OJMS  Vol.5 No.2 , April 2015
Sterile Surfaces of Mnemiopsis leidyi (Ctenophora) in Bacterial Suspension—A Key to Invasion Success?
ABSTRACT
Seawater is a dense microbial suspension with >106 prokaryotic and >104 eukaryotic propagules per milliliter. Hence, submerged surfaces get immediately covered by biofilm-forming colonizers upon contact with seawater. Since biofilms may reduce individual fitness through decreasing motility and attractiveness or increasing shearing stress by water currents and infection risk by pathogens, marine organisms have evolved countermeasures to regulate the number of surface-colonizers; alternatively they tolerate settlement and biofilm-formation. Antimicrobial defense mechanisms co-evolved with potentially colonizing microbes. By contrast, non-native animals (neozoa) are confronted with novel microbial colonizers upon colonizing a new habitat, and are expected to be less well protected against surface-colonization. Here we present results of a thorough screening of the epithelial surface of the ctenophore Mnemiopsis leidyi, being non-native in European marine environments, for epithelial bacteria and archaea. Neither light- and electron-microscopic inspection nor PCR-screening for bacterial and archaeal DNA of 134 adult specimens from different collection sites in the Western Baltic revealed any presence of prokaryotes on the surface epithelium of comb jellies in a recently invaded environment. A limited number of bacterial associates became evident from whole-body extracts of both juvenile and adult comb jellies. Their taxonomic diversity, however, was significantly lower in adult than in juvenile specimens, suggesting a maturation of anti-microbial defense upon ontogenetic development. The mechanisms underlying the effective defense of Mnemiopsisagainst microbial colonization, however, remain unknown. Based on our findings, we propose 1) to make use of invasion events as natural space-for-time experiments on how symbiotic interactions change upon environmental change; and 2) to study basal metazoan animals, such as ctenophores, to understand the evolutionary basics of symbiont-host interactions.

Cite this paper
Hammann, S. , Moss, A. , Zimmer, M. , (2015) Sterile Surfaces of Mnemiopsis leidyi (Ctenophora) in Bacterial Suspension—A Key to Invasion Success?. Open Journal of Marine Science, 5, 237-246. doi: 10.4236/ojms.2015.52019.
References
[1]   Weis, V.M. (2008) Cellular Mechanisms of Cnidarian Bleaching: Stress Causes the Collapse of Symbiosis. Journal of Experimental Biology, 211, 3059-3066.

[2]   Steinert, M., Hentschel, U. and Hacker, J. (2000) Symbiosis and Parthogenesis: Evolution of the Microbe-Host Interaction. Naturwissenschaften, 87, 1-11. http://dx.doi.org/10.1007/s001140050001

[3]   Mayer, A.G. (1912) Ctenophores of the Atlantic Coast of North America. Carnegie Institution of Washington, (Publ. 162), 58 pp. http://dx.doi.org/10.5962/bhl.title.5968

[4]   Faasse, M.A. and Bayha, K.M. (2006) The Ctenophore Mnemiopsis leidyi A. Agassiz 1865 in Coastal Waters of the Netherlands: An Unrecognized Invasion? Aquatic Invasions, 1, 270-277.
http://dx.doi.org/10.3391/ai.2006.1.4.9

[5]   Hansson, H.G. (2006) Ctenophores of the Baltic and Adjacent Seas—The Invader Mnemiopsis Is Here! Aquatic Invasion, 1, 295-298. http://dx.doi.org/10.3391/ai.2006.1.4.16

[6]   Javidpour, J., Sommer, U. and Shiganova, T. (2006) First Record of Mnemiopsis leidyi A. Agassiz 1865 in the Baltic Sea. Aquatic Invasions, 1, 299-302. http://dx.doi.org/10.3391/ai.2006.1.4.17

[7]   Boersma, M., Malzahn, A., Greve, W. and Javidpour, J. (2007) The First Occurrence of the Ctenophore Mnemiopsis leidyi in the North Sea. Helgoland Marine Research, 61, 153-155.
http://dx.doi.org/10.1007/s10152-006-0055-2

[8]   Vinogradov, M.E., Shushkina, E.A., Musayeva, E.I. and Sorokin, P.Y. (1989) A New Exotic Species in the Black Sea: The Ctenophore Mnemiopsis leidyi (Ctenophora: Lobata). Oceanology, 29, 220-224.

