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Mixture of new sulfated steroids functions as a migratory pheromone in the sea lamprey

Abstract

The sea lamprey is an ancient, parasitic fish that invaded the Great Lakes a century ago, where it triggered the collapse of many fisheries1. Like many fishes, this species relies on chemical cues to mediate key aspects of its life, including migration and reproduction2,3. Here we report the discovery of a multicomponent steroidal pheromone that is released by stream-dwelling larval lamprey and guides adults to spawning streams. We isolated three compounds with pheromonal activity (in submilligram quantities from 8,000 l of larval holding water) and deduced their structures. The most important compound contains an unprecedented 1-(3-aminopropyl)pyrrolidin-2-one subunit and is related to squalamine, an antibiotic produced by sharks4. We verified its structure by chemical synthesis; it attracts adult lamprey at very low (subpicomolar) concentrations. The second component is another new sulfated steroid and the third is petromyzonol sulfate, a known lamprey-specific bile acid derivative. This mixture is the first migratory pheromone identified in a vertebrate and is being investigated for use in lamprey control.

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Figure 1: Biological activity of fractions of larval sea lamprey holding waters.
Figure 2: Structures 13 and biological activities of the three principal components of the sea lamprey migratory pheromone.
Figure 3: 1H NMR spectral data used to determine the structures of PADS (1) and PSDS (2).
Figure 4: Behavioral preferences of migratory sea lampreys offered the choice of whole larval extract versus varying amounts of purified PADS in a laboratory maze.

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Acknowledgements

We thank the staffs of the Hammond Bay Biological Station, Ludington Biological Station, Marquette Biological Station and Sea Lamprey Control Centre at Sault Ste. Marie for collecting the sea lamprey. NMR instrumentation was acquired with funds from the US National Science Foundation (BIR-961477), the University of Minnesota Medical School and the Minnesota Medical Foundation. Access to MS instrumentation was provided through the courtesy of the University of Minnesota Mass Spectrometry Consortium for the Life Sciences. This research was supported by the Great Lakes Fishery Commission (P.W.S. and T.R.H.), the Minnesota Agricultural Experiment Station (P.W.S.) and the US National Institutes of Health (T.R.H., GM65597).

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Correspondence to Peter W Sorensen or Thomas R Hoye.

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Supplementary information

Supplementary Fig. 1

1H NMR comparison spectra (in CD3OD at 500 MHz) for various samples of natural and synthetic PADS. (PDF 1867 kb)

Supplementary Fig. 2

Map of the Ocqueoc River plume (a major lamprey spawning stream which enters Lake Huron) on May 1, 2002 showing the track of an acoustically tagged sea lamprey that approached the river. (PDF 66 kb)

Supplementary Methods (PDF 765 kb)

Supplementary Discussion (PDF 128 kb)

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Sorensen, P., Fine, J., Dvornikovs, V. et al. Mixture of new sulfated steroids functions as a migratory pheromone in the sea lamprey. Nat Chem Biol 1, 324–328 (2005). https://doi.org/10.1038/nchembio739

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