Morphology of the Symbiosis

In the first two descriptions of gutless oligochaetes, namely Inanidrilus albidus (albus = Latin: white) and I. leukodermatus (leukos = Greek: white), the intensive white color of the worms, now known to be common to all gutless oligochaetes, was mentioned but not further investigated (Fig. 4a) (Jamieson 1977; Giere 1979). This white coloring comes from the refraction of light by the symbiotic sulfur-oxidizing bacteria just below the cuticle of the worm that are filled with sulfur and the storage compound polyhydroxybutyric acid (PHB). The white color of the worms distinguishes them from other marine oligochaetes, making their identification in the field as symbiont-bearing worms easy, although only in live specimens (when preserved in alcohol or formaldehyde the white color is lost).

In all gutless oligochaetes the morphology of the symbiosis is remarkably similar. The worms have no mouth, gut, or anus, and unique among all gutless worms, they are the only host group that completely lack nephridia, excretory organs used to remove nitrogenous waste compounds and for osmoregulation. The symbiotic bacteria occur in a multicellular layer just below the thin cuticle of the worms, called the symbiotic region (Fig. 1). Calculations based on visual examinations of transmission electron micrographs indicate that an average sized worm harbors at least 106 bacterial cells, corresponding to roughly 25% of the worm's volume (Giere et al. 1995).

The bacteria in the apical part of the symbiotic region are extracellular, and sit between extensions of the epidermal cells. Diffusion experiments with fluorescein-labeled dextrane showed that the cuticle is permeable for substrates as large as 70 kDa as well as small negatively charged molecules such as fluorescein (J. Krieger and N. Dubilier, unpubl. data). This indicates that the symbiotic bacteria have free access to most substrates in the pore waters that the worms live in. In the basal area of the symbiotic region, the bacteria are regularly enclosed in vacuoles of the epidermal cells and appear to be in various stages of lysis. It is not known how important lysis of the bacteria is for the nutrition of the hosts, or whether "milking" of the bacteria, in which organic compounds are transferred to the host, may be the main mode of nutrient transfer. Lysis may also play a role in the regulation of bacterial growth (Giere et al. 1995).

Fig. 1. Transmission electron micrograph of symbiotic region below the cuticle (CU) of the gutless oligochaete O. crassitunicatus. Three bacterial morphotypes are clearly visible: large oval-shaped bacteria (LB) with sulfur and polyhydroxybutyric acid vesicles in the cytoplasm, small cocci- to rod-shaped bacteria (SB), and long, thin bacteria (SPI). In this host, the large bacteria have been identified as Gamma 1 symbionts, the small bacteria as delta proteobacterial symbionts, and the long thin bacteria as spirochetes (Fig. 2). The arrow shows a Gamma 1 symbiont in the final stages of division

Fig. 1. Transmission electron micrograph of symbiotic region below the cuticle (CU) of the gutless oligochaete O. crassitunicatus. Three bacterial morphotypes are clearly visible: large oval-shaped bacteria (LB) with sulfur and polyhydroxybutyric acid vesicles in the cytoplasm, small cocci- to rod-shaped bacteria (SB), and long, thin bacteria (SPI). In this host, the large bacteria have been identified as Gamma 1 symbionts, the small bacteria as delta proteobacterial symbionts, and the long thin bacteria as spirochetes (Fig. 2). The arrow shows a Gamma 1 symbiont in the final stages of division

Was this article helpful?

0 0

Post a comment