Abstract
For the first time, two Dynamic Energy Budget (DEB) models were developed for a chemosymbiotic deep-sea vesicomyid clam. A classical DEB model was applied and then an innovative DEB model was developed (named “farming”). The models were parameterized using data on host and symbionts, including original unpublished data. In the farming model the digestion of the sulfur-oxidizing bacterial symbionts for host nutrition was explicitly modeled. Unexpected results were obtained regarding the dynamics of host and symbionts with this model: the host appears to forgo a maximal ingestion for a lower and stable ingestion, revealing a new kind of homeostasis. Moreover, when the clam is adult, most of the oxygen consumed by the chemosynthetic symbiosis was predicted to be by the symbionts. A high host energy maintenance flux was predicted and consistent with the likely high energy demand of host ion homeostasis mechanisms to cope with symbiont protons and sulfates release.
Similar content being viewed by others
Data availability
The datasets generated and/or analysed during the current study are available in the Christineconcha_regab_dynamic_energy_budget repository, https://github.com/mvdb26/Christineconcha_regab_dynamic_energy_budget.
References
Dubilier, N., Bergin, C. & Lott, C. Symbiotic diversity in marine animals: The art of harnessing chemosynthesis. Nat. Rev. Microbiol. 6, 725–740. https://doi.org/10.1038/nrmicro1992 (2008).
Krylova, E. M. & Sahling, H. Vesicomyidae (Bivalvia): Current taxonomy and distribution. PLoS One 5, e9957. https://doi.org/10.1371/journal.pone.0009957 (2010).
Johnson, S. B., Krylova, E. M., Audzijonyte, A., Sahling, H. & Vrijenhoek, R. C. Phylogeny and origins of chemosynthetic vesicomyid clams. Syst. Biodivers. 15, 346–360. https://doi.org/10.1080/14772000.2016.1252438 (2017).
Decker, C., Olu, K., Arnaud-Haond, S. & Duperron, S. Physical proximity may promote lateral acquisition of bacterial symbionts in vesicomyid clams. PLoS One 8, e64830. https://doi.org/10.1371/journal.pone.0064830 (2013).
Newton, I. L. G., Girguis, P. R. & Cavanaugh, C. M. Comparative genomics of vesicomyid clam (Bivalvia: Mollusca) chemosynthetic symbionts. BMC Genomics 9, 585. https://doi.org/10.1186/1471-2164-9-585 (2008).
Stewart, F. J. & Cavanaugh, C. M. Pyrosequencing analysis of endosymbiont population structure: Co-occurrence of divergent symbiont lineages in a single vesicomyid host clam. Environ. Microbiol. 11, 2136–2147. https://doi.org/10.1111/j.1462-2920.2009.01933.x (2009).
Cruaud, P. et al. Ecophysiological differences between vesicomyid species and metabolic capabilities of their symbionts influence distribution patterns of the deep-sea clams. Mar. Ecol. 40, e12541. https://doi.org/10.1111/maec.12541 (2019).
Ip, J.-H. et al. Host-endosymbiont genome integration in a deep-sea chemosymbiotic clam. Mol. Biol. Evol. 38, 502–518. https://doi.org/10.1093/molbev/msaa241 (2021).
Perez, M. et al. Divergent paths in the evolutionary history of maternally transmitted clam symbionts. Proc. R. Soc. B Biol. Sci. 289, 20212137. https://doi.org/10.1098/rspb.2021.2137 (2022).
Szafranski, K. M., Gaudron, S. M. & Duperron, S. Direct evidence for maternal inheritance of bacterial symbionts in small deep-sea clams (Bivalvia: Vesicomyidae). Naturwissenschaften 101, 373–383. https://doi.org/10.1007/s00114-014-1165-3 (2014).
Ikuta, T. et al. Surfing the vegetal pole in a small population: Extracellular vertical transmission of an ‘intracellular’ deep-sea clam symbiont. R. Soc. Open Sci. 3, 160130. https://doi.org/10.1098/rsos.160130 (2016).
Cary, S. C. & Giovannoni, S. J. Transovarial inheritance of endosymbiotic bacteria in clams inhabiting deep-sea hydrothermal vents and cold seeps. Proc. Natl. Acad. Sci. U. S. A. 90, 5695–5699. https://doi.org/10.1073/pnas.90.12.5695 (1993).
Stewart, F. J., Young, C. R. & Cavanaugh, C. M. Lateral symbiont acquisition in a maternally transmitted chemosynthetic clam endosymbiosis. Mol. Biol. Evol. 25, 673–687. https://doi.org/10.1093/molbev/msn010 (2008).
