Research

Claudia Bergin, Christian Lott, Caroline Rühland, Cecilia Wentrup, Manuel Kleiner, Silke Wetzel


Gutless oligochaetes are a unique group of marine worms that have no mouth or gut, and are the only free-living animals known to have also reduced their nephridia (kidney-like excretory organs).

Gutless oligochaetes are bright white because of the elemental sulfur stored in their bacterial endosymbionts.

Who? 

The diversity of symbionts in gutless oligochaetes is higher than in all other chemosynthetic symbioses, with as many as six 16S rRNA phylotypes co-occurring in a single worm. Despite this remarkable diversity, the associations are highly specific and stable.


What? 

Our metagenomic analyses of the symbionts in Olavius algarvensis have revealed how its consortium of sulfur-oxidizing and sulfate-reducing bacteria uses different energy sources and metabolic pathways to provide it with an optimal energy supply.


How? 

Phylogenetic analyses of the oligochaete symbionts and their hosts suggest that both co-speciation and biogeography played a role in the establishment of these symbioses.
Different transmission modes of the symbionts may influence their evolutionary patterns.

In situ identification of 5 co-occurring bacterial symbionts in O. crassitunicatus. Epifluorescence image of the symbiont-containing region of the worm's body wall. Triple hybridization with the 2 gammaproteobacterial symbionts in red (using the general gammaproteobacterial probe GAM42), the 3 deltaproteobacterial symbionts in blue (using the general deltaproteobacterial probe for bacteria belonging to the Desulfosarcina, Desulfofaba, Desulfococcus, Desulfofrigus, and Desulforhopalus genera DSS658/DSR651), and spirochete symbionts in yellow using the specific probe for the spirochete symbionts of O. crassitunicatus (from Blazejak et al. 2005).

Gutless oligochaetes are small worms of 0.2 mm diameter and 1-2 cm length live in an obligate association with endosymbiotic bacteria. In contrast to intracellular endosymbionts that are not directly exposed to the external environment of the host, the endosymbionts of gutless oligochaetes are extracellular, living just below the "skin" of the worms in a space between the outer cuticle and the internal epidermal cells called the symbiont-containing region. The cuticle is highly permeable to both small charged molecules and uncharged substances so that the symbiotic bacteria have free access to most dissolved compounds in the sediment pore waters surrounding the worms.

Our studies on the phylogeny of the oligochaete bacteria have revealed a remarkable diversity of the symbionts, with up to 5 - 6 different 16S rRNA phylotypes co-occurring in the symbiont-containing region. In all host species, the primary endosymbionts are chemoautotrophic sulfide-oxidizers that belong to the gamma subclass of Proteobacteria and are related to free-living sulfide-oxidizers such as Allochromatium vinosum. In addition to the primary symbionts, up to 5 other bacterial phylotypes belonging to the Alphaproteobacteria (Blazejak et al. 2006), Deltaproteobacteria, or the Spirochaetes can co-exist in the same host species (Dubilier et al. 2006).

For the oligochaete hosts, the association is clearly obligate, given their complete reduction of a digestive and excretory system. For the symbionts, that remain as yet uncultivable, it is not known if they can also survive in a free-living stage in the environment.

Christian Borowski, Dennis Fink, Luciana Raggi, Karina van der Heijden, Jillian Petersen, Frank Zielinski, Silke Wetzel

Most of the biomass at hydrothermal vents and cold seeps is in invertebrates that harbor symbiotic bacteria. The bacteria use the reduced energy sources in these chemosynthetic environments to feed their hosts.

Gill symbionts

Who?

Our studies have revealed a previously unrecognized diversity of bacterial symbionts in vent and seep invertebrates.

How?

Phylogenetic analyses of the symbionts of vent shrimp show that these exhibit biogeographic patterns, while closely related free-living vent bacteria do not. This suggests that in shrimp symbioses, the host selects.

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.).

As part of the German Research Foundation Priority Program "Energy-, Material-, and Life-Cycles at Spreading Axes" we have begun investigating the transfer of geochemical energy to one of the major groups of primary producers at hydrothermal vents on the Mid-Atlantic Ridge (MAR), endosymbiotic bacteria of bivalve hosts. Cruises within the Priority Program to the Logatchev vent field on the northern MAR and newly discovered vent fields on the southern MAR were successful in collecting symbiotic invertebrates for the proposed studies. One of our first studies shows that the Bathymodiolus mussels from 4 different vent sites in the northern MAR harbor the same methanotrophic and thiotrophic symbionts (Duperron et al. 2006).

Further studies on symbioses from the northern Mid-Atlantic Ridge are currently underway as part of the European Commission Marie Curie Research Training Network MomarNet (Monitoring deep sea floor hydrothermal environments on the Mid-Atlantic Ridge).

In collaboration with Dr. Myriam Sibuet from IFREMER, France we have been examining the diversity and distribution of symbiotic bacteria in a mussel from a newly discovered cold seep on the East Atlantic margin. This study is the first to examine the sulfide-oxidizing bacteria of mussels from seeps and shows that these are phylogenetically distinct from the thiotrophic symbionts of mussels from vents (Dupperon et al. 2005).

Black Smoker from the Logatchev vent field on the Mid-Atlantic Ridge (MAR).
Source: MARUM_Forschungszentrum Ozeanränder, Universität Bremen.

Niculina Musat, Caroline Verna

Skeleton of a Grey Whale six years after its death. Photo by Craig Smith.

Whale falls

The skeletal remains of large whales are home to a unique genus of gutless polychaete worms called Osedax. These worms harbor heterotrophic bacteria that degrade lipids in whale bones to provide their host with nutrition.


Nematodes

Sulfur-oxidizing bacteria form symbioses with two unrelated groups of nematode worms: gutless nematodes harbor endosymbionts while gut-bearing nematodes are covered with episymbiotic bacteria. Surprisingly, these symbionts are very closely related despite the large phylogenetic distance between the hosts and the very different morphology of these
symbioses.