Abstract
The Bathymodiolinae are pervasive in reducing environments in the deep sea, yet data on post-larval and juvenile development and on the process of symbiont acquisition remain elusive. To understand how these opportunistic metazoans survive in ephemeral reducing habitats, individuals of the small bathymodiolin, Idas modiolaeformis, were examined histologically to trace their reproductive development, and with fluorescence and transmission electron microscopy to identify patterns of infection by their environmentally acquired bacterial symbionts. A size series of these mussels was retrieved from larval colonisation devices containing vegetative substrates, deployed for 51 weeks (November 2006–2007) in the central ‘Pockmarks’ region (site 2A) of the Nile deep-sea fan in the eastern Mediterranean (NDSF), a zone where methane seepage can occur (N 32° 31.97, E 30° 21.18, 1,693 m deep). Developmental patterns of germ cell migration, size at first maturity, and symbiont acquisition and localisation are presented for the post-larva to adult transition. The smallest mature adult was a male with shell length (SL) 2.35 mm. All larger individuals in the series were male (maximum SL 6.54 mm). Based on the absence of bacterial signals, plantigrades were asymbiotic, indicating strict heterotrophy in larvae and early post-larvae. During the early stages of dissoconch deposition, extracellular symbiont infection was non-specific. This was followed by increasing specificity on non-ciliated gill epithelia in adults. These observations on early development in I. modiolaeformis represent evolutionary adaptations to their ephemeral, reducing habitats.
Similar content being viewed by others
References
Arellano SM, Young CM (2009) Spawning, development, and the duration of larval life in a deep-sea cold-seep mussel. Biol Bull 216(2):149–162
Bayne B (1971) Some morphological changes that occur at the metamorphosis of the larvae of Mytilus edulis. In: Crisp D (ed) 4th EMBS. Cambridge University Press, Cambridge
Berg CJ (1985) Reproductive strategies of mollusks from abyssal hydrothermal vent communities. Bull Biol Soc Wash 6:185–197
Bienhold C, Pop Ristova P, Wenzhöfer F, Dittmar T, Boetius A (2013) How deep-sea wood falls sustain chemosynthetic life. PLoS ONE 8(1):e53590. doi:10.1371/journal.pone.0053590
Cannuel R, Beninger PG, McCombie H, Boudry P (2009) Gill development and its functional and evolutionary implications in the blue mussel Mytilus edulis (Bivalvia: Mytilidae). Biol Bull 217(2):173–188
Cavanaugh CM, Levering PR, Maki JS, Mitchell R, Lidstrom ME (1987) Symbiosis of methylotrophic bacteria and deep-sea mussels. Nature 325(6102):346–348. doi:10.1038/325346a0
Cavanaugh CM, McKiness ZP, Newton IL, Stewart FJ (2006) Marine chemosynthetic symbioses. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The Prokaryotes (3rd ed). A handbook on the biology of bacteria: symbiotic associations, biotechnology, applied microbiology. Springer, Berlin, pp 475–507
Coan EV, Valentich-Scott P (2012) Bivalve seashells of tropical West America. Marine bivalve mollusks from Baja California to northern Perú. Santa Barbara Museum of Natural History, Santa Barbara
Colaço A, Martins I, Laranjo M, Pires L, Leal C, Prieto C, Costa V, Lopes H, Rosa D, Dando PR, Serrão-Santos R (2006) Annual spawning of the hydrothermal vent mussel, Bathymodiolus azoricus, under controlled aquarium conditions at atmospheric pressure. J Exp Mar Biol Ecol 333(2):166–171. doi:10.1016/j.jembe.2005.12.005
