Responses of round goby (Neogobius melanostomus) olfactory epithelium to steroids released by reproductive males

Abstract

The wild perciform teleost Neogobius melanostomus (the round goby) originated from the Ponto-Caspian region and is now a highly successful invasive species in the Laurentian Great Lakes. Males may attract females into their nests for spawning by releasing reproductive pheromones, and it has been previously shown that reproductive males synthesize and release the 5β-reduced and 3α-hydroxyl steroids 3α-hydroxy-5β-androstane-11,17-dione (11-oxo-etiocholanolone; 11-O-ETIO) and 3α-hydroxy-5β-androstane-11,17-dione 3-sulfate (11-oxo-etiocholanolone-3-sulfate; 11-O-ETIO-3-s) and 3α,17β-dihydroxy-5β-androstan-11-one 17-sulfate. In this study, we investigated properties of these released steroids by recording field potential responses from the olfactory epithelium (electro-olfactogram, EOG). The steroid 3α,17β-dihydroxy-5β-androstan-11-one 17-sulfate did not elicit olfactory responses while both 11-O-ETIO and 11-O-ETIO-3-s stimulated olfactory field potentials in the round goby, but not in the goldfish. Cross-adaptation analysis demonstrated that round gobies discriminated between11-O-ETIO and 11-O-ETIO-3-s (as well as etiocholanolone, ETIO) at the sensory level. Second messenger cascades depending on both cAMP and IP(3) were inferred for steroids from pharmacological inhibition studies, while the canonical teleost odors taurocholic acid (a bile acid) and L: -alanine (an amino acid) used only cAMP and IP(3), respectively. The round goby presents itself as an excellent species for the study of olfactory function of fish in the wild, given its possible use of these released steroids as pheromones.

Differential nickel-induced responses of olfactory sensory neuron populations in zebrafish

“…cOSNs and crypt cells have a cAMP-mediated olfactory signaling pathway, whereas mOSNs possess an IP3-based pathway. The response of specific classes of OSNs to specific odors can be determined by exploiting differences in these pathways (Hansen et al, 2003;Kolmakov et al, 2009;Laframboise and Zielinski, 2011;Michel et al, 2003;Rolen et al, 2003). For example, a histological technique has demonstrated the specific action of taurocholic acid on cOSNs (Bazáes and In the US EPA ECOTOX database (http://cfpub.epa.gov/ecotox/), the LC 50 for nickel chloride measured in adults and juveniles exposed for 48 h was > 10 mg L −1 .…”

Chemical cues for intraspecific chemical communication and interspecific interactions in aquatic environments: applications for fisheries and aquaculture

“…In the round goby Neogobius melanostomus, reproductive males probably secrete female-attracting pheromones. The candidates for the active substances are ETIO, ETIO-glucosiduronate, 11-oxo-ETIO, and 11-oxo-ETIO-3-sulfate, as suggested by electrophysiological recordings from the olfactory epithelium of reproductive females (Murphy et al 2001;Laframboise and Zielinski 2011), behavioral observations of responses to goby holding water (Belanger et al 2004;Corkum et al 2008), and biochemical analyses of the holding water (Arbuckle et al 2005;Katare et al 2011). Additionally, the round goby shows sexually dimorphic responses to some steroids, with males showing ventilatory behavior to estrone, E 2 -3β-glucuronide, and ETIO and females responding only to ETIO (Murphy et al 2001).…”

Sensory cutaneous papillae in the sea lamprey (Petromyzon marinus L.): II. Ontogeny and immunocytochemical characterization of solitary chemosensory cells

“…Chemosensory transduction through PLC has been identified in olfactory sensory neurons in squid ( L . brevis : Mobley et al, ), teleosts (zebrafish, Yoshida et al, ; catfish, Ictalurus punctatus : Hansen et al, ; round goby, Neogobius melanostomus Laframboise & Zielinski, ), in mammalian vomeronasal sensory neurons (Hegg, Jia, Chick, Restrepo, & Hansen, ; Szebenyi et al, ) and a subset of olfactory sensory neurons (Lin, Margolskee, Donnert, Hell, & Restrepo, ). In mammalian taste cells, PLC mediates the release of calcium from intracellular stores through the opening cellular channels (Kinnamon, ).…”