4.7 Article

Gut microbiota promote biotransformation and bioaccumulation of arsenic in tilapia

Journal

ENVIRONMENTAL POLLUTION
Volume 305, Issue -, Pages -

Publisher

ELSEVIER SCI LTD
DOI: 10.1016/j.envpol.2022.119321

Keywords

Arsenic; Fish; Gut microbiota; Biotransformation; Bioaccumulation

Funding

  1. National Natural Science Foundation of China [41922042, 41876133, 41906137]
  2. Key Special Project for Introduced Talents Team of Southern Marine Science and Engineering Guangdong Laboratory-Guangzhou [GML2019ZD0405]
  3. Innovation Academy of South China Sea Ecology and Environmental Engineering, Chinese Academy of Sciences [ISEE2018ZD02]
  4. Science and Technology Plan-ning Project of Guangdong Province, China [2020B1212060058]

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The presence of gut microbiota, especially arsenic-resistant bacteria such as Stenotrophomonas maltophilia, plays an important role in the accumulation and transformation of arsenic in fish. Removing the gut microbiota through antibiotic treatment significantly reduces the levels of total arsenic and arsenobetaine in the intestines and muscles of fish. Arsenic exposure alters the composition of the fish gut microbiota, with S. maltophilia becoming the dominant species. In vitro experiments demonstrated that the gut contents of untreated fish can metabolize arsenate to arsenite and organoarsenicals, while antibiotic-treated fish lose this ability.
Aquatic organisms such as fish can accumulate high levels of arsenic (As) and transform toxic inorganic As (iAs) to non-toxic arsenobetaine (AsB). Whether the gut microbiota are involved in the process of As accumulation and transformation in fish is unclear. Herein, we subjected tilapia (Oreochromis mossambicus) to antibiotic treatment for 19 d to remove the gut microbiota, followed by the dietary exposure to arsenate (As(V)) for 16 d. The antibiotic-treated fish accumulated significantly less total As and AsB levels in the intestine and muscle than the fish in the control group. The gut contents (mixture of microbiota, digestive fluid, and diet debris) in the control fish metabolized As(V) to arsenite (As(III)) and organoarsenicals in vitro, while those in the antibiotic-treated fish lost this ability. As(V) exposure significantly changed the fish gut microbiota community. Stenotrophomonas maltophilia was found to be the dominant species (>60% of total operational taxonomic unit (OTU) number) in the gut microbiota of As-treated fish. The isolated As-resistant strain S. maltophilia SCSIOOM owned a high capability to metabolize As(V) to As(III) and organoarsenicals. Overall, these results demonstrated that the gut microbiota, at least the As-resistant bacteria, were involved in As biotransformation pathways in fish.

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