Skip to main content
Log in

Structural and ultrastructural analysis of the gills in the bacterial-bearing species Thyasira falklandica (Bivalvia, Mollusca)

  • Original Paper
  • Published:
Zoomorphology Aims and scope Submit manuscript

Abstract

In this study, the cellular organization of the gill that harbors symbiotic bacteria is described in the thyasirid Thyasira falklandica collected from South Shetlands in Antarctic. Sections of the gills revealed that T. falklandica belongs to the gill type 3, as described by Dufour (Biol Bull, 208:200–212, 2005), with an elongated lateral zone along the frontal-abfrontal axis of the gill filaments. The ciliated and intermediary zones looked similar to those described in symbionts-bearing bivalves. The lateral zone is more complex in T. falklandica than in other Thyasiridae already described. Such a zone is composed of four different cell types. Bacteriocytes are abundant in the frontal and abfrontal positions, while the middle part of the lateral zone is occupied mostly by numerous granule cells devoid of bacteria. All along the lateral zone, TEM and SEM observations show some ciliated cells, which are regularly interspersed between bacteriocytes and/or granule cells. Such cells, according to the long double ciliary roots of their cilia, should have a sensory function. Intercalary cells, which have never been observed between bacteriocytes, are restricted to the middle part of the lateral zone where their expansions overlap the adjacent granule cells. Bacterial symbionts occur only extracellularly among long microvilli differentiated by the bacteriocytes. They are abundant, usually spherical in shape (around 0.7 μm length), and covered by the glycocalix from bacteriocyte microvilli. According to TEM views, the empty vesicles located in the periplasmic space should be sulfur storage, as known for other sulfur-oxidizing symbionts.

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

Fig. 1
Figs. 2–6
Figs. 7–9
Figs. 10–14

Similar content being viewed by others

References

  • Allen JA (1958) On the basic form and adaptations to habitat in the Lucinacea (Eulamellibranchia). Philos Trans R Soc Lond B 684:421–482

    Article  Google Scholar 

  • Cavanaugh CM, Gardiner SL, Jones ML, Jannasch HW, Waterburry JB (1981) Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science 213:340–342

    Article  CAS  PubMed  Google Scholar 

  • Dando PR, Southward AJ (1986) Chemoautotrophy in bivalve Molluscs of the genus Thyasira. J Mar Biol Ass UK 66:915–929

    CAS  Google Scholar 

  • Dando PR, Spiro B (1993) Varying nutritional dependence of the thyasirid bivalves Thyasira sarsi and T. equalis on chemoautotrophic symbiotic bacteria, demonstrated by isotope ratios of tissue carbon and shell carbonate. Mar Ecol Progr Ser 92:151–158

    Article  CAS  Google Scholar 

  • Dando PR, Southward AJ, Southward EC, Terwilliger NB, Terwilliger RC (1985) Sulphur-oxidizing bacteria and haemoglobin in gills of the bivalve mollusk Myrtea spinifera. Mar Ecol Progr Ser 23:85–98

    Article  CAS  Google Scholar 

  • Dell RK (1990) Antarctic Mollusca. With special reference to the fauna of the Ross Sea. R Soc N Z Bull 27:1–311

    Google Scholar 

  • Distel DL, Felbeck H (1987) Endosymbiosis in the lucinid clams Lucinoma aequizonata, Lucinoma annulata, and Lucina floridana: a reexamination of the functional morphology of the gills as bacteria-bearing organs. Mar Biol 96:79–86

    Article  Google Scholar 

  • Distel DL, Felbeck H, Cavanaugh CM (1994) Evidence for phylogenetic congruence among sulfur-oxidizing chemoautotrophic bacterial endosymbionts and their bivalve hosts. J Mol Evol 38:533–542

    Article  CAS  Google Scholar 

  • Dufour SC (2005) Gill anatomy and relationship to chemoautotrophic symbiont presence in the bivalve family thyasiridae. Biol Bull 208:200–212

    Article  PubMed  Google Scholar 

  • Dufour SC, Felbeck H (2003) Sulphide mining by the superextensile foot of symbiotic thyasirid bivalves. Nature 426:65–67

