Molecular mechanisms of marine symbioses

All higher organisms are associated with microorganisms. The coexistence of these dissimilar partners and their host-microbe interactions are crucial for life on earth. Detailed knowledge of microbial physiology and molecular interaction mechanisms is therefore pivotal for understanding biological processes. Bacterial symbionts perform many functions: they supply their hosts with nutrients, provide access to inhospitable habitats or enable their hosts to produce antimicrobial or bioactive substances. However, many of these processes are poorly understood. To elucidate molecular mechanisms behind symbiotic associations, we therefore examine marine invertebratestube worms and bivalvesand their bacterial symbionts with (meta)proteomic methods.

Thiotrophic symbioses

Proteome analysis of the endosymbiont of Riftia pachyptila
Fig. 1. Physiological proteomics of the uncultivable Riftia pachyptila endosymbiont

Sulfidic habitats are toxic to most animals and plants. Yet, some animals are excellently adapted to these challenging ecosystems, e.g. at hot sulfur springs (hydrothermal vents) in the deep sea, or in sulfidic sediments of tropical seagrass meadows. Key to this adaptation are highly specialized symbioses with sulfur-oxidizing (thiotrophic) bacteria. The deep-sea tubeworm Riftia pachyptila (Fig. 1), for example, is an impressive representative of the diverse fauna at hydrothermal vents in the Eastern Pacific Ocean. Although they reach body lengths of up to 1.5 m, adult tubeworms completely lack a digestive system. Instead, they rely on bacterial symbionts inside their body cavity, which provide nutrition to their hosts. The bacteria are able to generate energy from hydrogen sulfide oxidation and use this energy for CO2 fixation. The resulting organic compounds not only feed the symbionts, but also the host. Similar host-microbe relationships are observed in deep-sea bivalves of the genus Bathymodiolus and in tropical shallow-water clams of the Lucinidae family.

During several DFG-funded projects, we were able to characterize the yet uncultured Riftia symbiont as well as its tubeworm host, thus gaining important insights into the physiology of the holobiont and fundamental host-symbiont interactions using high-resolution proteome analysis techniques [1-3]. During the EU-funded Symbiomics project, a collaboration with the Max Planck Institute for Marine Microbiology Bremen, our investigation of symbiotic interactions in deep-sea Bathymodiolus mussels yielded unprecedented insights into physiological interdependencies between mussel hosts and symbionts, as well as into similarities and differences between Pacific and Atlantic Bathymodiolus species [4, 5]. Together with colleagues from the Université des Antilles in Guadeloupe we were able to show that thiotropic lucinid symbionts not only detoxify sulfide and fix CO2, but that they are also capable of nitrogen fixation – thus serving their clam hosts in three ways [6].

Responsible staff members:

Dr. Stephanie Markert, Tjorven Hinzke

Heterotrophic symbioses

Shipworms are wood-boring bivalves that thrive in marine ecosystems of all oceans. They are of immense economic importance as they can destroy wooden structures such as ships, groynes and wharfs. The molluscs live in close symbiosis with nitrogen-fixing bacteria residing in the animals' gills. Our knowledge of the bacterial symbionts' physiology and their role in this symbiosis is very limited as yet. In a study funded by the German Federal Environmental Foundation (DBU), we were able to isolate a bacterial symbiont of the genus Teredinibacter from specimens of the Baltic Sea shipworm Teredo navalis LINNAEUS, 1758. In cooperation with the Göttingen Genomics Laboratory (G2L) and the German Collection of Microorganisms and Cell Cultures GmbH (DSMZ), we sequenced the genome of this new species. Based on this genome information, we are currently analyzing physiological proteome profiles of the symbiont in order to better understand the symbiosis and especially its ability to digest lignocellulose. In addition, we investigate the shipworm symbiont's pharmaceutically relevant potential for secondary metabolite production in cooperation with the Leibniz Institute for Natural Product Research and Infection Biology e. V. Hans-Knöll-Institut (HKI) Jena.

Responsible staff members:

Stefan E. Heiden, Christian Schmidt

 

Literature:

  1. Gardebrecht A, Markert S, Sievert SM, Felbeck H, Thürmer A, Albrecht D, Wollherr A, Kabisch J, Le Bris N, Lehmann R, Daniel R, Liesegang H, Hecker M, Schweder T. 2012. Physiological homogeneity among the endosymbionts of Riftia pachyptila and Tevnia jerichonana revealed by proteogenomics. ISME J. 6(4):766-76.
  2. Markert S, Arndt C, Felbeck H, Becher D, Sievert SM, Hügler M, Albrecht D, Robidart J, Bench S, Feldman RA, Hecker M, Schweder T. 2007. Physiological Proteomics of the Uncultured Endosymbiont of Riftia pachyptila. Science. 315(5809):247-50.
  3. Markert S, Gardebrecht A, Felbeck H, Sievert SM, Klose J, Becher D, Albrecht D, Thürmer A, Daniel R, Kleiner M, Hecker M, Schweder T. 2011. Status quo in physiological proteomics of the uncultured Riftia pachyptila endosymbiont. Proteomics. 11(15):3106-17.
  4. Ponnudurai R, Kleiner M, Sayavedra L, Petersen JM, Moche M, Otto A, Becher D, Takeuchi T, Satoh N, Dubilier N, Schweder T, Markert S. 2017. Metabolic and physiological interdependencies in the Bathymodiolus azoricus symbiosis. ISME J. 11(2):463-477.
  5. Ponnudurai R, Sayavedra L, Kleiner M, Heiden SE, Thürmer A, Felbeck H, Schlüter R, Sievert SM, Daniel R, Schweder T, Markert S. 2017. Genome sequence of the sulfur-oxidizing Bathymodiolus thermophilus gill endosymbiont. Stand Genomic Sci. 12:50.
  6. König S, Gros O, Heiden SE, Hinzke T, Thürmer A, Poehlein A, Meyer S, Vatin M, Mbéguié-A-Mbéguié D, Tocny J, Ponnudurai R, Daniel R, Becher D, Schweder T, Markert S. 2016. Nitrogen fixation in a chemoautotrophic lucinid symbiosis. Nat Microbiol. 2:16193.