Cunha MR, Matos FL, Génio L, Hilário A, Moura CJ, Ravara A, Rodrigues CF (2013) Are organic falls bridging reduced environments in the deep sea? Results from colonization experiments in the Gulf of Cádiz. PLoS ONE 8(10):e76688. doi:10.1371/journal.pone.0076688
Dixon D, Lowe D, Miller P, Villemin G, Colaço A, Serrao-Santos R, Dixon L (2006) Evidence of seasonal reproduction in the Atlantic vent mussel Bathymodiolus azoricus, and an apparent link with the timing of photosynthetic primary production. J Mar Biol Assoc UK 86(6):1363–1371. doi:10.1017/S0025315406014391
Dubilier N, Bergin C, Lott C (2008) Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nature Rev Microbiol 6(10):725–740
Dufour SC (2005) Gill anatomy and the evolution of symbiosis in the bivalve family Thyasiridae. Biol Bull 208(3):200–212. doi:10.2307/3593152
Duperron S (2010) The diversity of deep-sea mussels and their bacterial symbioses. In: Kiel S (ed) Vent and seep biota: aspects from microbes to ecosystems. Palgrave, Basingstoke, pp 137–167
Duperron S, Halary S, Lorion J, Sibuet M, Gaill F (2008a) Unexpected co-occurrence of six bacterial symbionts in the gills of the cold seep mussel Idas sp (Bivalvia: Mytilidae). Environ Microbiol 10(2):433–445. doi:10.1111/j.1462-2920.2007.01465.x
Duperron S, Laurent MCZ, Gaill F, Gros O (2008b) Sulphur-oxidizing extracellular bacteria in the gills of Mytilidae associated with wood falls. FEMS Microbiol Ecol 63(3):338–349. doi:10.1111/j.1574-6941.2008.00438.x
Duperron S, Gaudron SM, Rodrigues CF, Cunha MR, Decker C, Olu K (2013) An overview of chemosynthetic symbioses in bivalves from the North Atlantic and Mediterranean Sea. Biogeosciences 10(5):3241–3267. doi:10.5194/bg-10-3241-2013
Fabioux C, Huvet A, Lelong C, Robert R, Pouvreau S, Daniel J-Y, Minguant C, Le Pennec M (2004) Oyster vasa-like gene as a marker of the germline cell development in Crassostrea gigas. Biochem Biophys Res Commun 320(2):592–598. doi:10.1016/j.bbrc.2004.06.009
Gaudron SM, Pradillon F, Pailleret M, Duperron S, Le Bris N, Gaill F (2010) Colonization of organic substrates deployed in deep-sea reducing habitats by symbiotic species and associated fauna. Mar Environ Res 70(1):1–12. doi:10.1016/j.marenvres.2010.02.002
Gaudron SM, Demoyencourt E, Duperron S (2012) Reproductive traits of the cold-seep symbiotic mussel Idas modiolaeformis: gametogenesis and larval biology. Biol Bull 222(1):6–16
Ghiselin MT (1969) The evolution of hermaphroditism among animals. Q Rev Biol 44(2):189–208
Gosselin LA, Qian P-Y (1997) Juvenile mortality in benthic marine invertebrates. Mar Ecol Prog Ser 146(1):265–282. doi:10.3354/meps146265
Gros O, Guibert J, Gaill F (2007) Gill-symbiosis in mytilidae associated with wood fall environments. Zoomorphology 126(3):163–172. doi:10.1007/s00435-007-0035-3
Guisti F, Mietto P, Sbrana C (2012) Il genere Idas (Mytilidae, Bathymodiolinae) in Mediterraneo con la descrizione di quattro nuove specie. Boll Malacol 48(2):122–135
Gustafson R, Reid R (1986) Development of the pericalymma larva of Solemya reidi (Bivalvia: Cryptodonta: Solemyidae) as revealed by light and electron microscopy. Mar Biol 93(3):411–427. doi:10.1007/BF00401109
Juniper SK, Tunnicliffe V, Southward EC (1992) Hydrothermal vents in turbidite sediments on a Northeast Pacific spreading centre: organisms and substratum at an ocean drilling site. Can J Zool 70(9):1792–1809. doi:10.1139/z92-247
Kádár E, Lobo-da-Cunha A, Santos RS, Dando P (2006) Spermatogenesis of Bathymodiolus azoricus in captivity matching reproductive behaviour at deep-sea hydrothermal vents. J Exp Mar Biol Ecol 335(1):19–26. doi:10.1016/j.jembe.2006.02.016
