Abstract
During the 2010/2011 Exploration vessel Nautilus expedition to the Mediterranean Sea, samples of Lamellibrachia (Siboglinidae, Annelida) were imaged in situ and collected from hydrothermal vent and methane “cold seeps.” An analysis of these Lamellibrachia and their endosymbiotic thioautotrophic gammaproteobacteria reveals two distinct endosymbiont phylotypes. Phylotype 1 was present in Lamellibrachia specimens from 947 m at the Eratosthenes seamount seep (a seep off Cyprus in the Eastern Mediterranean), and Phylotype 2 was found in siboglinids from 618 m at a hydrothermal vent within Palinuro volcanic complex in Tyrrhenian Sea. Both phylotypes coexist in siboglinids at 1,036 m from the Palmachim disturbance, a cold seep in the Eastern Mediterranean’s Levantine basin. Our results, combined with existing knowledge of siboglinid host and endosymbiotic bacteria biogeography, reveal that two major groups of endosymbionts coexist within lamellibranchids and escarpids. The phylogenetic clustering of these bacteria is primarily influenced by geographic location, rather than selection by the siboglinid host.
Similar content being viewed by others
References
Carey SN, Croff Bell CL, Rosi M, Marani M, Nomikou P, Walker SL, Faure K, Kelly J (2012) Submarine volcanoes of the Aeolian Arc, Tyrrhenian Sea. Oceanography 25:32–33
Cavanaugh CM, Levering P, Maki J, Mitchell R, Lidstrom M (1987) Symbiosis of methylotrophic bacteria and deep-sea mussels. Nature 325:346–348
Corliss JB, Ballard R (1977) Oasis of life in the cold abyss. Natl Geogr Mag 152:441–453
Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, Hagevoort RG, Edrington TS (2008) Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol 8:125
Dubilier N, Bergin C, Lott C (2008) Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol 6:725–740
Duperron S, de Beer D, Zbinden M, Boetius A, Schipani V, Kahil N, Gaill F (2009) Molecular characterization of bacteria associated with the trophosome and the tube of Lamellibrachia sp., a siboglinid annelid from cold seeps in the eastern Mediterranean. FEMS Microbiol Ecol 69:395–409
Feldman R, Black M, Cary C, Lutz R, Vrijenhoek RC (1997) Molecular phylogenetics of bacterial endosymbionts and their vestimentiferan hosts. Mol Mar Biol Biotechnol 6:268–277
Feldman R, Shank T, Black M (1998) Vestimentiferan on a whale fall. Biol Bull 194:116–119
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Freytag JK, Girguis PR, Bergquist DC, Andras JP, Childress JJ, Fisher CR (2001) A paradox resolved: sulfide acquisition by roots of seep tubeworms sustains net chemoautotrophy. Proc Natl Acad Sci USA 98:13408–13413
Gambi MC, Schulze A, Amato E (2011) Record of Lamellibrachia (Annelida, Siboglinidae, Vestimentifera) from a deep shipwreck in the Western Mediterranean Sea (Italy). Mar Biodivers Rec 4:e24
Hasegawa M (1985) Dating the human-ape split by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174
Hilário A, Capa M, Dahlgren TG, Halanych KM, Little CTS, Thornhill DJ, Verna C, Glover AG (2011a) New perspectives on the ecology and evolution of siboglinid tubeworms. PLoS ONE 6:e16309
Hilário A, Comas MC, Azevedo L, Pinheiro L, Ivanov MK, Cunha MR (2011b) First record of a vestimentifera (Polychaeta: Siboglinidae) from chemosynthetic habitats in the western Mediterranean Sea—biogeographical implications and future exploration. Deep Sea Res Part I Oceanogr Res Pap 58:200–207
Hughes D, Crawford M (2008) A new record of the vestimentiferan Lamellibrachia sp. (Polychaeta: Siboglinidae) from a deep shipwreck in the eastern Mediterranean. Mar Biodivers Rec 1:e21
Jones ML (1981) Riftia pachyptila Jones: observations on the vestimentiferan worm in the Galapagos Rift. Science 213:333–336
Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
McMullin E, Hourdez S, Schaeffer S (2003) Phylogeny and biogeography of deep sea vestimentiferan tubeworms and their bacterial symbionts. Symbiosis 34:1–41
Nussbaumer AD, Fisher CR, Bright M (2006) Horizontal endosymbiont transmission in hydrothermal vent tubeworms. Nature 441:345–348
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 Part I Oceanogr Res Pap 51:1915–1936
Petersen JM, Wentrup C, Verna C, Knittel K, Dubilier N (2012) Origins and evolutionary flexibility of chemosynthetic symbionts from deep-sea animals. Biol Bull 223:123–137
Pflugfelder B, Fisher CR, Bright M (2005) The color of the trophosome: elemental sulfur distribution in the endosymbionts of Riftia pachyptila (Vestimentifera; Siboglinidae). Mar Biol 146:895–901
Pilloni G, Granitsiotis MS, Engel M, Lueders T (2012) Testing the limits of 454 pyrotag sequencing: reproducibility, quantitative assessment and comparison to T-RFLP fingerprinting of aquifer microbes. PLoS ONE 7:e40467
Schmaljohann R, Flügel H (1987) Methane-oxidizing bacteria in Pogonophora. Sarsia 72:91–98
Shakya M, Quince C, Campbell JH, Yang ZK, Schadt CW, Podar M (2013) Comparative metagenomic and rRNA microbial diversity characterization using archaeal and bacterial synthetic communities. Environ Microbiol 15:1882–1899
Smirnov R (2000) Two new species of Pogonophora from the arctic mud volcano off northwestern Norway. Sarsia 85:141–150
Southward EC, Andersen AC, Hourdez S (2011) Lamellibrachia anaximandri n. sp., a new vestimentiferan tubeworm (Annelida) from the Mediterranean, with notes on frenulate tubeworms from the same habitat. Zoosystema 33(3):245–279
Stewart FJ, Cavanaugh CM (2006) Symbiosis of thioautotrophic bacteria with Riftia pachyptila. Prog Mol Subcell Biol 41:197–225
Tamura K (1992) Estimation of the number of nucleotide substitutions when there are strong transition–transversion and G + C-content biases. Mol Biol Evol 9:678–687
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Thiel V, Hügler M, Blümel M et al (2012) Widespread occurrence of two carbon fixation pathways in tubeworm endosymbionts: lessons from hydrothermal vent associated tubeworms from the Mediterranean Sea. Front Microbiol 3:423
Tyler PA, Young CA (1999) Reproduction and dispersal at vents and cold seeps. J Mar Biol Assoc UK 79:193–208
Acknowledgments
We thank the European Commission FP7 research infrastructure initiative program, “Assemble 227799,” for partial support of this project. This research used samples and data provided by the E/V Nautilus Exploration Program—expeditions NA008, NA009, NA015 and NA019. The authors would like to thank all individuals who helped during the expedition, including onboard technical and scientific personnel, and the captain and crew of the E/V Nautilus.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. Kühl.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Rubin-Blum, M., Tsadok, R., Shemesh, E. et al. Distribution of the Lamellibrachia spp. (Siboglinidae, Annelida) and their trophosome endosymbiont phylotypes in the Mediterranean Sea. Mar Biol 161, 1229–1239 (2014). https://doi.org/10.1007/s00227-014-2413-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-014-2413-y