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Non-Commercial Use Only Journal of Xenobiotics 2018; volume 8:7820 Behavioral effects of the stage, an idea accepted under the concept of neurotoxin b-N-methylamino- Developmental Origin of Health and Correspondence: Alessandra Carion, Disease (DOHaD).2 However, even if Laboratory of Evolutionary and Adaptive L-alanine on the mangrove experimental and epidemiological studies Physiology, Institute of Life, Earth and rivulus (Kryptolebias support this concept, the mechanisms Environment, University of Namur, 61 Rue de Bruxelles, 5000 Namur, Belgium. explaining long-term delayed effects of marmoratus) larvae E-mail: [email protected] early life NCs exposure remain largely unclear.3 Alessandra Carion, Julie Hétru, Key words: Mangrove rivulus; Nowadays, an increasing number of Developmental origin of health and disease; Angèle Markey, people suffer from neurological disorders Neurotoxin; Behavior; b-N-methylamino-L- Victoria Suarez-Ulloa, Silvestre Frédéric such as Alzheimer’s, Parkinson’s or alanine.alanine. Laboratory of Evolutionary and Amyotrophic lateral sclerosis diseases, Conflict of interest: the authors declare no Adaptive Physiology, Institute of Life, which could be partly related to environ- potential conflict of interest. Earth and Environment, University of mental influences during ELS. Such dis- Namur, Namur, Belgium eases are triggered by a complex interplay Funding: this study was supported by the between genes, ageing, and environmental FRS-FNRS (Fonds de la Recherche conditions plus a random component.4 In Scientifique) PhD fellowship to A. Carion and this context, the need for understanding the a research grant number N°T.0174.14. role played by exposure to NCs has been Abstract growing in importance.5 Of particular inter- Conference presentation: part of this paper was presented at the 2018 EcoBIM meeting, Mangrove rivulus, Kryptolebias mar- est is b-N-methylamino-L-alanine May 22-25, Bordeaux, France. moratus, is a hermaphrodite fish capable of (BMAA), a non-protein amino acid NC pro- self-fertilization. This particularity allows duced by the extremely ubiquitous Received for publication: 6 September 2018. to naturally produce highly homozygous cyanobacteria, dinoflagellates and diatoms.6 Accepted for publication: 17 October 2018. and isogenic individuals. Despite the low Although the first link between BMAA and only genetic diversity, rivulus can live in neurodegenerative diseases was established This work is licensed under a Creative extremely variable environments and adjust more than 50 years ago, evidence of BMAA Commons Attribution NonCommercial 4.0 its phenotype accordingly. This species rep- effects on human brain is still inconclusive License (CC BY-NC 4.0). resents a unique opportunity to clearly dis- 7 and remains controversial. On the other ©Copyright A. Carion et al., 2018 tinguish the genetic and non-genetic factors use hand, considering that BMAA can be found Licensee PAGEPress, Italy implicated in adaptation and evolution, such in aquatic food webs at high Journal of Xenobiotics 2018; 8:7820 as epigenetic mechanisms. It is thus a great concentrations,8 further studies about doi:10.4081/xeno.2018.7820 model in aquatic ecotoxicology to investi- BMAA risk assessment on aquatic organ- gate the effects of xenobiotics on the isms are urgently required. epigenome, and their potential long-term With this aim in mind, the present work impacts. In the present study, we used the are one of the most often cited mechanisms has been developed using a strategic model potentially explaining neuronal disorders mangrove rivulus to investigate the effects organism, the mangrove rivulus fish. 3 b and DOHaD. Effects on the epigenome do of the neurotoxin -N-methylamino-L-ala- Together with its sister species, the man- not involve changes in the DNA sequence nine (BMAA) on larvae behaviors after 7 grove rivulus (Kryptolebias marmoratus) is but can modify gene expression patterns in days exposure to two sub-lethal concentra- the only known vertebrate that naturally a heritable manner through mechanisms tions. Results show that BMAA can affect reproduce by self-fertilization.9 In nature, such as DNA methylation (DNAme), his- the maximal speed and prey capture (trials this Cyprinodontiform oviparous fish is tone modifications, and non-coding RNAs. and failures), suggesting potential impacts characterized by an androdioecious mixed- Together, the emerging fields of neuroepi- on the organism’s fitness. mating reproductive system, in which her- genetics and environmental epigenetics maphrodites coexist with a low proportion Non-commercialof males (between 5 and 25%). While out- show that exposure to environmental NCs crossing with males is known to happen, it can affect the brain epigenome and conse- Introduction