Khelaifia S, Fardeau M-L, Pradel N, Aussignargues C, Garel M, Tamburini C, Cayol J-L, Gaudron S, Gaill F, Ollivier B (2011) Desulfovibrio piezophilus sp. nov., a piezophilic, sulfate-reducing bacterium isolated from wood falls in the Mediterranean Sea. Int J Syst Evol Microbiol 61(11):2706–2711. doi:10.1099/ijs.0.028670-0
Kiel S, Goedert JL (2006) Deep-sea food bonanzas: early Cenozoic whale-fall communities resemble wood-fall rather than seep communities. Proc R Soc Lond 273(1601):2625–2632. doi:10.1098/rspb.2006.3620
Laurent MCZ, Le Bris N, Gaill F, Gros O (2013) Dynamics of wood fall colonization in relation to sulfide concentration in a mangrove swamp. Mar Environ Res 87–88:85–95. doi:10.1016/j.marenvres.2013.03.007
Le Pennec M, Beninger PG (2000) Reproductive characteristics and strategies of reducing-system bivalves. Comp Biochem Physiol 126(1):1–16. doi:10.1016/S0742-8413(00)00100-6
Le Pennec G, Le Pennec M, Beninger PG, Dufour S (2002) Spermatogenesis in the archaic hydrothermal vent bivalve, Bathypecten vulcani, and comparison of spermatozoon ultrastructure with littoral pectinids. Invertebr Reprod Dev 41(1–3):13–19. doi:10.1080/07924259.2002.9652730
Lonsdale P (1977) Clustering of suspension-feeding macrobenthos near abyssal hydrothermal vents at oceanic spreading centers. Deep Sea Res 24(9):857–863. doi:10.1016/0146-6291(77)90478-7
Lorion J, Duperron S, Gros O, Cruaud C, Samadi S (2009) Several deep-sea mussels and their associated symbionts are able to live both on wood and on whale falls. Proc R Soc Lond 276(1654):177–185. doi:10.1098/rspb.2008.1101
Lorion J, Buge B, Cruaud C, Samadi S (2010) New insights into diversity and evolution of deep-sea Mytilidae (Mollusca: Bivalvia). Mol Phylogenet Evol 57(1):71–83. doi:10.1016/j.ympev.2010.05.027
Lorion J, Halary S, do Nasciment J, Samadi S, Couloux A, Duperron S (2012) Evolutionary history of Idas sp. Med. (Bivalvia: Mytilidae), a cold seep mussel bearing multiple symbionts. Cah Biol Mar 53(1):77–87
Lorion J, Kiel S, Faure B, Kawato M, Ho SY, Marshall B, Tsuchida S, Miyazaki J-I, Fujiwara Y (2013) Adaptive radiation of chemosymbiotic deep-sea mussels. Proc R Soc Lond 280(1770):20131243. doi:10.1098/rspb.2013.1243
Lubet P (1959) Recherches sur le cycle sexuel et remission des gametes chez les Mytilides et les Pectinides (Moll. Bivalves). Rev Trav Inst Peches marit 23(3):387–548
Lutz R, Jablonski D, Rhoads D, Turner R (1980) Larval dispersal of a deep-sea hydrothermal vent bivalve from the Galapagos Rift. Mar Biol 57(2):127–133
Murray J, Renard AF, Gibson J (1891) Report on deep-sea deposits based on the specimens collected during the voyage of HMS challenger in the years 1872 to 1876. Printed for HM Stationery off., by Neill and company
Nakaoka M (1994) Size-dependent reproductive traits of Yoldia notabilis (Bivalvia: Protobranchia). Mar Ecol Prog Ser 114:129
Nedoncelle K, Lartaud F, de Rafelis M, Boulila S, Le Bris N (2013) A new method for high-resolution bivalve growth rate studies in hydrothermal environments. Mar Biol 160:1427–1439. doi:10.1007/s00227-013-2195-7
Obata M, Sano N, Kimata S, Nagasawa K, Yoshizaki G, Komaru A (2010) The proliferation and migration of immature germ cells in the mussel, Mytilus galloprovincialis: observation of the expression pattern in the M. galloprovincialis vasa-like gene (Myvlg) by in situ hybridization. Dev Genes Evol 220(5–6):139–149. doi:10.1007/s00427-010-0335-3