[9]   Studenikina, Y.I., Volovik, S.P., Mirzoyan, I.A. and Luts, G.I. (1991) The Ctenophore Mnemiopsis leidyi in the Sea of Azov. Oceanology, 31, 722-725.

[10]   Shiganova, T.A. (1993) Ctenophore Mnemiopsis leidyi and Ichthyoplankton in the Sea of Marmara in October of 1992. Oceanology, 33, 900-903.

[11]   Dunn, C.W., Hejnol, A., Matus, D.Q., Pang, K., Browne, W.E., Smith, S.A., et al. (2008) Broad Phylogenomic Sampling Improves Resolution of the Animal Tree of Life. Nature, 452, 745-749.
http://dx.doi.org/10.1038/nature06614

[12]   Hejnol, A., Obst, M., Stamatakis, A., Ott, M., Rouse, G.W., Edgecombe, G.D., et al. (2009) Assessing the Root of Bilaterian Animals with Scalable Phylogenomic Methods. Proceedings of the Royal Society B, 276, 4261-4270. http://dx.doi.org/10.1098/rspb.2009.0896

[13]   Wallberg, A., Thollesson, M., Farris, J.S. and Jondelius, U. (2004) The Phylogenetic Position of the Comb Jellies (Ctenophora) and the Importance of Taxonomic Sampling. Cladistics, 20, 558-578. http://dx.doi.org/10.1111/j.1096-0031.2004.00041.x

[14]   Sorarrain, D.R., Ramirez, F. and Mianzan, H. (2001) Hyperoche medusarum (Kr?yer, 1838) (Amphipoda, Hyperiidae) and Mnemiopsis mccradyi (Mayer, 1910) (Ctenophora): A New Host and First Record of This Association for the Southwestern Atlantic. Crustaceana, 74, 407-410.
http://dx.doi.org/10.1163/156854001300104499

[15]   Gasca, R. and Haddock, H.D. (2004) Associations between Gelatinous Zooplankton and Hyperiid Amphipods (Crustacea: Peracarida) in the Gulf of California. Hydrobiologia, 530-531, 529-535. http://dx.doi.org/10.1007/s10750-004-2657-5

[16]   Martorelli, S.R. (2001) Digenea Parasites of Jellyfish and Ctenophores of the Southern Atlantic. Hydrobiologia, 451, 305-310. http://dx.doi.org/10.1023/A:1011862406670

[17]   Reitzel, A.M., Sullivan, J.C., Brown, B.K., Chin, D.W., Cira, E.K., Edquist, S.K., Genco, B.K., Joseph, O.C., Kaufman, C.A., Kovitvongsa, K., Mu-oz, M.M., Negri, T.L., Taffel, J.R., Zuehlke, R.T. and Finnerty, J.T. (2007) Ecological and Developmental Dynamics of a Host-Parasite System Involving a Sea Anemone and Two Ctenophores. Journal of Parasitology, 93, 1392-1402. http://dx.doi.org/10.1645/GE-1250.1

[18]   Mills, C.A. and McLean, N. (1991) Ectoparasitism by a Dinoflagellate (Dinoflagellata: Oodinidae) on 5 Ctenophores (Ctenophora) and a Hydromedusa (Cnidaria). Diseases of Aquatic Organisms, 10, 211-216. http://dx.doi.org/10.3354/dao010211

[19]   Estes, A.M., Reynolds, B.S. and Moss, A.G. (1997) Trichodina ctenophorii N. Sp., a Novel Symbiont of Ctenophores of the Northern Coast of the Gulf of Mexico. Journal of Eukaryotic Microbiology, 44, 420-426. http://dx.doi.org/10.1111/j.1550-7408.1997.tb05718.x

[20]   Moss, A.G., Estes, A.M., Muellner, L.A. and Morgan, D.D. (2001) Protistan Epibionts of the Ctenophore Mnemiopsis mccradyi Mayer. Hydrobiologia, 451, 295-304.
http://dx.doi.org/10.1023/A:1011846022599

[21]   Khan, R.A. (1990) Parasitism in Marine Fish after Chronic Exposure to Petroleum Hydrocarbons in the Laboratory and to the Exxon Valdez Oil Spill. Bulletin of Environmental Contamination and Toxicology, 44, 759-763. http://dx.doi.org/10.1007/BF01701799

