Short-term mercury exposure disrupts muscular and hepatic lipid metabolism in a migrant songbird
Bowler, D. E. et al. Mapping human pressures on biodiversity across the planet uncovers anthropogenic threat complexes. People Nat. 2, 380–394 (2020).Article
Google Scholar
Persson, L. et al. Outside the safe operating space of the planetary boundary for novel entities. Environ. Sci. Technol. https://doi.org/10.1021/acs.est.1c04158 (2022).Article
PubMed
PubMed Central
Google Scholar
United Nations Environment Programme (UNEP). 2019. Global Mercury Assessment 2018. UN Environment Programme, Chemicals and Health Branch Geneva, Switzerland. https://www.unep.org/resources/publication/global-mercury-assessment-2018Rimmer, C. C., Miller, E. K., McFarland, K. P., Taylor, R. J. & Faccio, S. D. Mercury bioaccumulation and trophic transfer in the terrestrial food web of a montane forest. Ecotoxicology 19, 697–709 (2010).CAS
PubMed
Article
Google Scholar
Cristol, D. A. et al. The movement of aquatic mercury through terrestrial food webs. Science 320, 335 (2008).ADS
CAS
PubMed
Article
Google Scholar
Evers, D. The effects of methylmercury on wildlife: A comprehensive review and approach for interpretation. Encycl. Anthropocene 5, 181–194 (2018).Article
Google Scholar
Whitney, M. C. & Cristol, D. A. Impacts of sublethal mercury exposure on birds: a detailed review. Rev. Environ. Contam. Toxicol. 244, 113–163 (2017).
Google Scholar
Seewagen, C. L. Threats of environmental mercury to birds: Knowledge gaps and priorities for future research. Bird Conserv. Int. 20, 112–123 (2010).Article
Google Scholar
Seewagen, C. L. The threat of global mercury pollution to bird migration: Potential mechanisms and current evidence. Ecotoxicology 29, 1254–1267 (2020).CAS
PubMed
Article
Google Scholar
Ma, Y., Branfireun, B. A., Hobson, K. A. & Guglielmo, C. G. Evidence of negative seasonal carry-over effects of breeding ground mercury exposure on survival of migratory songbirds. J. Avian Biol. 49, jav-01656 (2018).Article
Google Scholar
Newton, I. Can conditions experienced during migration limit the population levels of birds?. J. Ornithol. 147, 146–166 (2006).Article
Google Scholar
Klaassen, M., Hoye, B. J., Nolet, B. A. & Buttemer, W. A. Ecophysiology of avian migration in the face of current global hazards. Philos. Trans. R. Soc. B 367, 1719–1732 (2020).Article
Google Scholar
Zurell, D., Graham, C. H., Gallien, L., Thuiller, W. & Zimmermann, N. E. Long-distance migratory birds threatened by multiple independent risks from global change. Nat. Clim. Chang. 8, 992–996 (2018).ADS
PubMed
PubMed Central
Article
Google Scholar
Seewagen, C. L., Ma, Y., Morbey, Y. E. & Guglielmo, C. G. Stopover departure behavior and flight orientation of spring-migrant Yellow-rumped Warblers (Setophaga coronata) experimentally exposed to methylmercury. J. Ornithol. 160, 617–624 (2019).Article
Google Scholar
Seewagen, C. L. Blood mercury levels and the stopover refueling performance of a long-distance migratory songbird. Can. J. Zool. 91, 41–45 (2013).CAS
Article
Google Scholar
Adams, E. M., Williams, K. A., Olsen, B. J. & Evers, D. C. Mercury exposure in migrating songbirds: Correlations with physical condition. Ecotoxicology 29, 1240–1253 (2020).CAS
PubMed
Article
Google Scholar
Ma, Y., Perez, C. R., Branfireun, B. A. & Guglielmo, C. G. Dietary exposure to methylmercury affects flight endurance in a migratory songbird. Environ. Pollut. 234, 894–901 (2018).CAS