Ockelmann KW, Dinesen GE (2011) Life on wood–the carnivorous deep-sea mussel Idas argenteus (Bathymodiolinae, Mytilidae, Bivalvia). Mar Biol Res 7(1):71–84. doi:10.1080/17451001003714504
Olu-Le Roy K, Sibuet M, Fiala-Médioni A, Gofas S, Salas C, Mariotti A, Foucher J-P, Woodside J (2004) Cold seep communities in the deep eastern Mediterranean Sea: composition, symbiosis and spatial distribution on mud volcanoes. Deep Sea Res 51(12):1915–1936. doi:10.1016/j.dsr.2004.07.004
Paull CK, Hecker B, Commeau R, Freeman-Lynde RP, Neumann C, Corso WP, Golubic S, Hook JE, Sikes E, Curray J (1984) Biological communities at the Florida escarpment resemble hydrothermal vent taxa. Science 226(4677):965–967. doi:10.1126/science.226.4677.965
Ritt B, Duperron S, Lorion J, Sara Lazar C, Sarrazin J (2012) Integrative study of a new cold-seep mussel (Mollusca: Bivalvia) associated with chemosynthetic symbionts in the Marmara Sea. Deep Sea Res 67:121–132. doi:10.1016/j.dsr.2012.05.009
Rodrigues CF, Cunha MR, Génio L, Duperron S (2013) A complex picture of associations between two host mussels and symbiotic bacteria in the Northeast Atlantic. Naturwissenschaften 100(1):21–31. doi:10.1007/s00114-012-0985-2
Salerno JL, Macko SA, Hallam SJ, Bright M, Won YJ, McKiness Z, Van Dover CL (2005) Characterization of symbiont populations in life-history stages of mussels from chemosynthetic environments. Biol Bull 208(2):145–155. doi:10.2307/3593123
Samadi S, Quéméré E, Lorion J, Tillier A, von Cosel R, Lopez P, Cruaud C, Couloux A, Boisselier-Dubayle M-C (2007) Molecular phylogeny in mytilids supports the wooden steps to deep-sea vents hypothesis. C R Biol 330(5):446–456. doi:10.1016/j.crvi.2007.04.001
Seed R (1969) The ecology of Mytilus edulis L. (Lamellibranchiata) on exposed rocky shores. Oecologia 3(3–4):277–316. doi:10.1007/BF00390380
Seed R, Suchanek T (1992) The mussel Mytilus: ecology, physiology, genetics and culture. In: Gosling E (ed) Population and community ecology of Mytilus. Elsevier, Amsterdam, pp 87–170
Smith C, Kukert H, Wheatcroft R, Jumars P, Deming J (1989) Vent fauna on whale remains. Nature 341:27–28. doi:10.1038/341027a0
Southward EC (2008) The morphology of bacterial symbioses in the gills of mussels of the genera Adipicola and Idas (Bivalvia: Mytilidae). J Shellfish Res 27(1):139–146. doi:10.2983/0730-8000(2008)27[139:TMOBSI]2.0.CO;2
Stewart FJ, Newton ILG, Cavanaugh CM (2005) Chemosynthetic endosymbioses: adaptations to oxic–anoxic interfaces. Trends Microbiol 13(9):439–448. doi:10.1016/j.tim.2005.07.007
Streams M, Fisher C, Fiala-Medioni A (1997) Methanotrophic symbiont location and fate of carbon incorporated from methane in a hydrocarbon seep mussel. Mar Biol 129(3):465–476. doi:10.1007/s002270050187
Suchanek TH (1981) The role of disturbance in the evolution of life history strategies in the intertidal mussels Mytilus edulis and M. californianus. Oecologia 50(2):143–152. doi:10.1007/BF00348028
Taylor JD, Glover EA (2010) Chemosymbiotic bivalves. In: Kiel S (ed) Vent and seep biota: aspects from microbes to ecosystems. Springer, Basingstoke, pp 107–135
Thubaut J, Corbari L, Gros O, Duperron S, Couloux A, Samadi S (2013a) Integrative biology of Idas iwaotakii (Habe, 1958), a ‘model species’ associated with sunken organic substrates. PLoS ONE 8(7):e69680. doi:10.1371/journal.pone.0069680
Thubaut J, Puillandre N, Faure B, Cruaud C, Samadi S (2013b) The contrasted evolutionary fates of deep-sea chemosynthetic mussels (Bivalvia, Bathymodiolinae). Ecol. Evol 3(14):4748–4766. doi:10.1002/ece3.749
