Skip to main content
SpringerLink
Log in

Temporal variation in chemoautotrophic symbiont abundance in the thyasirid bivalve Thyasira cf. gouldi

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Within the bivalve family Thyasiridae, symbioses with chemoautotrophic, sulphur-oxidizing bacteria do not occur in all lineages; variation in symbiont presence and in the degree of abfrontal expansion of gill filaments occurs on fine phylogenetic scales within the family. Thyasirid symbionts are harboured extracellularly and are periodically engulfed and digested by host gill epithelial cells. Symbiotic thyasirids are mixotrophic, retaining the capacity to feed on particulate matter; the relative importance of particulate feeding and symbiont-derived nutrition to host metabolism may vary on temporal and spatial scales depending on the abundance of particulate organic matter and sediment sulphide availability. Here, we demonstrate the existence of a temporal trend in symbiont abundance in Thyasira cf. gouldi from Bonne Bay, Newfoundland, Canada, over 18 months (2011 and 2012): symbiont abundance is highest during the months of autumn and is lowest in spring. The density of membrane whorls, lysosomal microbodies associated with the digestion of bacterial symbionts, does not display a similar temporal trend, indicating that relationships between the contribution of symbiont-derived nutrition and seasonal fluctuations in environmental parameters are less clear. Along with the extracellular status of thyasirid symbioses, their highly dynamic nature may explain the possible evolutionary loss or gain of chemosymbioses among some members of this group.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Allen J (1958) On the basic form and adaptations to habitat in the Lucinacea (Eulamellibranchia). Philos Trans R Soc Lond Biol Sci 241:421–484. doi:10.1098/rstb.1958.0010

    Article  Google Scholar 

  • Baghdasarian G, Muscatine L (2000) Preferential expulsion of dividing algal cells as a mechanism for regulating algal-cnidarian symbiosis. Biol Bull 199:278–286. doi:10.2307/1543184

    Article  CAS  Google Scholar 

  • Batstone RT, Laurich JR, Salvo F, Dufour SC (2014) Divergent chemosymbiosis-related characters in Thyasira cf. gouldi (Bivalvia: Thyasiridae). PLoS One 9(3):e92856. doi:10.1371/journal.pone.0092856

    Article  Google Scholar 

  • Bayer K, Kamke J, Hentschel U (2014) Quantification of bacterial and archaeal symbionts in high and low microbial abundance sponges using real-time PCR. FEMS Microbiol Ecol 89:679–690. doi:10.1111/1574-6941.12369

    Article  CAS  Google Scholar 

  • Bedford Institute of Oceanography (2013) Operational remote sensing. www.bio.gc.ca/science/newtech-technouvelles/sensing-teledetection/index-eng.php (Accessed 7 Jan 2015)

  • Blacknell WM (1973) Aspects of the biology of Thyasira gouldi (Philippi) and its copepod parasite Axinophilus thyasirae (Bresciani and Ockelmann). Ph.D. thesis, University of Stirling, 191 pp

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Caro A, Got P, Bouvy M, Troussellier M, Gros O (2009) Effects of long-term starvation on a host bivalve (Codakia orbicularis, Lucinidae) and its symbiont population. Appl Environ Microbiol 75:3304–3313. doi:10.1128/AEM.02659-08

    Article  CAS  Google Scholar 

  • Chaston J, Goodrich-Blair H (2010) Common trends in mutualism revealed by model associations between invertebrates and bacteria. FEMS Microbiol Rev 34:41–58. doi:10.1111/j.1574-6976.2009.00193.x

    Article  CAS  Google Scholar 

  • Cunning R, Baker AC (2014) Not just who, but how many: the importance of partner abundance in reef coral symbioses. Front Microbiol 5:400. doi:10.3389/fmicb.2014.00400

    Article  Google Scholar 

  • Dando PR, Southward AJ (1986) Chemoautotrophy in bivalve molluscs of the genus Thyasira. J Mar Biol Assoc UK 66:915–929. doi:10.1017/S0025315400048529

    Article  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 Prog Ser 92:151–158. doi:10.3354/meps092151

    Article  CAS  Google Scholar 

  • Dando PR, Southward AJ, Southward EC (2004) Rates of sediment sulphide oxidation by the bivalve mollusc Thyasira sarsi. Mar Ecol Prog Ser 280:181–187. doi:10.3354/meps280181