Ozawa, G. et al. Ancient occasional host switching of maternally transmitted bacterial symbionts of chemosynthetic vesicomyid clams. Genome Biology and Evolution 9, 2226–2236. https://doi.org/10.1093/gbe/evx166 (2017).
Peek, A. S., Feldman, R. A., Lutz, R. A. & Vrijenhoek, R. C. Cospeciation of chemoautotrophic bacteria and deep sea clams. Proc. Natl. Acad. Sci. U. S. A. 95, 9962–9966. https://doi.org/10.1073/pnas.95.17.9962 (1998).
von Cosel, R. & Olu, K. Large Vesicomyidae (Mollusca: Bivalvia) from cold seeps in the Gulf of Guinea off the coasts of Gabon, Congo and northern Angola. Deep Sea Res. Part II Top. Stud. Oceanogr. 56, 2350–2379. https://doi.org/10.1016/j.dsr2.2009.04.016 (2009).
Ondréas, H. et al. Rov study of a giant pockmark on the Gabon continental margin. Geo Mar. Lett. 25, 281–292. https://doi.org/10.1007/s00367-005-0213-6 (2005).
Bridges, A. et al. Review of the central and south atlantic shelf and deep-sea benthos: science, policy, and management. In Oceanography and Marine Biology, 127–218, (CRC Press, 2023), 1 edn https://doi.org/10.1201/9781003363873-5.
Olu, K. et al. Influence of seep emission on the non-symbiont-bearing fauna and vagrant species at an active giant pockmark in the Gulf of Guinea (Congo-Angola margin). Deep Sea Res. Part II Top. Stud. Oceanogr. 56, 2380–2393. https://doi.org/10.1016/j.dsr2.2009.04.017 (2009).
Khripounoff, A. et al. Respiration of bivalves from three different deep-sea areas: Cold seeps, hydrothermal vents and organic carbon-rich sediments. Deep Sea Res. Part II Top. Stud. Oceanogr. 142, 233–243. https://doi.org/10.1016/j.dsr2.2016.05.023 (2017).
Rabouille, C. et al. Carbon and silica megasink in deep-sea sediments of the Congo terminal lobes. Quat. Sci. Rev. 222, 105854. https://doi.org/10.1016/j.quascirev.2019.07.036 (2019).
Olive, G., Rodrigues, C. F. & Cunha, M. R. Chemosymbiotic bivalves from the mud volcanoes of the Gulf of Cadiz, NE Atlantic, with descriptions of new species of Solemyidae, Lucinidae and Vesicomyidae. ZooKeys 1–38 (2011), https://doi.org/10.3897/zookeys.113.1402.
Rodrigues, C. F., Hilário, A. & Cunha, M. R. Chemosymbiotic species from the Gulf of Cadiz (NE Atlantic): Distribution, life styles and nutritional patterns. Biogeosciences 10, 2569–2581. https://doi.org/10.5194/bg-10-2569-2013 (2013).
Krylova, E. M., Sahling, H. & Janssen, R. Abyssogena: A new genus of the family Vesicomyidae (Bivalvia) from deep-water vents and seeps. J. Molluscan Stud. 76, 107–132. https://doi.org/10.1093/mollus/eyp052 (2010).
Decker, C. Diversité, écologie et adaptation des bivalves Vesicomyidae associés aux environnements réducteurs profonds des marges continentales. Ph.D. thesis, Brest (2011).
Boetius, A. et al. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407, 623–626. https://doi.org/10.1038/35036572 (2000).
Pruski, A. M. et al. Energy transfer in the Congo deep-sea fan: From terrestrially-derived organic matter to chemosynthetic food webs. Deep Sea Res. Part II Top. Stud. Oceanogr. 142, 197–218. https://doi.org/10.1016/j.dsr2.2017.05.011 (2017).
Childress, J. J. & Girguis, P. R. The metabolic demands of endosymbiotic chemoautotrophic metabolism on host physiological capacities. J. Exp. Biol. 214, 312–325. https://doi.org/10.1242/jeb.049023 (2011).
Sogin, E. M., Leisch, N. & Dubilier, N. Chemosynthetic symbioses. Curr. Biol. 30, R1137–R1142. https://doi.org/10.1016/j.cub.2020.07.050 (2020).
Lan, Y. et al. Host-symbiont interactions in deep-sea chemosymbiotic vesicomyid clams: Insights from transcriptome sequencing. Front. Mar. Sci. 6, 680. https://doi.org/10.3389/fmars.2019.00680 (2019).
Fiala-Medioni, A. & Le Pennec, M. Trophic structural adaptations in relation to the bacterial association of bivalve molluscs from hydrothermal vents and subduction zones. Symbiosis 63–74 (1987).