    Article  CAS  PubMed  Google Scholar 

  • Duperron S, Nadalig T, Caprais JC, Sibuet M, Fiala-Médioni A, Amann R, Dubilier N (2005) Dual symbiosis in a Bathymodiolus mussel from a methane seep on the Gabon continental margin (South East Atlantic): 16S rRNA phylogeny and distribution of the symbionts in the gills. Appl Environ Microbiol 71:1694–1700

    Article  CAS  PubMed  Google Scholar 

  • Felbeck H, Childress JJ, Somero GN (1981) Calvin benson cycle and sulphide oxidation enzymes in animals from sulphid-rich habitat. Nature 293:291–293

    Article  CAS  Google Scholar 

  • Fiala-Médioni A, Metivier C (1986) Ultrastructure of the gill of the hydrothermal vent bivalve Calyptogena magnifica, with a discussion of its nutrition. Mar Biol 90:215–222

    Article  Google Scholar 

  • Fischer CH (1990) Chemoautotrophic and methanotrophic symbioses in marine invertebrates. Rev Aquat Sci 2:399–436

    Google Scholar 

  • Frenkiel L, Mouëza M (1995) Gill ultrastructure and symbiotic bacteria in Codakia orbicularis (Bivalvia, Lucinidae). Zoomorphology 115:51–61

    Article  Google Scholar 

  • Frenkiel L, Gros O, Mouëza M (1996) Gill ultrastructure in Lucina pectinata (Bivalvia: Lucinidae) with reference to hemoglobin in bivalves with symbiotic sulphur-oxidizing bacteria. Mar Biol 125:511–524

    Google Scholar 

  • Fujiwara Y, Uematsu K (2002) Microdistribution of two endosymbionts in gill tissue from a hadal thyasirid clam Maorithyas hadalis. Cah Biol Mar 43:341–343

    Google Scholar 

  • Fujiwara Y, Kato C, Masui N, Jujikura K, Kojima S (2001) Dual symbiosis in the cold seep thyasirid clam Maorithyas hadalis from the hadal zone in the japan trench, western pacific. Mar Ecol Progr Ser 214:151–159

    Article  Google Scholar 

  • Gabe M (1968) Techniques histologiques. Masson, Paris

    Google Scholar 

  • Giere O (1985) Structure and position of bacterial endosymbionts in the gill filaments of Lucinidae from Bermuda (Mollusca, Bivalvia). Zoomorphology 105:296–301

    Article  Google Scholar 

  • Glauert AM (1975) Practical methods in electron microscopy. 3 (1): fixation, dehydration and embedding of biological specimens. Elsevier, Amsterdam

    Google Scholar 

  • Glover EA, Taylor JD, Rowden AA (2004) Bathyaustrellia thionipta, a new lucinid bivalve from a hydrothermal vent on the Kermadec ridge, New Zealand and its relationship to shallow-water taxa (Bivalvia: Lucinidae). J Molluscan Stud 70:283–295

    Article  Google Scholar 

  • Gros O, Frenkiel L, Mouëza M (1997) Embryonic, larval, and post-larval development in the symbiotic clam, Codakia orbicularis (Bivalvia : Lucinidae). Invertebr Biol 116:86–101

    Article  Google Scholar 

  • Gros O, Frenkiel L, Mouëza M (1998) Gill filament differentiation and experimental colonization by symbiotic bacteria in aposymbiotic juveniles of Codakia orbicularis (Bivalvia: Lucinidae). Invertebr Reprod Dev 34:219–231

    Google Scholar 

  • Gros O, Liberge M, Felbeck H (2003) Interspecific infection of aposymbiotic juveniles of Codakia orbicularis by various tropical lucinid gill-endosymbionts. Mar Biol 142:57–66

    Google Scholar 

  • Imhoff JF, Sahling H, Süling J, Kath T (2003) 16S rDNA-based phylogeny of sulfur-oxidising bacterial endosymbionts in marine bivalves from cold-seep habitats. Mar Ecol Progr Ser 249:39–51

    Article  CAS  Google Scholar 

  • Lechaire J-P, Frébourg G, Gaill F, Gros O (2006) In situ localization and characterization of sulfur in the thioautotrophic symbiotic model Lucina pectinata (Mollusca: Bivalvia) by cryofixation and EFTEM analysis. Biol Cell 98:163–170