    Article  CAS  Google Scholar 

  • Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol Rev 76:229–261. doi:10.1128/MMBR.05014-11

    Article  CAS  Google Scholar 

  • Donval A, Le Pennec M, Herry A, Diouris M (1989) Nutritional adaptations of littoral bivalve molluscs to reducing biotopes. In: Ryland JS, Tyler PA (eds) Reproduction, genetics and distributions of marine organisms. Proceedings of the 23rd European marine biology symposium, Swansea, pp 373–378

  • Dubilier N, Bergin C, Lott C (2008) Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol 6:725–740. doi:10.1038/nrmicro1992

    Article  CAS  Google Scholar 

  • Dufour SC (2005) Gill anatomy and the evolution of symbiosis in the bivalve family Thyasiridae. Biol Bull 208:200–212. doi:10.2307/3593152

    Article  Google Scholar 

  • Dufour SC, Felbeck H (2003) Sulphide mining by the superextensile foot of symbiotic thyasirid bivalves. Nature 426:65–67. doi:10.1038/nature02095

    Article  CAS  Google Scholar 

  • Dufour SC, Felbeck H (2006) Symbiont abundance in thyasirids (Bivalvia) is related to particulate food and sulphide availability. Mar Ecol Prog Ser 320:185–194. doi:10.3354/meps320185

    Article  CAS  Google Scholar 

  • Dufour SC, Laurich JR, Batstone RT, McCuaig B, Elliott A, Poduska KM (2014) Magnetosome-containing bacteria living as symbionts of bivalves. ISME J 8:2453–2462. doi:10.1038/ismej.2014.93

    Article  CAS  Google Scholar 

  • Duperron S, Gaudron SM, Rodrigues CF, Cunha MR, Decker C, Olu K (2012) An overview of chemosynthetic symbioses in bivalves from the North Atlantic and Mediterranean Sea. Biogeosci Discuss 9:16815–16875. doi:10.5194/bgd-9-16815-2012

    Article  Google Scholar 

  • Fagoonee I, Wilson HB, Hassell MP, Turner JR (1999) The dynamics of zooxanthellae populations: a long-term study in the field. Science 283:843–845. doi:10.1126/science.283.5403.843

    Article  CAS  Google Scholar 

  • Falkowski PG, Dubinsky Z, Muscatine L, McCloskey LR (1993) Population control in symbiotic corals. Bioscience 43:606–611. doi:10.2307/1312147

    Article  Google Scholar 

  • Fitt WK, McFarland FK, Warner ME, Chilcoat GC (2000) Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol Oceanogr 45:677–685. doi:10.4319/lo.2000.45.3.0677

    Article  CAS  Google Scholar 

  • Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage Publications, Thousand Oaks. http://socserv.socsci.mcmaster.ca/jfox/Books/Companion/

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

    Google Scholar 

  • Gilbert D, Pettigrew G (1993) Current-meter data from Bonne Bay, Newfoundland, during the summer of 1991. Can Data Rep Hydrogr Ocean Sci 122:1–60

    Google Scholar 

  • Gilboa-Garber N (1971) Direct spectrophotometric determination of inorganic sulfide in biological materials and in other complex mixtures. Anal Biochem 43:129–133. doi:10.1016/0003-2697(71)90116-3

    Article  CAS  Google Scholar 

  • Goldhaber MB, Kaplan IR (1975) Controls and consequences of sulfate reduction rates in recent marine sediments. Soil Sci 119:42–55. doi:10.1097/00010694-197501000-00008

    Article  CAS  Google Scholar 

  • Guezi H, Boutet I, Andersen AC, Lallier FH, Tanguy A (2014) Comparative analysis of symbiont ratios and gene expression in natural populations of two Bathymodiolus mussel species. Symbiosis 63:19–29. doi:10.1007/s13199-104-0284-0

    Article  CAS  Google Scholar 

  • Halary S, Riou V, Gaill F, Boudier T, Duperron S (2008) 3D FISH for the quantification of methane- and sulphur-oxidizing endosymbionts in bacteriocytes of the hydrothermal vent mussel Bathymodiolus azoricus. ISME J 2:284–292. doi:10.1038/ismej.2008.3