Newton, I. L. G. et al. The Calyptogena magnifica chemoautotrophic symbiont genome. Science 315, 998–1000. https://doi.org/10.1126/science.1138438 (2007).
Sogin, E. M., Kleiner, M., Borowski, C., Gruber-Vodicka, H. R. & Dubilier, N. Life in the dark: Phylogenetic and physiological diversity of chemosynthetic symbioses. Annu. Rev. Microbiol. 75, 695–718. https://doi.org/10.1146/annurev-micro-051021-123130 (2021).
Husson, B. et al. Modelling the interactions of the hydrothermal mussel Bathymodiolus azoricus with vent fluid. Ecol. Modell. 377, 35–50. https://doi.org/10.1016/j.ecolmodel.2018.03.007 (2018).
Martins, I. et al. Size-dependent variations on the nutritional pathway of Bathymodiolus azoricus demonstrated by a C-flux model. Ecol. Modell. 217, 59–71. https://doi.org/10.1016/j.ecolmodel.2008.05.008 (2008).
Kooijman, S. A. L. M. Dynamic energy budget theory for metabolic organisation (Cambridge University Press, 2010).
Gaudron, S. M., Lefebvre, S. & Marques, G. M. Inferring functional traits in a deep-sea wood-boring bivalve using dynamic energy budget theory. Sci. Rep. 11, 22720. https://doi.org/10.1038/s41598-021-02243-w (2021).
Martins, I. et al. Developing a dynamic energy budget model to project potential effects of deep-sea mining plumes on the Atlantic deep-sea mussel. Bathymodiolus azoricus. Ecol. Inform. 83, 102803. https://doi.org/10.1016/j.ecoinf.2024.102803 (2024).
Muller, E. B., Kooijman, S. A. L. M., Edmunds, P. J., Doyle, F. J. & Nisbet, R. M. Dynamic energy budgets in syntrophic symbiotic relationships between heterotrophic hosts and photoautotrophic symbionts. J. Theor. Biol. 259, 44–57. https://doi.org/10.1016/j.jtbi.2009.03.004 (2009).
Kaare-Rasmussen, J. O., Moeller, H. V. & Pfab, F. Modeling food dependent symbiosis in Exaiptasia pallida. Ecol. Modell. 481, 110325. https://doi.org/10.1016/j.ecolmodel.2023.110325 (2023).
Bénard, A., Vavre, F. & Kremer, N. Stress & symbiosis: Heads or tails?. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2020.00167 (2020).
Halary, S., Riou, V., Gaill, F., Boudier, T. & Duperron, S. 3D FISH for the quantification of methane- and sulphur-oxidising endosymbionts in bacteriocytes of the hydrothermal vent mussel Bathymodiolus azoricus. ISME J. 2(3), 284 (2008).
Pfab, F. et al. Timescale separation and models of symbiosis: State space reduction, multiple attractors and initialization. Conserv. Physiol. 10, coac026. https://doi.org/10.1093/conphys/coac026 (2022).
Distel, D. L. et al. Discovery of chemoautotrophic symbiosis in the giant shipworm Kuphus polythalamia (Bivalvia: Teredinidae) extends wooden-steps theory. Proc. Natl. Acad. Sci. U. S. A. 114, E3652–E3658. https://doi.org/10.1073/pnas.1620470114 (2017).
Petersen, J. M. & Yuen, B. The symbiotic “all-rounders’’: Partnerships between Marine Animals and chemosynthetic nitrogen-fixing bacteria. Appl. Environ. Microbiol. 87, e02129-20. https://doi.org/10.1128/aem.02129-20 (2021).
Martins, G. The metabolic theory of ecology as a mechanistic approach. In New Mechanism: Explanation, Emergence and Reduction (eds Cordovil, J. L. et al.) 29–60 (Springer International Publishing, 2024). https://doi.org/10.1007/978-3-031-46917-6_3.
Cunning, R., Muller, E. B., Gates, R. D. & Nisbet, R. M. A dynamic bioenergetic model for coral-Symbiodinium symbioses and coral bleaching as an alternate stable state. J. Theor. Biol. 431, 49–62. https://doi.org/10.1016/j.jtbi.2017.08.003 (2017).
Kooijman, S. A. L. M., Auger, P., Poggiale, J. C. & Kooi, B. W. Quantitative steps in symbiogenesis and the evolution of homeostasis. Biol. Rev. 78, 435–463. https://doi.org/10.1017/S1464793102006127 (2003).
Goffredi, S. K. & Barry, J. P. Species-specific variation in sulfide physiology between closely related Vesicomyid clams. Mar. Ecol. Prog. Ser. 225, 227–238. https://doi.org/10.3354/meps225227 (2002).
