Symbioses in shallow water sediments

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).

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.

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.

Paracatenula is a genus of small marine flatworms that live in the pore water of sands in warm temperate and tropical regions all around the globe. The worms have no mouth or gut and instead rely on intracellular chemosynthetic endosymbionts for nutrition. The bacteria are aerobe sulfur oxidizers, that need both oxygen and sulfide to generate the energy for carbon fixation and the rest of their metabolism. By migrating through the upper layers of the sand, the worm is the shuttle between the oxygenated layers in the top and the sulfidic layers 10–15 cm deep in the sand. The bacterial symbionts can make up to half of the total biomass of the worm and are housed in bacteriocytes that form the trophosome, the nutritive tissue.

The Paracatenula symbionts are so far the only known chemoautotrophic symbionts of the order Alphaproteobacteria. All other known chemoautotrophic and sulfur-oxidizing symbionts are either Gamma- or Epsilonproteobacteria. Their symbionts, named Candidatus Riegeria, have been vertically transmitted for over 500 million years ago. Such a long period of co-evolution suggests that Ca. Riegeria symbionts would show severe signatures of genome reduction and would only have a very limited set of metabolic functions. Just recently we could show that the symbiont of a mediterranean Paracatenula species has an unexpectedly versatile energy and storage metabolism despite its reduced genome. The Ca. Riegeria symbionts can fix carbon, store carbon in multiple soluble and non-soluble compounds and produce all necessary building blocks for cellular life, be it sugars, nucleotides, amino acids or vitamins. In contrast to other chemosynthetic symbioses, the Paracatenula host does not digest its symbionts for nutrient acquisition. Instead, the symbionts feed their host with outer-membrane vesicles (OMVs) that the symbionts secrete. With their high storage capabilities and the elegant ‘current’ like nutrition via OMVs, the symbionts form a bacterial battery for the highly integrated holobiont.