Uptake and effects of polybrominated diphenyl ethers on marine microalgae and invertebrates

Abstract

Polybrominated diphenyl ethers (PBDEs) are brominated flame retardants that have been widely used over the past 30 years. Due to their persistence and lipophilic properties, PBDEs have become ubiquitous in the physical environment and the biota of marine ecosystems. Although the uptake and biological effects of PBDEs such as endocrine disruption and neurotoxicity on mammals and fish are well documented, little is known about their effects on invertebrates. In particular, the parental transfer and transgenerational effects of PBDEs on marine invertebrates remain obscure. Moreover, high levels of hydroxylated- and methoxylated-PBDEs (OH-PBDEs and MeO-PBDEs), which are more potent than PBDEs, have been widely recorded in the marine environment. However, their origin remains controversial. In order to study the uptake and effects of BDE-47 (a predominant PBDE congener) on marine invertebrates, the effects of water exposure to BDE-47 at sub-lethal concentrations on larval growth, development, and settlement of intertidal invertebrates across three phyla (the barnacle Balanus amphitrite, the slipper limpet Crepidula onyx and the serpulid worm Hydroides elegans) were first investigated. The effects of BDE-47 on the attractiveness of biofilms and subsequently on larval settlement preference were also tested. In addition, a systematic study on the effects of BDE-47 life-long dietary exposure, which involved the microalgae Isochrysis galbana as the dietary carrier of BDE-47, on the Darwinian fitness traits (growth, development, and reproduction) of maturing C. onyx and their offspring were determined. Transcriptomic analysis by RNA sequencing of exposed C. onyx was conducted to unravel mechanisms underlying the observed phenotypic changes. Furthermore, the uptake efficiency of BDE-47 and the potential to synthesize OH-PBDEs and MeO-PBDEs from PBDEs through biotransformation were investigated in four microalgae species. The uptake of BDE-47 from water and diet were evidently efficient for both microalgae and invertebrates. Debromination to form BDE-28 occurred in all microalgae species studied, but biotransformation to OH-PBDEs was only found in I. galbana under extremely high concentration, and thus these microalgae were unlikely the sources for OH-PBDEs and MeO-PBDEs in the sea. While water exposure to BDE-47 caused no direct impact on larvae, reduction in bacterial abundance in biofilms with concomitant changes in settlement preference were clearly evident in all three invertebrates. In addition, dietary exposure caused lower juvenile survivorship, delayed maturation of males and reduced oviposition in the parental generation of C. onyx. More drastic transgenerational effects included an increase in percentage of non-viable eggs and malformed embryos in offspring. Furthermore, transcriptomic analysis revealed alterations in expression of genes related to cilia cells, steroid hormone synthesis and embryonic development upon BDE-47 exposure. The adverse effects found in marine invertebrates upon chronic exposure to BDE-47 at environmentally relevant concentrations may lead to alterations of settlement pattern of intertidal invertebrate communities. Overall, this study provided laboratory evidence suggesting that PBDEs may have a significant, long-term impact on marine invertebrate communities, and highlighted the need of further transgenerational studies of toxicants across different life stages in environmental risk assessments.