Arsenic biotransformation in earthworms from contaminated soils

Abstract

Two species of arsenic (As) resistant earthworm, Lumbricus rubellus and Dendrodrillus rubidus, their host soils and soil excretions (casts) were collected from 23 locations at a former As mine in 5 Devon, UK. Total As concentrations, measured by ICP-MS, ranged from 255 to 13,080 mg kg -1 in soils, 11 to 877 mg kg -1 in earthworms and 284 to 4221 mg kg -1 in earthworm casts from a subsample of 10 of the 23 investigated sites. The samples were also measured for As speciation using HPLC-ICP-MS to investigate potential As biotransformation pathways. Inorganic arsenate (As V ) and arsenite (As III ) were the only species detected in the soil. As V and As III were also the dominant 10 species found in the earthworms and cast material together with lower proportions of the organic species methylarsonate (MA V ), dimethylarsinate (DMA V ), arsenobetaine (AB) and three arsenosugars. Whilst the inorganic As content of the earthworms increased with increasing As body burden, the concentration of organic species remained relatively constant. These results suggest that the biotransformation of inorganic arsenic to organic species does not contribute to As 15 resistance in the sampled earthworm populations. Quantification of As speciation in the soil, earthworms and cast material allows a more comprehensive pathway for the formation of AB in earthworms to be elucidated. Received (in XXX, IntroductionThe chemistry of As in environmental and biological systems is complex. Whilst inorganic As species are the most prevalent in abiotic environments, the uptake of inorganic As 25 by living organisms can lead to the synthesis of organic As species 1 through biotransformation. The ubiquitous, epegeic earthworm species L. rubellus and D. rubidus are known to inhabit soils highly contaminated with As at the former mine site of Devon Great Consols (DGC), UK. [2][3][4][5] These earthworms 30 are clearly resistant to As toxicity and several potential coping mechanisms have been proposed, yet the underlying mechanism behind this resistance is unknown. Behavioural adaptation, whereby the earthworm avoids contact with the contaminant, 4 is unlikely as earthworms from DGC are known 35 to have elevated As body burdens. 2,4, 5 The biotransformation of highly toxic inorganic As to the less toxic organic species arsenobetaine (AB) has been speculated as a mode of mitigating As toxicity in DGC earthworms. 2,4 An alternative mechanism involves the sequestration of arsenic in the 40 metallothionein-rich chloragogenous tissue which separates the intestine from the coelomic cavity. 3 With this mechanism it is proposed that inorganic As III binds to the sulphur-rich metallothionein thereby sequestering ingested As in a form that is not biologically reactive. The study of As speciation can provide important information on As biotransformation and toxicity and to date a multitude of organic As species have been identified. 7 The occurrence of organic As species and their biotransformation pathways are well documented in marine organisms such as crus...

Organic Arsenic in the Soil Environment: Speciation, Occurrence, Transformation, and Adsorption Behavior

“…The surprisingly low As concentrations in ants (12 ppm) compared with ant-hill material (5,420 ppm As) hint a specific mechanism for As exclusion (Kuehnelt et al 1997). Earthworms (Lumbricus rubellus and Dendrodrilus rubidus) collected at Devon Great Consols, UK, with different extent of As soil contamination (up to 1.3%) confirmed again the findings of MMAA(V), DMAA (V), and AsB (Watts et al 2008;Button et al 2009). Dimethylarsinoylribosides (glycerol, phosphate, and sulfate) were also identified in earthworms, suggesting probable biotransformation and bioaccumulation of arsenosugars in the soil environments (Geiszinger et al 1998;Geiszinger et al 2002;Watts et al 2008;Button et al 2009).…”

Arsenic speciation in polychaetes (Annelida) and sediments from the intertidal mudflat of Sundarban mangrove wetland, India

“…Extraction efficiency was monitored using the CRM 627 tuna fish tissue (BCR, Brussels). A mean recovery of 108 ± 10% (n = 3, Table 3) of the total arsenic measured in the extract was obtained, comparable with Button et al (2009) 100 ± 6%. Duplicate samples provided a percentage difference of less than 1 %.…”

“…The extraction of arsenic species from the polychaetes followed the method described in Button et al (2009). Homogenized dried polychaete powder (0.25 g) was weighed directly into 50 ml polyethylene centrifuge tubes.…”

“…Marine samples have so far provided the greatest number of naturally occurring arsenic compounds with up to 50 compounds identified (Nischwitz and Pergantis, 2006), although recent work revealed that terrestrial organisms also contain many of these compounds (Geiszinger et al 1998;Kuehnelt et al 1997;Watts et al 2008;Button et al 2009). There are clear patterns of arsenic compounds among marine organisms (Francesconi & Edmonds, 1997).…”

ECOTOXICOLOGICAL BIOASSAYS OF THE EARTHWORMS <i>ALLOLOBOPHORA CALIGINOSA</i> SAVIGNY AND <i>PHERETIMA HAWAYANA</i> ROSA TREATED WITH ARSENATE

“…Heavy metal pollution is the case where the quantities of these elements in soils are higher than the natural environmental concentrations and is potentially harmful to biological life. Arsenic is a metalloid pollutant widelyintroduced into nature and the environment through industrial processes and agricultural practices (Button et al, 2009;2012). Samad et al (2010) ranked arsenic in abundance as 20th in the earth's crust, 14th in seawater and 12th in the human body.…”