Abstract
BackgroundIn vertebrates, bile salts are primarily synthesized in the liver and secreted into the intestine where they aid in absorption of dietary fats. Small amounts of bile salts that are not reabsorbed into enterohepatic circulation are excreted with waste. In sexually mature male sea lamprey (Petromyzon marinus L.) a bile salt is released in large amounts across gill epithelia into water where it functions as a pheromone. We postulate that the release of this pheromone is associated with a dramatic increase in its biosynthesis and transport to the gills upon sexual maturation.ResultsWe show an 8000-fold increase in transcription of cyp7a1, a three-fold increase in transcription of cyp27a1, and a six-fold increase in transcription of cyp8b1 in the liver of mature male sea lamprey over immature male adults. LC–MS/MS data on tissue-specific distribution and release rates of bile salts from mature males show a high concentration of petromyzonol sulfate (PZS) in the liver and gills of mature males. 3-keto petromyzonol sulfate (3kPZS, known as a male sex pheromone) is the primary compound released from gills, suggesting a conversion of PZS to 3kPZS in the gill epithelium. The PZS to 3kPZS conversion is supported by greater expression of hsd3b7 in gill epithelium. High expression of sult2b1 and sult2a1 in gill epithelia of mature males, and tissue-specific expression of bile salt transporters such as bsep, slc10a1, and slc10a2, suggest additional sulfation and transport of bile salts that are dependent upon maturation state.ConclusionsThis report presents a rare example where specific genes associated with biosynthesis and release of a sexual pheromone are dramatically upregulated upon sexual maturation in a vertebrate. We provide a well characterized example of a complex mechanism of bile salt biosynthesis and excretion that has likely evolved for an additional function of bile salts as a mating pheromone.
Highlights
In vertebrates, bile salts are primarily synthesized in the liver and secreted into the intestine where they aid in absorption of dietary fats
Mean concentration of petromyzonol sulfate (PZS) was highest in liver tissues of SM at 113401.1 ± 19784.8 ng/g, which was higher than a mean plasma concentration of 11678.6 ± 2089.7 ng/l-plasma) and mean gill concentration of 5604.5 ± 1028.4 ng/g, respectively (Tukey’s HSD, α = 0.05)
Mean concentrations of bile salts differed across tissues and plasma for 3-keto petromyzonol sulfate (3kPZS) (F2, 32 = 4.26, P = 0.023), 3-keto allocholic acid (3kACA) (F2, 27 = 11.11, P < 0.001), and petromyzonamine disulfate (PADS) (F2, 32 = 4.16, P = 0.025); concentrations of allocholic acid (ACA) did not differ across tissues and plasma (F2, 32 = 0.88, P = 0.424; Figure 2)
Summary
Bile salts are primarily synthesized in the liver and secreted into the intestine where they aid in absorption of dietary fats. In sexually mature male sea lamprey (Petromyzon marinus L.) a bile salt is released in large amounts across gill epithelia into water where it functions as a pheromone. Small amounts (roughly 5%) of these bile salts that are not returned to the liver via enterohepatic circulation are excreted from the body with waste [1,2,3]. Male sea lamprey have been shown to secrete bile salts and steroids through gill epithelia after sexual maturation [9]. Three of these compounds have been identified as 3-keto allocholic acid (3kACA), 3-keto petromyzonol sulfate (3kPZS), and petromyzestrosterol [5,10,11]. Three of these compounds have been identified as 3-keto allocholic acid (3kACA), 3-keto petromyzonol sulfate (3kPZS), and petromyzestrosterol [5,10,11]. 3kPZS has been shown to attract sexually mature females to the odorant source in streams, acting as a sex pheromone [5,6,12]
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