Discovery and characterization of natural products that act as pheromones in fish

Abstract

Covering: up to 2018 Fish use a diverse collection of molecules to communicate with conspecifics. Since Karlson and Lüscher termed these molecules 'pheromones', chemists and biologists have joined efforts to characterize their structures and functions. In particular, the understanding of insect pheromones developed at a rapid pace, set, in part, by the use of bioassay-guided fractionation and natural product chemistry. Research on vertebrate pheromones, however, has progressed more slowly. Initially, biologists characterized fish pheromones by screening commercially available compounds suspected to act as pheromones based upon their physiological function. Such biology-driven screening has proven a productive approach to studying pheromones in fish. However, the many functions of fish pheromones and diverse metabolites that fish release make predicting pheromone identity difficult and necessitate approaches led by chemistry. Indeed, the few cases in which pheromone identification was led by natural product chemistry indicated novel or otherwise unpredicted compounds act as pheromones. Here, we provide a brief review of the approaches to identifying pheromones, placing particular emphasis on the promise of using natural product chemistry together with assays of biological activity. Several case studies illustrate bioassay-guided fractionation as an approach to pheromone identification in fish and the unexpected diversity of pheromone structures discovered by natural product chemistry. With recent advances in natural product chemistry, bioassay-guided fractionation is likely to unveil an even broader collection of pheromone structures and enable research that spans across disciplines.

Intra- and Interspecific Variation in Production of Bile Acids That Act as Sex Pheromones in Lampreys

“…Notably, the intra-and interspecific patterns differed for individual compounds, supporting previous observations that male odor is composed of multiple components with different functions (Johnson et al 2012). Although most of the measured bile acids are either pheromones or precursors for P. marinus (Brant et al 2013;Li et al 2018b), our results should be interpreted bearing in mind uncertainties regarding their specific functions across species. Regardless, our results indicate distinct evolutionary patterns for male versus larval bile acids.…”

“…The compounds 3-keto petromyzonol sulfate (3kPZS), petromyzonol sulfate (PZS), petro-myzonamine monosulfate (PAMS), petromyzonamine disulfate (PADS), petromyzosterol disulfate (PSDS), 3-keto petromyzonol (3kPZ), petromyzonol (PZ), and 3-keto allocholic acid (3kACA) were quantified. All of these compounds are either known pheromones or suspected pheromone precursors in P. marinus (Li et al 2018b). Concentration data were standardized by the subsample mass.…”

“…Although liver bile acids are not direct measures of pheromone signals, they allow useful comparisons despite the lack of specific information on pheromone identity in most lampreys. Furthermore, we reasoned that the bile acids produced in the liver are important sexual traits because (1) the liver (which synthesizes bile acids) is essentially the pheromone gland of lamprey and a major determinant of pheromone release (Buchinger et al 2017a) and (2) known liver bile acids are either sex pheromones or pheromone precursors for P. marinus (Li et al 2018b).…”

Aggregation Pheromone for an Invasive Mussel Consists of a Precise Combination of Three Common Purines

“…As Ado, Ino, and Hyp are common metabolites found in aquatic environments (Cunliffe, 2015), we wondered how M. sallei larvae can distinguish conspecific adult-derived purine signals from background levels. The use of a blend of pheromone components that act synergistically has also been reported in insects (Meier et al., 2016), although there are few published examples for marine organisms (Li et al., 2018). Usually the ratio of the pheromone components is highly species specific in insects, allowing effective communication among related sympatric species (Symonds and Elgar, 2008).…”

Bile acid production is life-stage and sex dependent and affected by primer pheromones in the sea lamprey

“…1 ) ( Hagey et al, 2010 ; Haslewood and Tökes, 1969 ; Li et al, 2002 , 2017a , 2018c ; Yun et al, 2003 ). The diversity of sea lamprey bile salts mostly come from the saturation status of the carbon bond at the A/B ring junction, the substitution of functional groups (carboxyl/hydroxyl/keto/sulfate), and the conjugations at 3, 7, 12 and 24 carbon positions ( Li et al, 2018b ). Known sea lamprey bile salts can be classified into three groups including: (1) C 27 bile salts: petromyzonamine disulfate (PADS) and petromyzonsterol disulfate (PSDS); (2) C 24 bile salts with multiple double bonds: 3,12-diketo-4,6-petromyzonene-24-sulfate (dkPES) and several bile salt-like dienones; and (3) a group of structurally related C 24 bile salts: 3kPZS and its presumptive precursors petromyzonol sulfate (PZS), petromyzonol (PZ), 3-keto petromyzonol (3kPZ), allocholic acid (ACA) and 3kACA ( Fig.…”