[22]   Khan, R.A., Berker, D.E., Williams-Ryan, K. and Hooper, R.G. (1993) Influence of Crude Oil and Pulp and Paper Mill Effluent on Mixed Infections of Trichodina cottidarium and T. saintjohnsi (Ciliophora) Parasitizing Myoxiocephalus octodecemspinosus and M. scorpius. Canadian Journal of Zoology, 72, 247-251. http://dx.doi.org/10.1139/z94-033

[23]   Dale, C. and Moran, N.A. (2006) Molecular Interactions between Bacterial Symbionts and Their Hosts. Cell, 126, 453-465. http://dx.doi.org/10.1016/j.cell.2006.07.014

[24]   Moran, N. and Baumann, P. (2000) Bacterial Endosymbionts in Animals. Current Opinion in Microbiology, 3, 270-275. http://dx.doi.org/10.1016/S1369-5274(00)00088-6

[25]   Fraune, S. and Bosch, T.C.G. (2007) Long-Term Maintenance of Species-Specific Bacterial Microbiota in the Basal Metazoan Hydra. Proceedings of the National Academy of Sciences of the USA, 104, 13146-13151. http://dx.doi.org/10.1073/pnas.0703375104

[26]   Fraune, S. and Zimmer, M. (2008) Host-Specificity of Environmentally Transmitted Mycoplasma-Like Isopod Symbionts. Environmental Microbiology, 10, 2497-2504. http://dx.doi.org/10.1111/j.1462-2920.2008.01672.x

[27]   Moss, A.G., Rapoza, R.C. and Muellner, L. (2001) A Novel Cilia-Based Feature within the Food Grooves of the Ctenophore Mnemiopsis mccradyi Mayer. Hydrobiologia, 451, 287-294.
http://dx.doi.org/10.1023/A:1011833618965

[28]   Daniels, C. and Breitbart, M. (2012) Bacterial Communities Associated with the Ctenophores Mnemiopsis leidyi and Beroe ovata. FEMS Microbiology Ecology, 82, 90-101.
http://dx.doi.org/10.1111/j.1574-6941.2012.01409.x

[29]   Dinasquet, J., Granhag, L. and Riemann, L. (2012) Stimulated Bacterioplankton Growth and Selection for Certain Bacterial Taxa in the Vicinity of the Ctenophore Mnemiopsis leidyi. Frontiers in Microbiology, 3, 302. http://dx.doi.org/10.3389/fmicb.2012.00302

[30]   Sánchez, M.I., Rode, N.O., Flaven, E., Redón, S., Amat, F., Vasileva, G.P. and Lenormand, T. (2012) Differential Susceptibility to Parasites of Invasive and Native Species of Artemia Living in Sympatry: Consequences for the Invasion of A. franciscana in the Mediterranean Region. Biological Invasions, 14, 1819-1829. http://dx.doi.org/10.1007/s10530-012-0192-2

[31]   Slothouber, J.G.M., Smith, G.J.E., Becnel, J.J., Butlin, R.K. and Dunn, A.M. (2010) Reduction in Post-Invasion Genetic Diversity in Crangonyx pseudogracilis (Amphipoda: Crustacea): A Genetic Bottleneck or the Work of Hitchhiking Vertically Transmitted Microparasites? Biological Invasions, 12, 191-209. http://dx.doi.org/10.1007/s10530-009-9442-3

[32]   Henne, A., Daniel, R., Schmitz, R.A. and Gottschalk, G. (1999) Construction of Environmental DNA Libraries in Escherichia coli and Screening for the Presence of Genes Conferring Utilization of 4-Hydroxybutyrate. Applied and Environmental Microbiology, 65, 3901-3907.

[33]   Chao, A. (1984) Nonparametric Estimation of the Number of Classes in a Population. Scandinavian Journal of Statistics, 11, 265-270.