PubMed
Article
Google Scholar
Gerson, A. R., Cristol, D. A. & Seewagen, C. L. Environmentally relevant methylmercury exposure reduces the metabolic scope of a model songbird. Environ. Pollut. 246, 790–796 (2019).CAS
PubMed
Article
Google Scholar
Jenni, L. & Jenni-Eiermann, S. Fuel supply and metabolic constraints in migrating birds. J. Avian Biol. 29, 521–552 (1998).Article
Google Scholar
McWilliams, S. R., Guglielmo, C., Pierce, B. & Klaassen, M. Flying, fasting, and feeding in birds during migration: A nutritional and physiological ecology perspective. J. Avian Biol. 35, 377–393 (2004).Article
Google Scholar
Guglielmo, C. G. Move that fatty acid: Fuel selection and transport in migratory birds and bats. Integr. Comp. Biol. 50, 336–345 (2010).PubMed
Article
Google Scholar
Guglielmo, C. G. Obese super athletes: Fat-fueled migration in birds and bats. J. Exp. Biol. 221(Suppl_1), 165753 (2018).Article
Google Scholar
Kawakami, T. et al. Differential effects of cobalt and mercury on lipid metabolism in the white adipose tissue of high-fat diet-induced obesity mice. Toxicol. Appl. Pharmacol. 258, 32–42 (2012).CAS
PubMed
Article
Google Scholar
Yadetie, F. et al. Global transcriptome analysis of Atlantic cod (Gadus morhua) liver after in vivo methylmercury exposure suggests effects on energy metabolism pathways. Aquat. Toxicol. 126, 314–325 (2013).CAS
PubMed
Article
Google Scholar
Park, K. & Seo, E. Association between toenail mercury and metabolic syndrome is modified by selenium. Nutrients 8, 424 (2016).PubMed Central
Article
CAS
Google Scholar
Caito, S. W., Newell-Caito, J., Martell, M., Crawford, N. & Aschner, M. Methylmercury induces metabolic alterations in Caenorhabditis elegans: Role for C/EBP transcription factor. Toxicol. Sci. 174, 112–123 (2020).CAS
PubMed
Article
Google Scholar
Edmonds, S. T., O’Driscoll, N. J., Hillier, N. K., Atwood, J. L. & Evers, D. C. Factors regulating the bioavailability of methylmercury to breeding rusty blackbirds in northeastern wetlands. Environ. Pollut. 171, 148–154 (2012).CAS
PubMed
Article
Google Scholar
Rowse, L. M., Rodewald, A. D., Mažeika, S. & Sullivan, P. Pathways and consequences of contaminant flux to Acadian flycatchers (Empidonax virescens) in urbanizing landscapes of Ohio, USA. Sci. Total Environ. 485, 461–467 (2014).ADS
PubMed
Article
CAS
Google Scholar
Marsh, R. L. Catabolic enzyme activities in relation to premigratory fattening and muscle hypertrophy in the gray catbird (Dumetella carolinensis). J. Comp. Physiol. 141, 417–423 (1981).CAS
Article
Google Scholar
Guglielmo, C. G., Haunerland, N. H., Hochachka, P. W. & Williams, T. D. Seasonal dynamics of flight muscle fatty acid binding protein and catabolic enzymes in a migratory shorebird. Am. J. Physiol.-Regul. Integr. Comp. Physiol. 282(5), R1405–R1413 (2002).CAS
PubMed
Article
Google Scholar
Maillet, D. & Weber, J. M. Relationship between n-3 PUFA content and energy metabolism in the flight muscles of a migrating shorebird: Evidence for natural doping. J. Exp. Biol. 210, 413–420 (2007).CAS
PubMed
Article
Google Scholar
Weber, J. M. Metabolic fuels: Regulating fluxes to select mix. J. Exp. Biol. 214, 286–294 (2011).CAS
PubMed
Article
Google Scholar
Feige, J. N., Gelman, L., Michalik, L., Desvergne, B. & Wahli, W. From molecular action to physiological outputs: Peroxisome proliferator-activated receptors are nuclear receptors at the crossroads of key cellular functions. Prog. Lipid. Res. 45, 120–159 (2006).CAS
