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.
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