[34]   Elton, C.S. (1958) The Ecology of Invasions by Animals and Plants. Methuen, London.
http://dx.doi.org/10.1007/978-1-4899-7214-9

[35]   Keane, R.M. and Crawley, M.J. (2002) Exotic Plant Invasions and the Enemy Release Hypothesis. Trends in Ecology and Evolution, 17, 164-170. http://dx.doi.org/10.1016/S0169-5347(02)02499-0

[36]   Mitchell, C.E. and Power, A.G. (2003) Release of Invasive Plants from Fungal and Viral Pathogens. Nature, 421, 625-627. http://dx.doi.org/10.1038/nature01317

[37]   De Walt, S.J., Denslow, J.S. and Ickes, K. (2004) Natural-Enemy Release Facilitates Habitat Expansion of the Invasive Tropical Shrub Clidemia hirta. Ecology, 85, 471-483. http://dx.doi.org/10.1890/02-0728

[38]   Blumenthal, D.M. (2006) Interactions between Resource Availability and Enemy Release in Plant Invasion. Ecology Letters, 9, 887-895. http://dx.doi.org/10.1111/j.1461-0248.2006.00934.x

[39]   Williamson, M. and Fitter, A. (1996) The Varying Success of Invaders. Ecology, 77, 1661-1666. http://dx.doi.org/10.2307/2265769

[40]   Lockwood, J.L., Hoopes, M. and Marchetti, M. (2007) Invasion Ecology. Blackwell Publishers, Oxford.

[41]   Donovan, E.W., Dodson, M.B. and Moss, A.G. (2010) Bacterial Assemblages of the Lobate Ctenophore, Mnemiopsis. Proceedings of the Annual Meeting American Society for Limnology and Oceanography, Santa Fe, 6-11 June 2010.

[42]   Taylor, J.C., Odom, D.C. and Moss, A.G. (2006) Benthic Interactions in Mnemiopsis. Proceedings of the Annual Meeting of the American Society of Limnology and Oceanography, Victoria, 4-9 June 2006.

[43]   Hernandez-Nicaise, M.-L. (1973) The Nervous System of Ctenophores III. Ultrastructure of Synapses. Journal of Neurocytology, 2, 249-263. http://dx.doi.org/10.1007/BF01104029

[44]   Hernandez-Nicaise, M.-L. (1974) Ultrastructural Evidence for a Sensory-Motor Neuron in Ctenophora. Tissue and Cell, 6, 43-47. http://dx.doi.org/10.1016/0040-8166(74)90021-4

[45]   Doebeli, M. and Dieckmann, U. (2000) Evolutionary Branching and Sympatric Speciation Caused by Different Types of Ecological Interactions. The American Naturalist, 156, 77-101.
http://dx.doi.org/10.1086/303417

[46]   Buckling, A. and Rainey, P.B. (2002) The Role of Parasites in Sympatric and Allopatric Host Diversification. Nature, 420, 496-499. http://dx.doi.org/10.1038/nature01164

[47]   Leonardo, T.E. and Muiru, G.T. (2003) Facultative Symbionts Are Associated with Host Plant Specialization in Pea Aphid Populations. Proceedings of the Royal Society of London B, 270, S209-S212. http://dx.doi.org/10.1098/rsbl.2003.0064

[48]   Watson, R.A. and Pollack, J.B. (2003) A Computational Model of Symbiotic Composition in Evolutionary Transitions. Biosystems, 69, 187-209. http://dx.doi.org/10.1016/S0303-2647(02)00135-1

[49]   Mills, C.E. (1998) Phylum Ctenophora: List of all Valid Species Names.
http://faculty.washington.edu/cemills/Ctenolist.html

[50]   Morrow, K.M. and Chadwick, N. (2010) Competition among Sessile Organisms on Coral Reefs. In: Dubinsky, Z. and Stambler, N., Eds., Coral Reefs: An Ecosystem in Transition, Springer, New York.

[51]   Morrow, K.M., Moss, A.G., Chadwick, N. and Liles, M. (2012) Bacterial Associates of Two Caribbean Coral Species Reveal Species-Specific Distribution and Geographic Variability. Applied and Environmental Microbiology, 78, 6438-6449. http://dx.doi.org/10.1128/AEM.01162-12

[52]   Morrow, K.M., Liles, M.R., Paul, V.J., Moss, A.G. and Chadwick, N.E. (2013) Bacterial Shifts Associated with Coral-Macroalgal Competition at Three Caribbean Reef Locations. Marine Ecology Progress Series, 488, 103-117.

 
 
Top