Transmission of obligate bacterial symbionts between generations is vital for the survival of the host. Although the larvae of certain hydrothermal vent tubeworms (Vestimentifera, Siboglinidae) are symbiont-free and possess a transient digestive system, these structures are lost during development, resulting in adult animals that are nutritionally dependent on their bacterial symbionts. Thus, each generation of tubeworms must be newly colonized with its specific symbiont. Here we present a model for tubeworm symbiont acquisition and the development of the symbiont-housing organ, the trophosome. Our data indicate that the bacterial symbionts colonize the developing tube of the settled larvae and enter the host through the skin, a process that continues through the early juvenile stages during which the trophosome is established from mesodermal tissue. In later juvenile stages we observed massive apoptosis of host epidermis, muscles and undifferentiated mesodermal tissue, which was coincident with the cessation of the colonization process. Characterizing the symbiont transmission process in this finely tuned mutualistic symbiosis provides another model of symbiont acquisition and additional insights into underlying mechanisms common to both pathogenic infections and beneficial host-symbiont interactions.
Zoothamnium niveum is a giant, colonial marine ciliate from sulfide-rich habitats obligatorily covered with chemoautotrophic, sulfide-oxidizing bacteria which appear as coccoid rods and rods with a series of intermediate shapes. Comparative 16S rRNA gene sequence analysis and fluorescence in situ hybridization showed that the ectosymbiont of Z. niveum belongs to only one pleomorphic phylotype. The Z. niveum ectosymbiont is only moderately related to previously identified groups of thiotrophic symbionts within the Gammaproteobacteria, and shows highest 16S rRNA sequence similarity with the free-living sulfur-oxidizing bacterial strain ODIII6 from shallowwater hydrothermal vents of the Mediterranean Sea (94.5%) and an endosymbiont from a deep-sea hydrothermal vent gastropod of the Indian Ocean Ridge (93.1%). A replacement of this specific ectosymbiont by a variety of other bacteria was observed only for senescent basal parts of the host colonies. The taxonomic status "Candidatus Thiobios zoothamnicoli" is proposed for the ectosymbiont of Z. niveum based on its ultrastructure, its 16S rRNA gene, the intergenic spacer region, and its partial 23S rRNA gene sequence.
Recent evidence suggests that deep-sea vestimentiferan tube worms acquire their endosymbiotic bacteria from the environment each generation; thus, free-living symbionts should exist. Here, free-living tube worm symbiont phylotypes were detected in vent seawater and in biofilms at multiple deep-sea vent habitats by PCR amplification, DNA sequence analysis, and fluorescence in situ hybridization. These findings support environmental transmission as a means of symbiont acquisition for deep-sea tube worms.
Evolutionary theory predicts potential shifts between cooperative and uncooperative behaviour under fluctuating environmental conditions. This leads to unstable benefits to the partners and restricts the evolution of dependence. High dependence is usually found in those hosts in which vertically transmitted symbionts provide nutrients reliably. Here we study host dependence in the marine, giant colonial ciliate Zoothamnium niveum and its vertically transmitted, nutritional, thiotrophic symbiont from an unstable environment of degrading wood. Previously, we have shown that sulphidic conditions lead to high host fitness and oxic conditions to low fitness, but the fate of the symbiont has not been studied. We combine several experimental approaches to provide evidence for a sulphide-tolerant host with striking polyphenism involving two discrete morphs, a symbiotic and an aposymbiotic one. The two differ significantly in colony growth form and fitness. This polyphenism is triggered by chemical conditions and elicited by the symbiont’s presence on the dispersing swarmer. We provide evidence of a single aposymbiotic morph found in nature. We propose that despite a high fitness loss when aposymbiotic, the ciliate has retained a facultative life style and may use the option to live without its symbiont to overcome spatial and temporal shortage of sulphide in nature.
The marine Stilbonematinae (Nematoda) are known for their highly specific mutualistic association with thiotrophic ectosymbiotic bacteria. The mechanism mediating recognition and binding between symbionts and host was studied in 5 host species. When incubated with D-mannose and L-rhamnose the symbionts detached in 2 species, Laxus cosmopolitus and L. oneistus, most likely due to competitive interactions with sugars involved in the binding mechanism; 3 other species, Stilbonema maium, Eubostrichus topiarius and E. dianae, did not lose their bacteria during any tested sugar incubations. Incubations with lectins binding specifically to D-glucose/D-mannose (ConA, concanavalin agglutinin) and to D-mannose (NPA, Narcissus pseudonarcissus agglutinin) respectively, both in vivo and on ultrathin sections, confirmed that accessible D-mannose is located on the symbionts of L. cosmopolitus, but not on the host's surface. Our results showed an involvement of D-mannose and L-rhamnose residues of the bacterial surface in the attachment mechanism. We hypothesize that the recognition and binding of the environmentally transmitted symbionts in the 2 Laxus species, which harbor only 1 phylotype of symbiotic γ-proteobacterium each, is most probably mediated through a yet unknown mannose/rhamnose-specific lectin of host origin.
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