    CAS  PubMed  Google Scholar 

  • Le Pennec M, Diouris M, Herry A (1988) Endocytosis and lysis of bacteria in gill epithelium of Bathymodiolus thermophilus, Thyasira flexuosa, and Lucinella divaricata (Bivalve, Molluscs). J Shellfish Res 7:483–489

    Google Scholar 

  • Liberge M, Gros O, Frenkiel L (2001) Lysosomes and sulfide-oxidizng bodies in the bacteriocytes of Lucina pectinata, a cytochemical and microanalysis approach. Mar Biol 139:401–409

    Article  CAS  Google Scholar 

  • McKiness ZP, Mc Mullin ER, Fisher CR, Cavanaugh CM (2005) A new bathymiodoline mussel symbiosis at the Juan de Fuca hydrothermal vents. Mar Biol 148:109–116

    Article  Google Scholar 

  • Narchi W, Domaneschi O, Passos FD (2002) Bivalves Antárticos e Subantárticos coletados durante as Expedições Científicas Brasileiras à Antártica I a IX (1982–1991). Rev Brasiliana Zool 19:645–675

    Google Scholar 

  • Owen G, McCrae JM (1976) Further studies on the latero-frontal tracts of bivalves. Proc R Soc Lond B 194:527–544

    Article  Google Scholar 

  • Read KRH (1962) The hemoglobin of the bivalved Mollusc, Phacoides pectinatus Gmelin. Biol Bull 123:605–661

    Article  CAS  Google Scholar 

  • Reid RGB (1990) Evolutionnary implications of sulphide-oxidizing symbioses in bivalves. In: Morton B (ed) The Bivalvia—Proceedings of a memorial symposium in Honour of Sir CM Yonge, Edinburgh, 1986. Hong Kong University Press, Hong Kong, pp 127–140

    Google Scholar 

  • Smith EA (1885) Report on the Lamellibranchiata collected by H.M.S. Challenger during the years 1873–1876. Report on the Scientific Results of the Voyage of H.M.S. Challenger. Zoology 13:1–341

    Google Scholar 

  • Southward EC (1986) Gill symbionts in thyasirids and other bivalve mollusks. J Mar Biol Ass UK 66:889–914

    Google Scholar 

  • Spiro B, Greenwood PB, Southward AJ, Dando PR (1986) 13C/12C ratio in marine invertebrates from reducing sediments: confirmation of nutritional importance of chemoautotrophic endosymbiotic bacteria. Mar Ecol Progr Ser 28:233–240

    Article  CAS  Google Scholar 

  • Taylor JD, Glover EA (2000) Functional anatomy, chemosymbiosis and evolution of the Lucinidae. In: Harper EM, Taylor JD, Crame A (eds) The evolutionary biology of the bivalvia. Geol Soc Lond Spec Publ 177:207–225

  • Williams ST, Taylor JD, Glover EA (2003) Molecular phylogeny of the Lucinoidea (Bivalvia): non-monophyly and separate acquisition of bacterial symbiosis. J Molluscan Stud 70:187–202

    Article  Google Scholar 

Download references

Acknowledgements

This work was carried out within the Brazilian Antarctic Programme (PROANTAR) with financial and logistic support provided by the CNPq, SECIRM, the Brazilian Navy and Brazilian Air Force; it was also supported by scholarships of FAPESP and of “Pós-Graduação, Área Zoologia, IBUSP”. Our thanks are due to E. Mattos, W. Caldeira and M. V. Cruz (IBUSP), who provided assistance in the techniques of microscopy, and Dr. J. R. M. C. da Silva (USP) for their personal engagements and encouragement in field and laboratory studies.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Olivier Gros.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Passos, F.D., de Lima Curi Meserani, G. & Gros, O. Structural and ultrastructural analysis of the gills in the bacterial-bearing species Thyasira falklandica (Bivalvia, Mollusca). Zoomorphology 126, 153–162 (2007). https://doi.org/10.1007/s00435-007-0034-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00435-007-0034-4

Keywords

Navigation