A comparative analysis of putative oxygen-sensing cells in the fish gill

Abstract

SUMMARYWe investigated the distribution of serotonin (5-HT)-containing neuroepithelial cells (NECs), the putative O 2 sensing cells, in the gills of four species of fish: trout (Oncorhynchus mykiss), goldfish (Carassius auratus), trairão (Hoplias lacerdae) and traira (Hoplias malabaricus) using immunohistochemical markers for 5-HT, synaptic vesicles and neural innervation. We found that all fish had a cluster of innervated, serotonergic NECs at the filament tips, but there were species-specific distributions of serotonincontaining NECs within the primary gill filaments. Trout gill filaments had a greater number of serotonin-containing NECs than both trairão and traira, whereas goldfish primary filaments had none. Serotonin-containing NECs in the secondary lamellae were most numerous in goldfish, present in trairão and traira, but absent in trout. Those found in the primary filament were generally associated with the efferent filamental artery. Innervated, serotonin-containing cells (NECs or Merkel-like cells) were also found in the gill rakers of trout and goldfish although vesicular serotonin was only found in the gill rakers of goldfish. These differences in serotonergic NEC distribution appear to reflect paracrine versus chemoreceptive roles related to hypoxia tolerance in the different fish species.

Characterisation of putative oxygen chemoreceptors in bowfin (Amia calva)

“…6A,C). These cells were similar in morphology and location to those previously described in the filaments of all other species of fish studied (Coolidge et al, 2008;Jonz et al, 2004;Regan et al, 2011;Saltys et al, 2006;Tzaneva and Perry, 2010). Additionally, Type I cells, just as in NECs in this same location in goldfish (Carassius auratus) and trout (O. mykiss), did not label with the HNK-1 antibody, suggesting they are either not derived from the neural crest, or more probably, not proliferative (Porteus et al, 2013), as some neural crest cells stop expressing HNK-1 once they differentiate (Metcalfe et al, 1990).…”

“…This was surprising because previous studies have shown that the reflex hypoxic bradycardia exhibited by this species is mediated exclusively by externally oriented receptors (McKenzie et al, 1991a;McKenzie et al, 1991b). It should be noted, however, that our study only examined the first gill arch and that elimination of the hypoxic bradycardia required denervation of all four gill arches, and NECs have been found in all four gill arches of all species studied to date (Coolidge et al, 2008;Jonz and Nurse, 2003;Zhang et al, 2011). Thus, it is possible that chemoreceptors exclusively oriented to sample water could be located on other gill arches of bowfin.…”

“…Thus, it is possible that chemoreceptors exclusively oriented to sample water could be located on other gill arches of bowfin. However, although other gill arches contain NECs, these NECs are generally found in the same locations and have similar distributions to those found in the first gill arch (Coolidge et al, 2008;Jonz and Nurse, 2003;Zhang et al, 2011). This conundrum remains to be resolved.…”

“…Type IV cells found in the lamellae have been described in most species of fish studied to date (Coolidge et al, 2008;Jonz et al, 2004;Saltys et al, 2006;Vulesevic et al, 2006), but not in trout or mangrove rivulus (Coolidge et al, 2008;Regan et al, 2011;Saltys et al, 2006). In other fish species, Type IV cells typically contain synaptic vesicles and are innervated.…”

“…For NECs to be oxygen chemoreceptors involved in a central reflex response to hypoxia they must be innervated in order for the information to be relayed to the central nervous system for processing, and they must release their neurotransmitters from vesicles into a synapse onto these nerves. A synaptic vesicle marker SV2 and a neuronal marker zn-12 have been previously used to identify NECs in fish and their nearby innervation (Coolidge et al, 2008;Jonz et al, 2004;Jonz and Nurse, 2003;Regan et al, 2011;Tzaneva and Perry, 2010). Additionally, glomus cells from the carotid bodies of birds and mammals are derived from the neural crest (Pearse et al, 1973).…”