PubMed
Article
Google Scholar
Bensinger, S. J. & Tontonoz, P. Integration of metabolism and inflammation by lipid-activated nuclear receptors. Nature 454, 470–477. https://doi.org/10.1038/nature07202 (2008).ADS
CAS
Article
PubMed
Google Scholar
Ynalvez, R., Gutierrez, J. & Gonzalez-Cantu, H. Mini-review: Toxicity of mercury as a consequence of enzyme alteration. Biometals 29, 781–788 (2016).CAS
PubMed
Article
Google Scholar
Gerson, A. R. & Guglielmo, C. G. Energetics and metabolite profiles during early flight in American robins (Turdus Migratorius). J. Comp. Physiol. B. 183, 983–991 (2013).CAS
PubMed
Article
Google Scholar
Price, E. R., McFarlan, J. T. & Guglielmo, C. G. Preparing for migration? The effects of photoperiod and exercise on muscle oxidative enzymes, lipid transporters, and phospholipids in white-crowned sparrows. Physiol. Biochem. Zool. 83, 252–262 (2010).CAS
PubMed
Article
Google Scholar
Bradley, S. S., Dick, M. F., Guglielmo, C. G. & Timoshenko, A. V. Seasonal and flight-related variation of galectin expression in heart, liver and flight muscles of yellow-rumped warblers (Setophaga coronata). Glycoconj. J. 34, 603–611 (2017).CAS
PubMed
Article
Google Scholar
McFarlan, J. T., Bonen, A. & Guglielmo, C. G. Seasonal upregulation of fatty acid transporters in flight muscles of migratory white-throated sparrows (Zonotrichia albicollis). J. Exp. Biol. 212, 2934–2940 (2009).CAS
PubMed
Article
Google Scholar
Zhang, Y., King, M. O., Harmon, E., Eyster, K. & Swanson, D. L. Migration-induced variation of fatty acid transporters and cellular metabolic intensity in passerine birds. J. Comp. Physiol. B. 185, 797–810 (2015).CAS
PubMed
Article
Google Scholar
Dick, M. F. & Guglielmo, C. G. Dietary polyunsaturated fatty acids influence flight muscle oxidative capacity but not endurance flight performance in a migratory songbird. Am. J. Physiol.-Regul. Integr. Compar. Physiol. 316(4), R362–R375 (2019).CAS
Article
Google Scholar
Schmittgen, T. D. & Livak, K. J. Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3, 1101–1108 (2008).CAS
PubMed
Article
Google Scholar
Bittencourt, L. O. et al. Oxidative biochemistry disbalance and changes on proteomic profile in salivary glands of rats induced by chronic exposure to methylmercury. Oxid. Med. Cell. Longev. https://doi.org/10.1155/2017/5653291 (2017).Article
PubMed
PubMed Central
Google Scholar
Shi, Q., Sun, N., Kou, H., Wang, H. & Zhao, H. Chronic effects of mercury on Bufo gargarizans larvae: Thyroid disruption, liver damage, oxidative stress and lipid metabolism disorder. Ecotoxicol. Environ. Saf. 164, 500–509 (2018).CAS
PubMed
Article
Google Scholar
Nøstbakken, O. J. et al. Dietary methylmercury alters the proteome in Atlantic salmon (Salmo salar) kidney. Aquat. Toxicol. 108, 70–77 (2012).PubMed
Article
CAS
Google Scholar
Zink, E. M. Comparison of the mercury induced proteomes of Escherichia coli MG1655 with and without the NR1 plasmid. MSc thesis, Washington State University, Pullman, WA (2009).Lundgren, B. O. & Kiessling, K. H. Seasonal variation in catabolic enzyme activities in breast muscle of some migratory birds. Oecologia 66, 468–471 (1985).ADS
PubMed
Article
Google Scholar
