Stable associations of more than one species of symbiont within a single host cell or tissue are assumed to be rare in metazoans because competition for space and resources between symbionts can be detrimental to the host. In animals with multiple endosymbionts, such as mussels from deep-sea hydrothermal vents and reef-building corals, the costs of competition between the symbionts are outweighed by the ecological and physiological flexibility gained by the hosts. A further option for the coexistence of multiple symbionts within a host is if these benefit directly from one another, but such symbioses have not been previously described. Here we show that in the gutless marine oligochaete Olavius algarvensis, endosymbiotic sulphate-reducing bacteria produce sulphide that can serve as an energy source for sulphide-oxidizing symbionts of the host. Thus, these symbionts do not compete for resources but rather share a mutalistic relationship with each other in an endosymbiotic sulphur cycle, in addition to their symbiotic relationship with the oligochaete host.
Abstract. The gutless marine oligochaete, Olavius crassitunicatus
finogenova 1986 (Tubificidae), from suboxic to sulfidic sediments off Peru, consistently harbored 3 structurally distinct types of extracellular bacterial symbionts. Large, oval bacteria were labeled immunocytochemically, proving their nature as autotrophs. Spectroscopical analysis documented storage of sulfur in this numerically dominant morphotype. Small, rod‐shaped bacteria attained a more peripheral position adjacent to the cuticle. The third bacterial type was represented by long, filamentous forms which were often in close contact to the oval bacteria. With their curved or undulate cells, these filiform bacteria resembled spirochetes. They were clearly distinguishable and consistently found in all investigated host specimens.
While molecular analyses could not be performed, structural and immunocytochemical evidence indicated that the oval bacteria seemed equivalent to the γ‐proteobacteria in related gutless oligochaetes. On the basis of morphological similarity and indications from closely related symbiotic tubificids, the possible relationship of the two other morphoptypes must remain unsolved and needs further molecular analysis. The three bacterial morphotypes live in a consistent, elaborate, and apparently obligate coexistence with a host that has completely reduced its digestive and excretory organs.
The blackening of tissues or mucus of benthic animals from sulphidic environments is a remarkable phenomenon whose ecological interpretation is disputed. In the Baltic clam Macoma balthica the mantle edge turned black after sulphide exposure owing to numerous precipitates in the extracellular matrix underneath the epidermal cells. In the apical parts of these cells, similar precipitates were found, albeit in lower abundance. Elemental analyses showed that copper (214.7 pg g-' ww [wet weight]) and sulphur (1328.6 pg g.' ww) were the main components, with iron (311.2 pg g-' ww) and zinc (112.7 pg g-' \W) in lower concentration. Apparently, these precipitates become phagocytosed by amoebocytes and concentrated in haemocytic granules. This is interpreted as a pathway of removal from the mantle edge. On the basis of calculated diffusion rates (DHS-= 1.9 X cm2 S-'). there is a sulphide influx of 61 nmol h-' into the body of M. balthica. Even under conservative assumptions, this would lead to the binding of all the copper present in about 30 min. It is concluded that the process of sulphide precipitation can represent a temporarily effective pathway attenuating sulphide toxification.
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