    Article  CAS  Google Scholar 

  • Kádár E, Bettencourt R, Costa V, Santos RS, Lobo-da-Cunha A, Dando P (2005) Experimentally induced endosymbiont loss and re-acquirement in the hydrothermal vent bivalve Bathymodiolus azoricus. J Exp Mar Biol Ecol 318:99–110. doi:10.1016/j.jembe.2004.12.025

    Article  Google Scholar 

  • Krueger DM, Gustafson RG, Cavanaugh CM (1996) Vertical transmission of chemoautotrophic symbionts in the bivalve Solemya velum (Bivalvia: Protobranchia). Biol Bull 190:195–202

    Article  CAS  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 

  • Le Pennec M, Beninger PG, Herry A (1995a) Feeding and digestive adaptations of bivalve molluscs to sulphide-rich habitats. Comp Biochem Physiol 111A:183–189

    Article  Google Scholar 

  • Le Pennec M, Herry A, Johnson M, Beninger PG (1995b) Nutrition-gametogenesis relationship in the endosymbiont host bivalve Loripes lucinalis (Lucinidae) from reducing coastal habitats. In: Eleftheriou A, Ansell AD, Smith CJ (eds) Biology and ecology of shallow coastal waters. Olsen & Olsen, Fredensborg, pp 139–142

    Google Scholar 

  • 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. doi:10.1007/s002270000526

    Article  CAS  Google Scholar 

  • McIlroy SE, Smith GJ, Geller JB (2014) FISH-Flow: a quantitative molecular approach for describing mixed clade communities of Symbiodinium. Coral Reefs 33:157–167. doi:10.1007/s00338-013-1087-0

    Article  Google Scholar 

  • Nyholm SV, Song P, Dang J, Bruce C, Girguis PR (2012) Expression and putative function of innate immunity genes under in situ conditions in the symbiotic hydrothermal vent tubeworm Ridgeia piscesae. PLoS One 7:e38267. doi:10.1371/journal.pone.0038267

    Article  CAS  Google Scholar 

  • Oliver PG, Kileen IJ (2002) The Thyasiridae (Mollusca: Bivalvia) of the British continental shelf and North Sea oil fields: an identification manual. BIOMOR reports, 3, National Museum of Wales, Cardiff, pp 1–73

  • Rasband WS (1997) ImageJ. U.S. National Institutes of Health, Bethesda. http://imagej.nih.gov/ij/

  • Reid RGB, Brand DG (1986) Sulfide-oxidizing symbiosis in Lucinaceans: implications for bivalve evolution. Veliger 29:3–24

    Google Scholar 

  • R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. www.R-project.org

  • Reynolds LK, Berg P, Zieman JC (2007) Lucinid clam influence on the biogeochemistry of the seagrass Thalassia testudinum sediments. Estuar Coast 30:482–490. doi:10.1007/BF02819394

    Article  CAS  Google Scholar 

  • Riou V, Halary S, Duperron S, Bouillon S, Elskens M, Bettencourt R, Santos RS, Dehairs F, Colaço A (2008) Influence of CH4 and H2S availability on symbiont distribution, carbon assimilation and transfer in the dual symbiotic vent mussel Bathymodiolus azoricus. Biogeosciences 5:1681–1691. doi:10.5194/bg-5-1681-2008

    Article  CAS  Google Scholar 

  • Riou V, Duperron S, Halary S, Dehairs F, Bouillon S, Martins I, Colaço A, Serrão-Santos R (2010) Variation in physiological indicators in Bathymodiolus azoricus (Bivalvia: Mytilidae) at the Menez Gwen Mid-Atlantic Ridge deep-sea hydrothermal vent site within a year. Mar Environ Res 70:264–271. doi:10.1016/j.marenvres.2010.05.008

    Article  CAS  Google Scholar 

  • Rodrigues CF, Duperron S (2011) Distinct symbiont lineages in three thyasirid species (Bivalvia: Thyasiridae) from the eastern Atlantic and Mediterranean Sea. Naturwissenschaften 98:281–287. doi:10.1007/s00114-011-0766-3

    Article  CAS  Google Scholar 

  • Roeselers G, Newton ILG (2012) On the evolutionary ecology of symbioses between chemosynthetic bacteria and bivalves. Appl Microbiol Biotechnol 94:1–10. doi:10.1007/s00253-011-3819-9

