Synonymous single nucleotide polymorphism in arsenic (+3) methyltransferase of the Western mosquitofish (Gambusia affinis) and its gene expression among field populations

Daesik Park,Catherine R Propper,Guangning Wang,Matthew C Salanga

doi:10.1007/s10646-021-02376-8

Daesik Park, Catherine R Propper + Show 2 more

Open Access

https://doi.org/10.1007/s10646-021-02376-8

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Abstract

Naturally occurring arsenic is toxic at extremely low concentrations, yet some species persist even in high arsenic environments. We wanted to test if these species show evidence of evolution associated with arsenic exposure. To do this, we compared allelic variation across 872 coding nucleotides of arsenic (+3) methyltransferase (as3mt) and whole fish as3mt gene expression from three field populations of Gambusia affinis, from water sources containing low (1.9 ppb), medium-low (3.3 ppb), and high (15.7 ppb) levels of arsenic. The high arsenic site exceeds the US EPA’s Maximum Contamination Level for drinking water. Medium-low and high populations exhibited homozygosity, and no sequence variation across all animals sampled. Eleven of 24 fish examined (45.8%) in the low arsenic population harbored synonymous single nucleotide polymorphisms (SNPs) in exons 4 and/or 10. SNP presence in the low arsenic population was not associated with differences in as3mt transcript levels compared to fish from the medium-low site, where SNPs were noted; however, as3mt expression in fish from the high arsenic concentration site was significantly lower than the other two sites. Low sequence variation in fish populations from sites with medium-low and high arsenic concentrations suggests greater selective pressure on this allele, while higher variation in the low population suggests a relaxed selection. Our results suggest gene regulation associated with arsenic detoxification may play a more crucial role in influencing responses to arsenic than polymorphic gene sequence. Understanding microevolutionary processes to various contaminants require the evaluation of multiple populations across a wide range of pollution exposures.

Highlights

Rapid evolutionary responses to contaminants occur through both changes in gene sequence and gene expression
In human populations exposed to high arsenic concentrations over many generations, the frequency of protective mutations is often higher than those seen in populations living with lower levels of exposure, and differences in relative urinary production of MMA and DMA is a representative phenotype of Arsenic (+3) methyltransferase (AS3MT) single nucleotide polymorphisms (SNPs) variation and alterations in enzyme methylation activity (Engström et al 2007, 2011; Watanabe and Hirano 2013; Antonelli et al 2014; Apata and Pfeifer 2020)
Because two of our study populations had gene sequences similar to each other and to the zebrafish genome, our results suggest that SNPs identified in the Willow Lake population occurred over the relatively short period since their introduction to this region (Dees 1961; Miller and Lowe 1967) and future studies can investigate whether these differences in as3mt haplotypes provide protection against the toxic effects of arsenic exposure

Summary

Introduction

Rapid evolutionary responses to contaminants occur through both changes in gene sequence and gene expression. As well-known carcinogens, arsenics including inorganic arsenic (iAs), arsenate (iAsV), and arsenite (iAsIII) are widely found in drinking water, food, and other environmental sources. These compounds are involved in various negative impacts on health and welfare in humans and wildlife (Hughes et al 2011; Carlin et al 2016; Minatel et al 2018). Vulnerable animal populations living in arsenic contaminated water face selective pressure to maintain alleles which encode arsenic detoxifying enzymes, such as As3mt, which metabolizes ingested arsenic into lowertoxicity compounds (Zhang et al 2012)

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