.2018 Aug 10;361(6402):591-594.

doi: 10.1126/science.aap7714.

Ancient convergent losses ofParaoxonase 1 yield potential risks for modern marine mammals

Wynn K Meyer¹, Jerrica Jamison², Rebecca Richter³, Stacy E Woods⁴, Raghavendran Partha¹, Amanda Kowalczyk¹, Charles Kronk², Maria Chikina¹, Robert K Bonde⁵, Daniel E Crocker⁶, Joseph Gaspard⁷, Janet M Lanyon⁸, Judit Marsillach³, Clement E Furlong^{3 9}, Nathan L Clark^{10 11}

Affiliations

¹ Department of Computational and Systems Biology, University of Pittsburgh, Pittsburgh, PA, USA.
² Dietrich School of Arts and Sciences, University of Pittsburgh, Pittsburgh, PA, USA.
³ Division of Medical Genetics, Department of Medicine, University of Washington, Seattle, WA, USA.
⁴ Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD, USA.
⁵ Wetland and Aquatic Research Center, U.S. Geological Survey, Gainesville, FL, USA.
⁶ Department of Biology, Sonoma State University, Rohnert Park, CA, USA.
⁷ Pittsburgh Zoo and PPG Aquarium, Pittsburgh, PA, USA.
⁸ School of Biological Sciences, The University of Queensland, St. Lucia, QLD 4072, Australia.
⁹ Department of Genome Sciences, University of Washington, Seattle, WA, USA.
¹⁰ Department of Computational and Systems Biology, University of Pittsburgh, Pittsburgh, PA, USA. nclark@pitt.edu.
¹¹ Pittsburgh Center for Evolutionary Biology and Medicine, University of Pittsburgh, Pittsburgh, PA, USA.

PMID:30093596
PMCID: PMC6317340
DOI: 10.1126/science.aap7714

Ancient convergent losses ofParaoxonase 1 yield potential risks for modern marine mammals

Wynn K Meyer et al. Science.2018.

.2018 Aug 10;361(6402):591-594.

doi: 10.1126/science.aap7714.

Authors

Affiliations

¹ Department of Computational and Systems Biology, University of Pittsburgh, Pittsburgh, PA, USA.
² Dietrich School of Arts and Sciences, University of Pittsburgh, Pittsburgh, PA, USA.
³ Division of Medical Genetics, Department of Medicine, University of Washington, Seattle, WA, USA.
⁴ Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD, USA.
⁵ Wetland and Aquatic Research Center, U.S. Geological Survey, Gainesville, FL, USA.
⁶ Department of Biology, Sonoma State University, Rohnert Park, CA, USA.
⁷ Pittsburgh Zoo and PPG Aquarium, Pittsburgh, PA, USA.
⁸ School of Biological Sciences, The University of Queensland, St. Lucia, QLD 4072, Australia.
⁹ Department of Genome Sciences, University of Washington, Seattle, WA, USA.
¹⁰ Department of Computational and Systems Biology, University of Pittsburgh, Pittsburgh, PA, USA. nclark@pitt.edu.
¹¹ Pittsburgh Center for Evolutionary Biology and Medicine, University of Pittsburgh, Pittsburgh, PA, USA.

PMID:30093596
PMCID: PMC6317340
DOI: 10.1126/science.aap7714

Abstract

Mammals diversified by colonizing drastically different environments, with each transition yielding numerous molecular changes, including losses of protein function. Though not initially deleterious, these losses could subsequently carry deleterious pleiotropic consequences. We have used phylogenetic methods to identify convergent functional losses across independent marine mammal lineages. In one extreme case,Paraoxonase 1 (PON1) accrued lesions in all marine lineages, while remaining intact in all terrestrial mammals. These lesions coincide with PON1 enzymatic activity loss in marine species' blood plasma. This convergent loss is likely explained by parallel shifts in marine ancestors' lipid metabolism and/or bloodstream oxidative environment affecting PON1's role in fatty acid oxidation. PON1 loss also eliminates marine mammals' main defense against neurotoxicity from specific man-made organophosphorus compounds, implying potential risks in modern environments.

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Conflict of interest statement

Competing interests: The authors declare no competing financial interests.

Figures

**Fig. 1.. PON1 functions and evolutionary history.**
Illustration of PON1’s proposed roles in(A) preventing oxidative damage to low- and high-density lipoproteins (14, 15) and(B) detoxifying the oxon byproduct/metabolite of a common organophosphorus pesticide, chlorpyrifos (25).(C) Evolutionary rate ofPON1 coding sequence across the phylogeny of 62 eutherian mammals. Branch lengths representd_N, and colors representd_N/d_S (see color legend).d_N/d_S values greater than 1.2 were set to 1.2. Blue: marine species. ψ: genetic lesion(s) present.

**Fig. 2.. Blood plasma enzymatic activity against two organophosphate-derived substrates.**
Points represent rates of hydrolysis of chlorpyrifos oxon (left) or diazoxon (right) in μmol/min/mL for plasma from marine and semi-aquatic species (in blue) and terrestrial outgroups. Values for sheep, goat, and rat are from Furlong et al. (33), who performed assays under the same experimental conditions as in this study. Control assays of alkaline phosphatase activity show samples were not degraded (Fig. S3).

**Fig. 3.. Manatee and adjacency of its habitat to agricultural land use.**
Left: Florida manatee (photo by Robert K. Bonde, 2006). Center: Manatee protection zones and agricultural land in Florida. Right: Manatee protection zones, waterways, and agricultural land in Brevard County.

See this image and copyright information in PMC

Comment in

Pollution threatens toothed whales.
Sonne C, Jepson PD, Desforges JP, Alstrup AKO, Olsen MT, Eulaers I, Hansen M, Letcher RJ, McKinney MA, Dietz R.Sonne C, et al.Science. 2018 Sep 21;361(6408):1208. doi: 10.1126/science.aav2403.Science. 2018.PMID:30237348No abstract available.

References

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Ancient convergent losses ofParaoxonase 1 yield potential risks for modern marine mammals

Affiliations

Ancient convergent losses ofParaoxonase 1 yield potential risks for modern marine mammals

Authors

Affiliations

Abstract

Conflict of interest statement

Figures

Comment in

References

Publication types

MeSH terms

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Grants and funding

LinkOut - more resources

Full Text Sources

Other Literature Sources

Miscellaneous