Grape pomace compost harbors organohalide-respiring Dehalogenimonas species with novel reductive dehalogenase genes

Abstract

Organohalide-respiring bacteria have key roles in the natural chlorine cycle; however, most of the current knowledge is based on cultures from contaminated environments. We demonstrate that grape pomace compost without prior exposure to chlorinated solvents harbors a Dehalogenimonas (Dhgm) species capable of using chlorinated ethenes, including the human carcinogen and common groundwater pollutant vinyl chloride (VC) as electron acceptors. Grape pomace microcosms and derived solid-free enrichment cultures were able to dechlorinate trichloroethene (TCE) to less chlorinated daughter products including ethene. 16S rRNA gene amplicon and qPCR analyses revealed a predominance of Dhgm sequences, but Dehalococcoides mccartyi (Dhc) biomarker genes were not detected. The enumeration of Dhgm 16S rRNA genes demonstrated VC-dependent growth, and 6.55±0.64 × 10 cells were measured per μmole of chloride released. Metagenome sequencing enabled the assembly of a Dhgm draft genome, and 52 putative reductive dehalogenase (RDase) genes were identified. Proteomic workflows identified a putative VC RDase with 49 and 56.1% amino acid similarity to the known VC RDases VcrA and BvcA, respectively. A survey of 1,173 groundwater samples collected from 111 chlorinated solvent-contaminated sites in the United States and Australia revealed that Dhgm 16S rRNA genes were frequently detected and outnumbered Dhc in 65% of the samples. Dhgm are likely greater contributors to reductive dechlorination of chlorinated solvents in contaminated aquifers than is currently recognized, and non-polluted environments represent sources of organohalide-respiring bacteria with novel RDase genes.

Hydrochemical Conditions for Aerobic/Anaerobic Biodegradation of Chlorinated Ethenes—A Multi-Site Assessment

“…Frequent detection of Dehalogenimonas spp. in our samples (94%) is consistent with the findings of Yang et al [13], who detected Dehalogenimonas spp. in 81% of 1173 samples collected in the United States and Australia.…”

“…Similarly, VC concentration was positively correlated to the ethenotroph functional genes etnC and etnE and the reductive dehalogenase genes vcrA and bvcA, as well as the reductive dechlorinators D. mccartyi and Dehalogenimonas spp. The positive correlation of cis-1,2-DCE and VC to abundance of Dehalogenimonas spp., whose ability to degrade cis-1,2-DCE and VC was only recently confirmed by Yang et al [13], indicates a potentially notable contribution of Dehalogenimonas spp. in reductive dechlorination at the sites tested.…”

Organohalide respiration in pristine environments: implications for the natural halogen cycle

“…Not found (Krzmarzick et al, 2014) Grape pomace compost Stuttgart, Germany PCE, VC Dehalogenimonas sp. cerA (Yang et al, 2017) tetrachloro-4-methoxyphenol (TCMP, 18) by Desulfitobacterium hafniense strain PCP-1 and mixed microbial communities (Milliken et al, 2004a). TCMP is an environmentally important fungal product from chlorinated hydroquinone metabolites due to its potential physiological role during lignin degradation and has been detected in composite forest litter (De Jong and Field, 1997).…”

Integrative isotopic and molecular approach for the diagnosis and implementation of an efficient in-situ enhanced biological reductive dechlorination of chlorinated ethenes

“…(Dhc) and Dehalogenimonas sp. are the only genera, to date, capable of fully dechlorinating CEs to ETH (Adrian and Löffler, 2016;Yang et al, 2017b). Reductive dehalogenases (rdh) are the key enzymes driving organohalide respiration and can be used as biomarkers to investigate the intrinsic bioremediation potential at polluted sites (Blázquez-Pallí et al, 2019;Dugat-Bony et al, 2012;Hermon et al, 2019;Scheutz et al, 2008).…”