Tyler PA, Young CM, Dolan E, Arellano SM, Brooke SD, Baker M (2007a) Gametogenic periodicity in the chemosynthetic cold-seep mussel “Bathymodiolus” childressi. Mar Biol 150(5):829–840. doi:10.1007/s00227-006-0362-9
Tyler PA, Young CM, Dove F (2007b) Settlement, growth and reproduction in the deep-sea wood-boring bivalve mollusc Xylophaga depalmai. Mar Ecol Prog Ser 343:151–159. doi:10.3354/meps06832
Tyler PA, Marsh L, Baco-Taylor A, Smith CR (2009) Protandric hermaphroditism in the whale-fall bivalve mollusc Idas washingtonia. Deep Sea Res 56(19–20):1689–1699. doi:10.1016/j.dsr2.2009.05.014
Van Dover CL (2002) Community structure of mussel beds at deep-sea hydrothermal vents. Mar Ecol Prog Ser 230:137–158. doi:10.3354/meps230137
Van Dover CL, Berg CJ Jr, Turner RD (1988) Recruitment of marine invertebrates to hard substrates at deep-sea hydrothermal vents on the East Pacific Rise and Galapagos spreading center. Deep Sea Res 35(10–11):1833–1849. doi:10.1016/0198-0149(88)90052-0
Van Dover CL, Aharon P, Bernhard JM, Caylor E, Doerries M, Flickinger W, Gilhooly W, Goffredi SK, Knick KE, Macko SA, Rapoport S, Raulfs EC, Ruppel C, Salerno JL, Seitz RD, Sen Gupta BK, Shank T, Turnipseed M, Vrijenhoek R (2003) Blake Ridge methane seeps: characterization of a soft-sediment, chemosynthetically based ecosystem. Deep Sea Res 50(2):281–300. doi:10.1016/S0967-0637(02)00162-0
Wentrup C, Wendeberg A, Huang JY, Borowski C, Dubilier N (2013) Shift from widespread symbiont infection of host tissues to specific colonization of gills in juvenile deep-sea mussels. ISME J 7(6):1244–1247. doi:10.1038/ismej.2013.5
Young CM (2003) Reproduction, development and life-history traits. In: Tyler PA (ed) Ecosystems of the deep oceans. Elsevier, Amsterdam, pp 381–426
Young CM, Emson RH, Rice ME, Tyler PA (2013) A paradoxical mismatch of fecundity and recruitment in deep-sea opportunists: cocculinid and pseudococculinid limpets colonizing vascular plant remains on the Bahamian Slope. Deep Sea Res 92:36–45. doi:10.1016/j.dsr2.2013.01.027
Acknowledgments
We thank Antje Boetius and Catherine Pierre for samples collected during the BIONIL (M70/2b) and MEDECO cruises with RVs Meteor and RV Pourquoi Pas? funded by the ESF EUROCORES projects: CHEMECO and EuroDEEP and by the European Commission: EU HERMES and DIWOOD programs. Additional funding and logistics were met by IFREMER, CNRS and the Max-Planck-Institut für Mikrobiologie. We thank the captains and crews of RVs Meteor and RVs Pourquoi Pas? and those teams operating Quest 4000 (MARUM, Bremen, Germany) and ROVs Victor 6000 (Ifremer, France). At UPMC, our thanks go to Ghislaine Frébourg and Géraldine Toutirais (IFR 83) for assistance with TEM analysis. This work was co-funded by UPMC, HERMIONE EC (FP7/2007-2013-n° 226354) and a MARES grant. MARES is a Joint Doctorate Programme selected under Erasmus Mundus coordinated by Ghent University (FPA 2011-0016). See www.mares-eu.org for extra information. Our thanks go to the Editor and two anonymous reviewers whose comments greatly improved the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by J. Grassle.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Laming, S.R., Duperron, S., Cunha, M.R. et al. Settled, symbiotic, then sexually mature: adaptive developmental anatomy in the deep-sea, chemosymbiotic mussel Idas modiolaeformis . Mar Biol 161, 1319–1333 (2014). https://doi.org/10.1007/s00227-014-2421-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-014-2421-y