Three-dimensional reconstruction of the amphid sensilla in the microbial feeding nematode, Acrobeles complexus (Nematoda: Rhabditida)

Abstract

Amphid sensilla are the primary olfactory, chemoreceptive, and thermoreceptive organs in nematodes. Their function is well described for the model organism Caenorhabditis elegans, but it is not clear to what extent we can generalize these findings to distantly related nematodes of medical, economic, and agricultural importance. Current detailed descriptions of anatomy and sensory function are limited to nematodes that recent molecular phylogenies would place in the same taxonomic family, the Rhabditidae. Using serial thin-section transmission electron microscopy, we reconstructed the anatomy of the amphid sensilla in the more distantly related nematode, Acrobeles complexus (Cephalobidae). Amphid structure is broadly conserved in number and arrangement of cells. Details of cell anatomy differ, particularly for the sensory neurite termini. We identify an additional sensory neuron not found in the amphid of C. elegans and propose homology with the C. elegans interneuron AUA. Hypotheses of homology for the remaining sensory neurons are also proposed based on comparisons between C. elegans, Strongyloides stercoralis, and Haemonchus contortus.

Figure 1

Transmission electron micrographs of an amphid in an adult female of Acrobeles complexus. A: The amphid posterior to the expansion of the sheath cell. The sensory dendrites ASA (a), ASB (b), ADC (c), AFD (d), ASE (e), ASF (f), ASG (g), ASH (h), ASI (i), ASJ (j), ASK (k), ASL (l), and ASM (m) are shown. Also indicated are the sheath cell (sh), socket cell (so), and the pharynx (ph). The labels for A apply to all other panels. B: The amphid posterior to the entrance of dendrites into the sensory channel formed by the sheath cell. Note coils of lamellar processes formed by the sheath cell (large black arrow) that wrap around the ASK dendritic process. Junctions with a distinct morphology (white arrow) occur between the sheath cell and the dendrite ASA. Microvilli branching off of the AFD dendrite are indicated (small black arrows). C: The belt of adherens junctions between adjacent amphid dendrites and the sheath cell, forming a single opening into the sensory channel. A bulbous extension of AFD extending into the sheath cell, with microvilli branching from this bulb. Note the granular appearance of the cytosol in the center of the bulb. D: One of two AFD cilia originating on the bulbous process (white arrow). E: The sensory channel of the amphid, showing the transition zones of most sensory amphid dendrites. Note the two cilia of ADC. F: Transition between the sheath and socket cells, showing adherens junctions between the two cells. Scale bar = 1 μm (applies to all).

Figure 2

Model of the amphid of Acrobeles complexus. In the rendering on the left the left amphid is viewed from the left side of the animal, and in the rendering on the right the same amphid is viewed from the opposite side. The amphid socket cell (so) is rendered transparent red and the sheath cell (sh) is rendered transparent green. For reference, on the left side a portion of the HYP-E epidermal syncytium (he) is rendered transparent gray and a portion of the HYP-D epidermal syncytium (hd) is rendered solid yellow, showing where they form the amphid opening to the outside environment. Behind the amphid, a portion of the pharynx is rendered in gray. A belt of adherens junctions at the point where dendritic processes enter the sensory channel (aj) is indicated by a red and green striped texture. A small accessory process of ASF (black arrows) terminates in a pocket of the sheath cell, rather than in the sensory channel of the amphid. The bulbous swelling of ASE (white arrow) rests between the two cilia of ADC. Black lines with letters indicate the approximate region of the amphid from which the images in Figure 1 were obtained.

Figure 3

Model of the morphology of individual amphid dendrites. Adherens junctions at the opening in the sheath cell to the sensory channel are indicated with a striped green and red texture. The positions of transition zones (x) are indicated for all dendrites. The perspective is identical to the right-hand side of Figure 2. A: The neurites ASF (f) and ADF (d). Note the small projection (black arrow) near the transition zone. B: The neurites ASG (g) and ASH (h). C: The neurites ASK (k) and ASJ (j). D: The neurites ASB (b) and ASE (e). The bulbous swelling (black arrow) of ASE rests between the two cilia of ADC. E: The neurites ASM (m) and ADC (c). The cilium of ADC that is further from the pharynx has a more robust swelling near the transition zone (black arrow). F: The neurites ASI (i), ASL (l), and ASA (a).

Figure 4

Transmission electron micrographs of an amphid in an adult female of Acrobeles complexus. A: Anterior region of amphid sensory channel showing the self-junction (black arrow) of the socket cell (so). B: Transition zone of an amphid sensory cilium. C: Distinctive cell membranes (black arrow) of the AFD microvilli (d) shown adjacent to the sheath cell (sh) membrane. D: Amphid in the region of the AFD (d) microvilli. The amphid sensory channel (sc) in this individual is filled with a secretion from the sheath cell. E: Longitudinal image through the amphid finger cell (d) showing two sensory cilia (black arrows) and granular material in the cytosol of the finger cell bulb (x). F: The same individual as in D, shown in the anterior region of the sensory channel (sc) where large secretory vesicles (v) merge with the sensory channel. G: Lamellar projections (black arrow) of the sheath cell (sh) wrapping around the sensory dendrite ASK (k) just posterior to where it enters the sheath cell sensory channel. Note the numerous vesicles (v) in this region. Scale bar = 1 μm. H: Longitudinal section through the amphid. The partially formed cilium of ASA (a) is shown terminating adjacent to the AFD cell (d). The rootlet is indicated (black arrow). Note the greater surface area of adherens junctions (white arrows) along ASA as compared to the other sensory dendrites. Scale bars = 0.5 μm in A; 0.25 μm in B,C; 1 μm in D–H.

Figure 5

Transmission electron micrograph of an amphid in the J1 of Acrobeles complexus. The sensory dendrites ASB (b), ADC (c), AFD (d), ASE (e), ASF (f), ASG (g), ASH (h), ASI (i), ASJ (j), ASK (k), ASL (l), and ASM (m) are shown at the entrance to the sheath cell sensory channel. Also indicated are the sheath cell (sh), socket cell (so), and the pharynx (ph). The AFD cell is surrounded by microvilli, three of them are indicated (black arrows). Scale bar = 0.5 μm.

Figure 6

Arrangement of amphid dendrites at the posterior entrance into the sheath cell. The bottom row is from J1 while the top row is from the oldest life stage for which there is data. The right side of each image is adjacent to the pharynx, and the top is dorsal. Letters correspond to the name of dendrites according to current nomenclature. Cells that are colored the same represent stronger hypotheses of homology that are based on multiple types of similarity, with dendrites of the same color being presumably homologous. Types of similarity considered include number of cilia, results of laser ablation studies that imply related function, and relative position at the proximal end of the amphid. Data for Strongyloides stercoralis are redrawn from Ashton et al. (1995). Data for Haemonchus contortus are redrawn from Li et al. (2000a, . Data for C. elegans are redrawn from Ward et al. (1975).