    Article  CAS  Google Scholar 

  • Southward EC (1986) Gill symbionts in Thyasirids and other bivalve molluscs. J Mar Biol Assoc UK 66:889–914

    Article  Google Scholar 

  • Stewart FJ, Cavanaugh CM (2006) Bacterial endosymbioses in Solemya (Mollusca: Bivalvia)—model systems for studies of symbiont-host adaptation. Antonie van Leeuwenhoek 90:343–360. doi:10.1007/s10482-006-9086-6

    Article  Google Scholar 

  • Szafranski KM, Piquet B, Shillito B, Lallier FH, Duperron S (2015) Relative abundances of methane- and sulfur-oxidizing symbionts in gills of the deep-sea hydrothermal vent mussel Bathymodiolus azoricus under pressure. Deep Sea Res I 101:7–13. doi:10.1016/j.dsr.2015.03.003

    Article  CAS  Google Scholar 

  • Taylor JD, Glover EA (2006) Lucinidae (Bivalvia) - the most diverse group of chemosymbiotic molluscs. Zool J Linn Soc Lond 148:421–438. doi:10.1111/j.1096-3642.2006.00261.x

    Article  Google Scholar 

  • Thornhill DJ, Rotjan RD, Todd BD, Chilcoat GC, Iglesias-Prieto R, Kemp DW et al (2011) A connection between the colony biomass and death in Caribbean reef-building corals. PLoS One 6:e29535. doi:10.1371/journal.pone.0029535

    Article  CAS  Google Scholar 

  • Tian RC, Vézina AF, Starr M, Saucier F (2001) Seasonal dynamics of coastal ecosystems and export production at high latitudes: a modeling study. Limnol Oceanogr 46:1845–1859. doi:10.4319/lo.2001.46.8.1845

    Article  CAS  Google Scholar 

  • van der Geest M, Sall AA, Ely SO, Nauta RW, van Gils JA, Piersma T (2014) Nutritional and reproductive strategies in a chemosymbiotic bivalve living in a tropical intertidal seagrass bed. Mar Ecol Prog Ser 501:113–126. doi:10.3354/meps10702

    Article  Google Scholar 

  • Westrich JT, Berner RA (1984) The role of sedimentary organic matter in bacterial sulfate reduction: the G model tested. Limnol Oceanogr 29:236–249. doi:10.4319/lo.1984.29.2.0236

    Article  CAS  Google Scholar 

  • Wlodarska-Kowalczuk M (2007) Molluscs in Kongsfjorden (Spitsbergen, Svalbard): a species list and patterns of distribution and diversity. Polar Res 26:48–63. doi:10.1111/j.1751-8369.2007.00003.x

    Article  Google Scholar 

  • Wood SN (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J R Stat Soc Ser B 73:3–36. doi:10.1111/j.1467-9868.2010.00749.x

    Article  Google Scholar 

Download references

Acknowledgments

We thank R. Hooper and the staff of the Bonne Bay Marine Station for help with sampling, and C. Caverhill, Bedford Institution of Oceanography, who provided data on phytoplankton blooms. K. Williams and S. Tucker at Memorial University’s EM flow unit assisted with transmission electron microscopy. Financial support was obtained through an NSERC Discovery Grant (S.C.D.), an NSERC post-graduate scholarship (J.R.L.), an RDC Ignite R&D grant (S.C.D.) and an RDC Ocean Industries Student Research Award (R.T.B.).

Author information

Authors and Affiliations

  1. Department of Biology, Memorial University of Newfoundland, St. John’s, NL, A1B 3X9, Canada

    Jason R. Laurich, Rebecca T. Batstone & Suzanne C. Dufour

Authors
  1. Jason R. Laurich
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rebecca T. Batstone
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Suzanne C. Dufour
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Suzanne C. Dufour.

Additional information

Responsible Editor: M. Kühl.

Reviewed by undisclosed experts.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 13 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Laurich, J.R., Batstone, R.T. & Dufour, S.C. Temporal variation in chemoautotrophic symbiont abundance in the thyasirid bivalve Thyasira cf. gouldi . Mar Biol 162, 2017–2028 (2015). https://doi.org/10.1007/s00227-015-2727-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-015-2727-4

Keywords

Search

Navigation