PAH-pollution effects on sensitive and resistant embryos: Integrating structure and function with gene expression

Abstract

Polycyclic aromatic hydrocarbons (PAHs) are among the most widespread natural and anthropogenic pollutants, and some PAHs are proven developmental toxicants. We chemically characterized clean and heavily polluted sites and exposed fish embryos to PAH polluted sediment extracts during four critical developmental stages. Embryos were collected from Fundulus heteroclitus populations inhabiting the clean and heavily polluted Superfund estuary. Embryos of parents from the clean sites are sensitive to PAH pollutants while those of parents from the heavily polluted site are resistant. Chemical analysis of embryos suggests PAH accumulation and pollution-induced toxicity among sensitive embryos during development that ultimately kills all sensitive embryos before hatching, while remarkably, the resistant embryos develop normally. The adverse effects on sensitive embryos are manifested as developmental delays, reduced heart rates, and severe heart, liver, and kidney morphological abnormalities. Gene expression analysis of early somitogenesis, heartbeat initiation, late organogenesis, and pre-hatching developmental stages reveals genes whose expression significantly differs between sensitive and resistant embryo populations and helps to explain mechanisms of sensitivity and resistance to polluted environments during vertebrate animal development.

Cardiac physiology and metabolic gene expression during late organogenesis among F. heteroclitus embryo families from crosses between pollution-sensitive and -resistant parents

“…For example, embryonic exposure to weathered crude oil containing PAHs lead to impaired heart looping, atrioventricular conduction block, and cardiac ventricular conduction. We reported PAH-induced morphological and physiological cardiotoxicity in developing sensitive embryos during four critical developmental stages, while the severity of such effects was not observed in resistant embryo populations [7]. While embryo exposure to a simple PAH mixture results in cardiac deformities [3], exposure to individual PAHs alone at similar concentrations alters heart rates but does not induce morphological deformities [53].…”

“…Can populations evolve and adapt fast enough in response to human-caused strong selective pressures, including environmental pollution? The effects of pollution on populations often include increased mortality, decreased fecundity, and impaired physiological performances, but not all individuals respond the same: some are sensitive, while others adapt and become resistant [3][4][5][6][7][8][9][10][11][12]. Polluted stressful environments result in resource-deficient and energy-deficient phenotypes [13] and individual differences in stress response emerge through various geneenvironment interactions [4,[8][9][10]14].…”

“…Fundulus heteroclitus is one of the few studied species in North America that has shown resistance to pollutants among both adults and embryos: while sediment extracts from such environments can be lethal to F. heteroclitus embryos from clean sites, embryos of parents from polluted sites are remarkably resistant [3,7,[37][38][39][40][41][42]. Rapidly evolved tolerance phenotypes to environmental toxicants [11,12,43] have evolved independently multiple times [10,11,44], and each independent population can be associated with site-specific primary pollutants [5,7,8,11,20,34].…”

“…Fundulus heteroclitus is one of the few studied species in North America that has shown resistance to pollutants among both adults and embryos: while sediment extracts from such environments can be lethal to F. heteroclitus embryos from clean sites, embryos of parents from polluted sites are remarkably resistant [3,7,[37][38][39][40][41][42]. Rapidly evolved tolerance phenotypes to environmental toxicants [11,12,43] have evolved independently multiple times [10,11,44], and each independent population can be associated with site-specific primary pollutants [5,7,8,11,20,34]. While much is known about the molecular mechanisms of action for the major chemical pollutants to which they have adapted and about their transcriptome-wide response to relevant chemical toxicants [3][4][5][6][8][9][10], less is known about functionally important variation in gene expression underlying resistant phenotypes and signatures of adaptive divergence within and between populations.…”

Development of gold(i) phosphorescent tweezers for sensing applications

“…34 It has been demonstrated that these pollutants alter specific and non-specific immunities in fish and mammals 35 and can also affect pregnant women, developing health issues in the embryo. 36 On the other hand, PFCs show very stable carbon–fluoride bonds and so their degradation under environmental conditions does not occur easily. 37 Humans are obviously exposed to these pollutants, absorbing them through dermal, ingestion or inhalation pathways.…”