Complete Reductive Dechlorination of 4-Hydroxy-chlorothalonil by Dehalogenimonas Populations

Environ Sci Technol. 2022 Sep 6;56(17):12237-12246. doi: 10.1021/acs.est.2c02574. Epub 2022 Aug 11.

Abstract

Chlorothalonil (2,4,5,6-tetrachloroisophthalonitrile, TePN) is one of the most widely used fungicides all over the world. Its major environmental transformation product 4-hydroxy-chlorothalonil (4-hydroxy-2,5,6-trichloroisophthalonitrile, 4-OH-TPN) is more persistent, mobile, and toxic and is frequently detected at a higher concentration in various habitats compared to its parent compound TePN. Further microbial transformation of 4-OH-TPN has never been reported. In this study, we demonstrated that 4-OH-TPN underwent complete microbial reductive dehalogenation to 4-hydroxy-isophthalonitrile via 4-hydroxy-dichloroisophthalonitrile and 4-hydroxy-monochloroisophthalonitrile. 16S rRNA gene amplicon sequencing demonstrated that Dehalogenimonas species was enriched from 6% to 17-22% after reductive dechlorination of 77.24 μmol of 4-OH-TPN. Meanwhile, Dehalogenimonas copies increased by one order of magnitude and obtained a yield of 1.78 ± 1.47 × 108 cells per μmol Cl- released (N = 6), indicating that 4-OH-TPN served as the terminal electron acceptor for organohalide respiration of Dehalogenimonas species. A draft genome of Dehalogenimonas species was assembled through metagenomic sequencing, which harbors 30 putative reductive dehalogenase genes. Syntrophobacter, Acetobacterium, and Methanosarcina spp. were found to be the major non-dechlorinating populations in the microbial community, who might play important roles in the reductive dechlorination of 4-OH-TPN by the Dehalogenimonas species. This study first reports that Dehalogenimonas sp. can also respire on the seemingly dead-end product of TePN, paving the way to complete biotransformation of the widely present TePN and broadening the substrate spectrum of Dehalogenimonas sp. to polychlorinated hydroxy-benzonitrile.

Keywords: 4-hydroxy-chlorothalonil; Dehalogenimonas; obligate organohalide-respiring bacteria; organohalide respiration; reductive dechlorination; transformation products.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Biodegradation, Environmental
  • Biotransformation
  • Chloroflexi* / metabolism
  • Nitriles
  • RNA, Ribosomal, 16S / genetics

Substances

  • Nitriles
  • RNA, Ribosomal, 16S
  • tetrachloroisophthalonitrile