Banerjee, S. & Chaturvedi, C. M. Migratory preparation associated alterations in pectoralis muscle biochemistry and proteome in Palearctic-Indian emberizid migratory finch, red-headed bunting, Emberiza bruniceps. Comp. Biochem. Physiol. D Genom. Proteom. 17, 9–25 (2016).CAS
Google Scholar
Dick, M. F. The long haul: migratory flight preparation and performance in songbirds. Ph.D. dissertation, University of Western Ontario, London, Canada (2017).Driedzic, W. R., Crowe, H. L., Hicklin, P. W. & Sephton, D. H. Adaptations in pectoralis muscle, heart mass, and energy metabolism during premigratory fattening in semipalmated sandpipers (Calidris pusilla). Can. J. Zool. 71, 1602–1608 (1993).Article
Google Scholar
De Moranville, K. J. et al. PPAR expression, muscle size and metabolic rates across the gray catbird’s annual cycle are greatest in preparation for fall migration. J. Exper. Biol. 222, 198028 (2019).Article
Google Scholar
Zajac, D. M., Cerasale, D. J., Landman, S. & Guglielmo, C. G. Behavioral and physiological effects of photoperiod-induced migratory state and leptin on Zonotrichia albicollis: II. Effects on fatty acid metabolism. Gen. Comp. Endocrinol. 174, 269–275 (2011).CAS
PubMed
Article
Google Scholar
Tinant, G. et al. Methylmercury displays pro-adipogenic properties in rainbow trout preadipocytes. Chemosphere 263, 127917 (2021).ADS
CAS
PubMed
Article
Google Scholar
Cambier, S. et al. At environmental doses, dietary methylmercury inhibits mitochondrial energy metabolism in skeletal muscles of the zebra fish (Danio rerio). Int. J. Biochem. Cell Biol. 41, 791–799 (2009).CAS
PubMed
Article
Google Scholar
Ferain, A. et al. Transcriptional effects of phospholipid fatty acid profile on rainbow trout liver cells exposed to methylmercury. Aquat. Toxicol. 199, 174–187 (2018).CAS
PubMed
Article
Google Scholar
Börchers, T., Højrup, P., Nielsen, S. U., Roepstorff, P., Spener, F., Knudsen, J. Revision of the amino acid sequence of human heart fatty acid-binding protein. In Cellular Fatty Acid-binding Proteins 127–133 (Springer, Boston, 1990).Dörmann, P. et al. Amino acid exchange and covalent modification by cysteine and glutathione explain isoforms of fatty acid-binding protein occurring in bovine liver. J. Biol. Chem. 268, 16286–16292 (1993).PubMed
Article
Google Scholar
Su, X. & Abumrad, N. A. Cellular fatty acid uptake: A pathway under construction. Trends Endocrinol. Metab. 20(2), 72–77 (2009).CAS
PubMed
PubMed Central
Article
Google Scholar
van Oort, M. M. et al. Each of the four intracellular cysteines of CD36 is essential for insulin-or AMP-activated protein kinase-induced CD36 translocation. Arch. Physiol. Biochem. 120, 40–49 (2014).PubMed
Article
CAS
Google Scholar
Wang, G., Bonkovsky, H. L., de Lemos, A. & Burczynski, F. J. Recent insights into the biological functions of liver fatty acid binding protein 1. J. Lipid Res. 56, 2238–2247 (2015).CAS
PubMed
PubMed Central
Article
Google Scholar
Vallee, B. L. & Ulmer, D. D. Biochemical effects of mercury, cadmium, and lead. Annu. Rev. Biochem. 41, 91–128 (1972).CAS
PubMed
Article
Google Scholar
Aschner, M. & Syversen, T. Methylmercury: Recent advances in the understanding of its neurotoxicity. Ther. Drug Monit. 27, 278–283 (2005).PubMed
PubMed Central
Article
Google Scholar
Kenow, K. P., Meyer, M. W., Hines, R. K. & Karasov, W. H. Distribution and accumulation of mercury in tissues of captive-reared common loon (Gavia immer) chicks. Environ. Toxicol. Chem. 26, 1047–1055 (2007).CAS
PubMed
Article
