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Symbioses from hydrothermal vents and cold seeps

Teeming 'oases of life' in the deep sea

Deep-sea hydrothermal vents and cold seeps are colonized by dense communities of animals hosting chemosynthetic symbiotic bacteria that provide them with nutrition. These symbionts use geofuels such as methane, reduced sulfur compounds and hydrogen, emitted from the sea floor at vents and seeps, as an energy source to fix inorganic carbon or methane into biomass. The establishment of symbioses with chemosynthetic bacteria as primary producers is the evolutionary innovation that allowed invertebrate animals to thrive in these extreme habitats where the input of organic matter from photosynthesis is extremely low.

One of our major research topics is the symbiosis between deep-sea Bathymodiolus mussels and their chemosynthetic symbionts. We use a wide array of methods to try to answer questions such as:

How have hosts and symbionts co-evolved?

How does biogeography shape these symbiotic associations?

How is the association established and maintained?

How does the environment shape the ecology and evolution of the associations?
Hydrothermal vent on the Mid Atlantic Ridge
(c)IFREMER
Gaz Hydrate -Cold Seep- in the Gulf Of Mexico
(c)Marum

Research highlights

Bathymodiolus mussels: a symbiotic foursome (at least!)

Christian Borowski, Adrien Assie, Lizbeth Sayavedra, Rebecca Ansorge, Benedikt Geier, Merle Ücker, Maxim Rubim Blum, Målin Tietjen, Miguel Ángel González Porras, Maximillian Franke


Bathymodiolus mussels are one of the most dominant members of the biota at many hydrothermal vents and cold seeps worldwide. Bathymodiolus mussels can produce biomass of up to 70 kg per square meter - two to five times as much as their shallow-water relative the blue mussel Mytilus edilus produces in natural or commercial mussel beds - because these deep-sea mussels benefit from the chemosynthetic symbionts in their gills. The symbiotic bacteria are intracellular and occur in membrane-enclosed host vacuoles of specialized gill cells called bacteriocytes. Many Bathymodiolus mussels live in a dual symbiosis with both sulfur- and methane-oxidizing bacteria.

FISH picture of Bathymodiolus gills
Fluorescent in situ Hybridization image done with structured illumination microscopy of a Bathymodiolus puteoserpentis gill filament. Thiotrophic symbiont 16S rRNA (green: Cy5) Methanotrophic symbiont 16S rRNA (red: Atto488) Host DNA (blue: DAPI) © M. Á. González Porras
Our research is constantly revealing an unexpectedly high diversity of symbionts in these mussels. Some species such as B. heckerae have at least four gill symbionts including two distinct but closely related sulfur oxidizers, a methanotroph, and a methylotroph Duperron et al. 2008. Other species are infected by intranuclear bacteria Zielinski et al. 2009. Together with our collaborators Kai-Uwe Hinrichs and Florence Schubotz from Marum at the University of Bremen, we recently investigated Bathymodiolus mussels from the Chapopote asphalt seep in the Gulf of Mexico. Intriguingly, B. heckerae from this unique site associate with an additional Cycloclasticus symbiont that may use hydrocarbons from the asphalt as an energy source Raggi et al. 2013.

In addition to unexpected symbiont diversity, we are also constantly discovering novel metabolic traits in the symbionts. We recently discovered that the sulfur-oxidizing symbionts of Bathymodiolus mussels can use hydrogen as an energy source Petersen et al. 2011. Until our study, only two energy sources (methane and reduced sulfur compounds) had been shown to power chemosynthetic symbioses in the 30 years since their discovery. This study was a great collaborative effort with partners from Europe and the USA, including Wolfgang Bach and Thomas Pape from MARUM at the University of Bremen, Pete Girguis from Harvard University, Stephane Hourdez from the Biological Station in Roscoff, Richard Seifert from the University of Hamburg, and Rudolf Amann, head of the Department of Molecular Ecology here at the MPI.

The Bathymodiolus sulfur-oxidizing symbionts are closely related to free-living SUP05 bacteria found worldwide in marine oxygen minimum zones, and to the obligate symbionts of vesicomyid clams Petersen et al. 2012. We are currently comparing the genomes of these closely related sulfur-oxidizing bacteria to search for genomic signatures of their unique lifestyles. Our Bathymodiolus genomics projects are currently done in collaboration with Genoscope in France and with Nori Satoh at the Okinawa Institute for Science and Technology, Japan. To analyze gene expression in the symbionts, we do proteomics together with our collaborator Thomas Schweder from the University of Greifswald, and transcriptomics with Thorsten Reusch from Geomar and Philip Rosenstiel from the IKMB in Kiel.

The symbionts of Bathymodiolus mussels are thought to be horizontally transmitted, which means that the symbionts are taken up from the environment by each new host generation. Moreover, in bivalves, gill tissues grow continuously throughout the animal's lifetime, and new gill tissue must be colonized by symbionts, but nothing is known about these colonization processes. We are currently investigating symbiont uptake in juvenile and adult Bathymodiolus mussels using fluorescence in situ hybridization (FISH) and transmission electron microscopy (TEM). We are comparing colonization patterns in Bathymodiolus mussels with those in vesicomyid clams, which pass their symbionts directly to the next generation via the eggs (termed vertical transmission), to investigate how transmission mode affects colonization. Our first results showed that symbionts broadly colonize tissues of the smallest Bathymodiolus mussels, and are restricted to the gill tissues at later ontogenic stages Wentrup et al. 2013.
Rimicaris shrimp

Adrien Assie, Jillian Petersen, Christian Borowski

Rimicaris shrimp form giant swarms on hydrothermal vent chimneys in the Atlantic and Indian oceans. They host a dense community of chemosynthetic epibionts in their modified gill chamber. The epibiosis is dominated by filamentous gamma- and epsilonproteobacteria. Although the epibionts are assumed to contribute to the shrimp's nutrition, direct evidence for this is still lacking. We showed that epibionts on R. exoculata from Mid-Atlantic Ridge vents have distinct biogeographic distribution patterns Petersen et al. 2010. We are currently investigating epibiont biogeography on R. hybisae from two vents in the Mid-Cayman Spreading Center, which are only 20 km apart but are separated by 2.5 km water depth. The shrimp epibionts have a free-living stage during their life cycle, and these free-living symbionts are abundant at the vent sites colonized by Rimicaris. We will compare the biogeography of the free-living and host-associated symbionts to answer the question: Is everything everywhere and the partners select? In this project we collaborate with Cindy Van Dover (Duke University, USA) and Julie Huber (Marine Biological Laboratory, USA).
Rimicaris shrimp on a hydrothermal chimney
(c)IFREMER
Ifremeria nautilei

Christian Borowski

One of the most abundant animals at hydrothermal vent systems of the Western Pacific is the snail Ifremeria nautilei. These hosts harbor at least 4 bacterial symbionts in their gills, sulfide- and methane-oxidizing gammaproteobacteria and at least 2 alphaproteobacterial phylotypes of unknown function. We are currently using comparative sequence analysis of phylogenetic and functional genes to gain a better understanding of these symbioses (Borowski et al. In prep.).
Vestimentiferan tubeworms

Judith Zimmermann, Jillian Petersen

Lamellibrachia and Escarpia tubeworms can be found worldwide at hydrothermal vents, cold seeps, whale falls and shipwrecks. They completely lack a digestive system and rely on endosymbiotic chemosynthetic symbionts for nutrition. We study tubeworms from the Chapopote asphalt seep in the Gulf of Mexico and the Marsili hydrothermal vent in the Mediterranean Sea (See article Do Mediterranean tubeworms like it hot?).
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