfur-oxidizing symbiotic bacteria on marine nematodes: Morphological and biochemical characterization. Microb Ecol 24, 313–329 (1992). https://doi.org/10.1007/BF00167789

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00167789

Keywords

Navigation