is much less frequent than self-fertilization quently lead to impacts on behavior and/or cognitive faculties.11 In this context, the Pollution involving neurotoxic com- of hermaphrodites. Consistent self-fertiliza- rivulus constitutes an optimal model choice pounds (NCs) is one of the emerging issues tion is an extreme form of inbreeding and it for human health but also for wild species consequently naturally produces isogenic to investigate the role of epigenetic mecha- and ecosystems. In wild organisms, the lineages after a few generations.10 nisms in DOHaD and in transgenerational adverse outcome of exposure to NCs is a Additionally, despite its low genetic vari- inheritance via sexual reproduction, while change in behavior, which can affect an ability, the rivulus displays a high level of minimizing the confounding effects of 12,13 individual’s fitness and potentially lead to phenotypic plasticity and it is capable to genetic variation. population decline.1 Moreover, it is well efficiently acclimate to the highly variable The main objective of this study was to established that embryonic development environment of mangrove forests. These determine the immediate effects of BMAA and early life stages (ELS) are periods dur- features have recently put the mangrove exposure during ELS on locomotion and ing which the organism is particularly sen- rivulus in the spotlight of scientific prey capture behaviors in the rivulus. sitive to environmental stress, and conse- research, as it constitutes an innovative and Moreover, this preliminary work paves the quently to NCs exposure. In addition to valuable model for the identification of true ground towards a better understanding of immediate effects on ELS, developmental cause-effect relationships between the envi- the conspicuous consequences that NCs exposure at relatively low dose can lead to ronment, the phenotype and the epigenome. may have for populations of aquatic organ- adverse outcomes later in life, at the adult Impacts of NCs on the brain epigenome isms and their link with molecular mecha- [Journal of Xenobiotics 2018; 8:7820] [page 7] Article nisms, such mechanisms including modifi- Ethovision® software. Afterwards, 10 nau- 1 and Figure 1A), while no effect has been cations of the expression level of some key plii of Artemia were provided in each well observed at the highest concentration. The genes involved in behavior and in nervous to measure larvae prey capture ability dur- prey capture assay revealed significant cells metabolism as well as potential varia- ing 5 min. Results are expressed as the per- effects of BMAA exposure on the percent- tions in epigenetic mechanisms. centage of success and failure, calculated as age of failure in prey capture and on the the proportion between successful capture total trials expressed by larvae to capture or failed capture trials over the total number prey (Figure 1B-C). The 20 µg/L and 15 of trials. mg/L groups respectively expressed a 14% Materials and Methods Agostino and Pearson tests were per- and 17% increases in total trials compared formed to confirm data normality. Rivulus larvae were exposed to 2 doses to group-controls. Moreover, these two Accordingly, one-way ANOVA or non- of BMAA directly after hatching for 7 days: exposure concentrations respectively parametric Kruskal-Wallis tests were 20 µg/L and 15 mg/L, plus a control unex- expressed a 13% and 15% increases in per- applied followed by Dunn’s multiple com- posed group (n = 24). Larvae were fed ad centage of prey capture failure compared to parisons test in order to evaluate an effect of libitum with Artemia salina every day. The controls. BMAA on larvae locomotion, thigmotaxis BMAA working solution was made from L- According to these results, BMAA or capability to capture prey. Percentages of BMAA Hydrochloride powder (Sigma- exposure during development impacts lar- success and failure were arcsine square root Aldrich®) mixed with 25 ppt (± 1) water. vae locomotion and capabilities to behave transformed. Statistical analyses were per- About 2/3 of water was renewed every day. appropriately to efficiently hunt their prey. formed using GraphPad Prism 7 Software. During exposure period, mortality was BMAA appears to mainly disrupt brain Significance level was set at P<0.05. assessed and larvae were individually meas- functions. Larvae maximum velocity was ured at 1, 3, 5 and 7 days post-hatching impacted by BMAA exposure at lowest (dph) using a Nikon Digital Camera USB3 concentration (20 µg/L) while no effect was ½.5 15 IM/SEC mounted on a Nikon evident at higher concentration (15 mg/L). SMZ1270 stereomicroscope and the NIS- Results and Discussion This suggests that an environmentally rele- Elements® program. Larvae locomotion No effect of BMAA exposure was
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