The “gut feeling” of arsenic contamination

Yong-Guan Zhu, H. T. Wang, G. W. Zhou and X. M. Xue

Institute of Urban Environment, Chinese Academy of Sciences, China

ygzhu@iue.ac.cn

Arsenic is a ubiquitous trace element and adversely affects soil biota and human health. Microorganisms regulate the bioavailability and energy metabolism process of arsenic in the soil ecosystem. Previous studies indicated that the gut microbiome of soil fauna living in a key transient anoxic micro-zone makes a significant contribution to the metabolism and biogeochemical cycles of carbon and nitrogen in the host. Gut microbiome is the extended genotype of the host. So far, the effect of soil contamination on gut bacterial community and arsenic related genes (we term this as the “gut feeling”) of soil fauna remains poorly understood. To investigate the “gut feeling” of soil fauna to arsenic contamination, we choose the earthworms and nematode as the model organisms. Gut microbial community and arsenic biotransformation genes (ABGs) were characterized by using Illumina sequencing of 16S rRNA and high-throughput quantitative PCR, respectively. High Performance Liquid Chromatography-Inductively coupled plasma -mass spectrometry was used to analyze arsenic species. Using four earthworm species (the epigeic Eisenia Andrei, anecic Amynthas hupeiensis, Metaphire californica and M. vulgaris) from soils with low arsenic concentration, we found that both of low arsenic and ecological niches caused shifts in the abundance of ABGs and the community structure of gut microbiota. A microcosm experiment, conducted using the model species E. fetida treated with different arsenic concentrations, demonstrated that arsenic contamination exerted a significant inhibition on the growth and survival of animals. ABGs involved in arsenic redox and efflux were predominant, and those involved in arsenic methylation and demethylation were very low. Moreover, exposure to arsenate (As(V)) led to a substantial alteration of gut microbial community which was dominated by Actinobacteria, Firmicutes, and Proteobacteria at the phylum level. To further determine the influence of microbiota on physiology of soil animals exposed to arsenic, the nematode Caenorhabditis elegans was fed with As(V) and three Escherichia coli strains, E. coli AW3110 (ΔarsRBC), E. coli BL 21</i>,</i> or E. coli BL 21 containing arsM. The results showed that As(V) was not transformed in the gut of C. elegans fed on E. coli AW3110 (ΔarsRBC), part of As(V) was reduced in the gut containing E. coli BL 21, and methylated arsenic species was found in the gut with E. coli BL 21 containing arsM. In addition, As(III) in the gut decreased the broodsize of C. elegans, and methylated arsenic in the gut of C. elegans alleviated the adverse impact of As(III) on the broodsize. Vitellogenin, the precursor of egg yolk phosphoproteins, was induced by increased As(III) concentration in the C. elegans, suggesting that As(III) performed a critical impact on the reproduction of C. elegans. In summary, our study reveals that the earthworm is a reservoir of microbes with the capability of reducing As(V) and extruding As(III) with little methylation of arsenic, and arsenic transformation by gut microbiota in turn impacted the health of their hosts. The “gut feeling” is carried out and regulated by its microbiota.

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