Google Scholar
Varian-Ramos, C. W., Whitney, M., Rice, G. W. & Cristol, D. A. Form of dietary methylmercury does not affect total mercury accumulation in the tissues of zebra finch. Bull. Environ. Contam. Toxicol. 99, 1–8 (2017).CAS
PubMed
Article
Google Scholar
Rizzetti, D. A. et al. Chronic mercury at low doses impairs white adipose tissue plasticity. Toxicology 418, 41–50 (2019).CAS
PubMed
Article
Google Scholar
Richter, C. A. et al. Methylmercury-induced changes in gene transcription associated with neuroendocrine disruption in largemouth bass (Micropterus salmoides). Gen. Comp. Endocrinol. 203, 215–224 (2014).CAS
PubMed
Article
Google Scholar
Barnes, D. M., Hanlon, P. R. & Kircher, E. A. Effects of inorganic HgCl2 on adipogenesis. Toxicol. Sci. 75(2), 368–377 (2003).CAS
PubMed
Article
Google Scholar
Corder, K. R., DeMoranville, K. J., Russell, D. E., Huss, J. M. & Schaeffer, P. J. Annual life-stage regulation of lipid metabolism and storage and association with PPARs in a migrant species: the gray catbird (Dumetella carolinensis). J. Exp. Biol. 219, 3391–3398 (2016).PubMed
Google Scholar
DeMoranville, K. J., Carter, W. A., Pierce, B. J. & McWilliams, S. R. Flight training in a migratory bird drives metabolic gene expression in the flight muscle but not liver, and dietary fat quality influences select genes. Am. J. Physiol.-Regul. Integr. Compar. Physiol. 319(6), R637–R652 (2020).CAS
Article
Google Scholar
Gavrilova, O. et al. Liver peroxisome proliferator-activated receptor γ contributes to hepatic steatosis, triglyceride clearance, and regulation of body fat mass. J. Biol. Chem. 278(36), 34268–34276 (2003).CAS
PubMed
Article
Google Scholar
Bedoucha, M., Atzpodien, E. & Boelsterli, U. A. Diabetic KKAy mice exhibit increased hepatic PPARγ1 gene expression and develop hepatic steatosis upon chronic treatment with antidiabetic thiazolidinediones. J. Hepatol. 35, 17–23 (2001).CAS
PubMed
Article
Google Scholar
Egeler, O., Williams, T. D. & Guglielmo, C. G. Modulation of lipogenic enzymes, fatty acid synthase and Δ 9-desaturase, in relation to migration in the western sandpiper (Calidris mauri). J. Comp. Physiol. B 170, 169–174 (2000).CAS
PubMed
Article
Google Scholar
Klaper, R. et al. Use of a 15k gene microarray to determine gene expression changes in response to acute and chronic methylmercury exposure in the fathead minnow (Pimephales promelas). J. Fish Biol. 72, 2207–2280 (2008).CAS
Article
Google Scholar
Calow, P. Physiological costs of combating chemical toxicants: Ecological implications. Comp. Biochem. Physiol. C 100, 3–6 (1991).CAS
PubMed
Article
Google Scholar
Spalding, M. G. et al. Histologic, neurologic, and immunologic effects of methylmercury in captive great egrets. J. Wildl. Dis. 36, 423–435 (2000).CAS
PubMed
Article
Google Scholar
Carlson, J. R., Cristol, D. & Swaddle, J. P. Dietary mercury exposure causes decreased escape takeoff flight performance and increased molt rate in European starlings (Sturnus vulgaris). Ecotoxicology 23, 1464–1473 (2014).CAS
PubMed
Article
Google Scholar
Faaborg, J. et al. Conserving migratory land birds in the New World: Do we know enough?. Ecol. Appl. 20, 398–418 (2010).PubMed
Article
Google Scholar
Duijns, S. et al. Body condition explains migratory performance of a long-distance migrant. Proc. R. Soc. B https://doi.org/10.1098/rspb.2017.1374 (2017).Article
PubMed
PubMed Central
Google Scholar More