Sublette, K. L. Aerobic oxidation of hydrogen sulfide by Thiobacillus denitrificans. Biotechnology and Bioengineering 29, 690–695. https://doi.org/10.1002/bit.260290605 (1987).
Goffredi, S. K. & Barry, J. P. Energy acquisition and allocation in vesicomyid symbioses. Cahiers de Biol. Mar. 43, 345–350. https://doi.org/10.21411/CBM.A.5ADE9CC5 (2002).
Barry, J. P., Whaling, P. J. & Kochevar, R. K. Growth, production, and mortality of the chemosynthetic vesicomyid bivalve, Calyptogena kilmeri from cold seeps off central California. Mar. Ecol. 28, 169–182. https://doi.org/10.1111/j.1439-0485.2007.00119.x (2007).
Turekian, K. K. & Cochran, J. K. Growth Rate of a Vesicomyid Clam from the Galápagos Spreading Center. Science 214, 909–911. https://doi.org/10.1126/science.214.4523.909 (1981).
Turekian, K. K., Cochran, J. K. & Bennett, J. T. Growth rate of a vesicomyid clam from the 21\(^\circ\) N East Pacific Rise hydrothermal area. Nature 303, 55–56. https://doi.org/10.1038/303055a0 (1983).
Olu, K. et al. Cold-seep-like macrofaunal communities in organic- and sulfide-rich sediments of the Congo deep-sea fan. Deep. Sea Res. Part II: Top. Stud. Oceanogr. 142, 180–196. https://doi.org/10.1016/j.dsr2.2017.05.005 (2017).
Rabouille, C. et al. The Congolobe project, a multidisciplinary study of Congo deep-sea fan lobe complex: Overview of methods, strategies, observations and sampling. Deep. Sea Res. Part II: Top. Stud. Oceanogr. 142, 7–24. https://doi.org/10.1016/j.dsr2.2016.05.006 (2017).
Pop Ristova, P. et al. Bacterial diversity and biogeochemistry of different chemosynthetic habitats of the REGAB cold seep (West African margin, 3160 m water depth). Biogeosciences 9, 8337–8385. https://doi.org/10.5194/bgd-9-8337-2012. (2012).
Add-My-Pet Species List. https://www.bio.vu.nl/thb/deb/deblab/add_my_pet/species_list.html (2024)
Marques, G. M. et al. The AmP project: Comparing species on the basis of dynamic energy budget parameters. PLoS Comput. Biol. 14, e1006100. https://doi.org/10.1371/journal.pcbi.1006100 (2018).
Rabouille, C., Baudin, F., Dennielou, B. & Olu, K. Organic carbon transfer and ecosystem functioning in the terminal lobes of the Congo deep-sea fan: Outcomes of the Congolobe project. Deep Sea Res. Part II Top. Stud. Oceanogr. 142, 1–6. https://doi.org/10.1016/j.dsr2.2017.07.006 (2017).
Sen, A. et al. Fauna and habitat types driven by turbidity currents in the lobe complex of the Congo deep-sea fan. Deep Sea Res. Part II Top. Stud. Oceanogr. 142, 167–179. https://doi.org/10.1016/j.dsr2.2017.05.009 (2017).
Lika, K. et al. The “covariation method’’ for estimating the parameters of the standard Dynamic Energy Budget model I: Philosophy and approach. J. Sea Res. 66, 270–277. https://doi.org/10.1016/j.seares.2011.07.010 (2011).
Marques, G. M., Lika, K., Augustine, S., Pecquerie, L. & Kooijman, S. A. L. M. Fitting multiple models to multiple data sets. J. Sea Res. 143, 48–56. https://doi.org/10.1016/j.seares.2018.07.004 (2019).
Funding
Marine Vandenberghe was funded by a PhD fellowship provided by the CNRS through the 80-Prime Program. This work was financially supported by both the French National Program EC2CO and the 80-Prime Program.
Author information
Authors and Affiliations
Contributions
S.M.G. conceived the project. M.V. and G.M. designed the new farming model. M.V. wrote the manuscript with inputs of S.M.G and G.M.. A.C.A., C.D., K.O. and S.D. performed some experimentations and provided data. All authors reviewed the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.
About this article
Cite this article
Vandenberghe, M., Marques, G.M., Andersen, A.C. et al. A novel bioenergetic model outlines the metabolism of a deep-sea clam and that of its sulfur-oxidizing symbionts. Sci Rep (2026). https://doi.org/10.1038/s41598-026-41176-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1038/s41598-026-41176-0


